1. bookVolume 72 (2021): Edition 2 (June 2021)
Détails du magazine
License
Format
Magazine
eISSN
2719-5430
Première parution
30 Mar 2016
Périodicité
4 fois par an
Langues
Anglais
access type Accès libre

Modulation of the endosomal pathway for optimized response to drought stress: from model to crop plants

Publié en ligne: 09 May 2022
Volume & Edition: Volume 72 (2021) - Edition 2 (June 2021)
Pages: 57 - 72
Reçu: 12 May 2021
Accepté: 16 Jun 2021
Détails du magazine
License
Format
Magazine
eISSN
2719-5430
Première parution
30 Mar 2016
Périodicité
4 fois par an
Langues
Anglais
Abstract

The current climate situation potentiates the need for distinctive crops which have to be high yielding and resilient to abiotic and biotic stresses, particularly to drought stress. Responses to stresses are regulated and coordinated by phytohormones, whose transport and perception are commonly centered around plasma membrane (PM)-localized proteins. Localization and abundance of these are organized by endosomal trafficking, whereby the post-translational modification of PM proteins with the small protein ubiquitin is key in signaling their endocytosis and degradation. This review focuses on the endosomal degradation pathway in plants with a special focus on a protein family termed TARGET OF MYB1 (TOM1)-LIKE (TOLs), responsible for initiating sorting of ubiquitinated proteins destined for degradation. TOLs, albeit having apparent redundancies, play a role in very specific pathways where they may be relevant for fine-tuning of plant hormone signaling by means of tightly controlled protein turnover. Understanding the function of TOLs could give key insights into the mechanisms by which plants define the trade-off between stress tolerance and plant development when faced with challenging environments. Findings obtained in the model plant Arabidopsis thaliana provide a solid foundation for translational research aimed at breeding more tolerant crops.

Keywords

Schlagwörter

Introduction

Plants, as sessile organisms, persistently encounter diverse biotic and abiotic stresses that can adversely impact on their growth and thus severely impair crop production. One of the main objectives in agriculture is therefore to obtain high-yielding plants, resilient not only to diseases but also to increasingly higher temperature (Kim et al., 2021). From basic research in the model plant Arabidopsis thaliana, we have gained unparalleled insights into molecular circuits underlying essential processes in how plants manage to fine-tune their responses and adapt to their environment. It thus provides a solid foundation for translational research aimed at breeding more tolerant crops.

At a cellular-molecular level, plants have evolved a plethora of mechanisms to be able to respond quickly and accurately to their ever-changing, often stressful environment. The plasma membrane (PM), acting as an interface between the extracellular surroundings and cellular constituents, is densely packed with an array of proteins involved in the sensing and transmitting of stimuli essential for adaptive responses. The transport and perception of, for example, plant hormones, which are indispensable for plant development, are centered around PM-localized proteins. Thus, their localization and abundance need to be tightly regulated and understanding this regulation is of exceptional interest. It is therefore not surprising that several regulatory pathways participate in the control of PM proteins, underlining the key functions for the spatiotemporal control of PM protein turnover in plant development and various adaptive growth responses (Korbei and Luschnig, 2013; Luschnig and Vert, 2014).

The plant endosomal system

In eukaryotes, protein homeostasis at membranes is modulated by the endomembrane network. This intricate system of internal membranes provides spatial organization for cell activities by compartmentalizing processes and functions in transporting proteins to their site of action. Vesicular transport and membrane trafficking are pivotal for higher plants, as they not only maintain the functions of organelles and cells, but are also required for fast and dynamic reactions to fluctuating inputs and stimuli (Inada and Ueda, 2014). The plant endosomal system is responsible for the transport of endocytic and biosynthetic cargo, and therefore contributes to the regulation of the protein composition of the PM, the trans-Golgi network (TGN), which in plants coincides with early endosomes (EEs) (Dettmer et al., 2006), lytic and protein storage vacuoles, as well as the cell wall. At the TGN/EE, two major trafficking pathways meet: the endocytic pathway, which represents a set of trafficking routes with cargo sorting, recycling, and degradative functions, and the secretory pathway, which exports proteins from the ER via the Golgi apparatus to the TGN/EE (Robinson et al., 2008; Viotti et al., 2010; Paez Valencia et al., 2016).

Endocytosis

Through endocytosis, which can be either dependent on the scaffolding protein clathrin (clathrin-mediated endocytosis [CME]) or independent of it, cells internalize PM-localized proteins, lipids, and extracellular material (Robinson, 2015; Sandvig et al., 2018). CME was first demonstrated in plants only quite recently (Dhonukshe et al., 2007), and extensive descriptions of the events that encompass CME are often times still based on elaborate studies in animal and yeast systems (reviewed in McMahon and Boucrot, 2011). The clathrin coat self-assembles into units composed of three clathrin heavy chains and three clathrin light chains that oligomerize together to form three-legged structures called triskelia (Chen et al., 2011; Robinson, 2015).

PM proteins in plant cells are primarily internalized by CME, which can be divided into five successive steps: nucleation, cargo selection, clathrin coat assembly, membrane scission, and uncoating (McMahon and Boucrot, 2011). In plants, CME first manifests in the bending of the PM toward the cytoplasm into a clathrin-coated pit. As clathrin does not interact directly with the membranes or cargos, the formation of these clathrin-coated pits is initiated by the recruitment of adaptor and accessory proteins to the proximity of the membrane. These hetero-tetrameric adaptor protein complexes, like the adaptor protein 2 (AP-2) complex and the plant-specific TPLATE complex (Zhang et al., 2015; Reynolds et al., 2018), as well as monomeric adaptor proteins interact with the membrane lipids and sorting motifs in cargo proteins as well as clathrin and assist in guiding them from the cytoplasm to nucleation sites. Adaptors are thus key to the formation of transport vesicles and to selection of cargo for incorporation into vesicles (Cocucci et al., 2012; Arora and Van Damme, 2021).

The clathrin-coated pits eventually mature and bud off to form clathrin-coated vesicles (CCVs). After budding from the PM, the clathrin coat is shed, allowing for recycling of its monomeric constituents in further rounds of endocytosis. In mammals and yeast, this happens directly following scission from the membrane, whereas the coat of plant CCVs appears to be retained and the components are only gradually discarded on route to the TGN/EEs (Narasimhan et al., 2020). The removal of the clathrin coat frees the vesicles for fusion with TGN/EE, the site where the decision for further sorting, either recycling back to the PM or to the vacuole for degradation, takes place (Chen et al., 2011; Reynolds et al., 2018; Rodriguez-Furlan et al., 2019).

Cargo selection

To actively regulate the abundance of proteins at the PM, they need to be recognized by components of the CME machinery, specifically by adaptors. These distinguish the proteins to be internalized by motifs found in the cytosolic domains of such prospective cargo. Sorting motifs can be present in the protein sequence (intrinsic motifs) or can occur through covalently linked specific post-translational modifications like phosphorylation or ubiquitination. Importantly, several distinct sorting signals in the same cargo protein can participate in cargo recognition, adding some flexibility to subsequent sorting events (Traub, 2009; Traub and Bonifacino, 2013; Arora and Van Damme, 2021).

Linear sorting motifs found in the cytosolic domain of the proteins, like the di-leucine- and the tyrosine (YXXΦ)-based sorting motif (where Y is tyrosine, X is any amino acid, and Φ is a bulky hydrophobic residue), have also been identified in plant PM proteins (Arora and Van Damme, 2021). Nevertheless, only the tyrosine motifs have so far been linked to endocytic sorting from the PM (Geldner and Robatzek, 2008), where they were found to be important for the internalization of several PM proteins like the pin-formed (PIN) auxin efflux facilitators (Kleine-Vehn et al., 2011; Sancho-Andres et al., 2016), the brassinosteroid hormone receptor brassinosteroid insensitive 1 (BRI1) (Liu et al., 2020), the tomato pathogen-related receptor-like protein Lycopersicon esculentum ethylene-inducing xylanase receptor (LeEIX2) (Ron and Avni, 2004), and the borate exporter boron transporter 1 (BOR1) (Takano et al., 2010). Protein phosphorylation is a dynamic post-translational modification, which has a central regulatory function in the endocytosis of PM proteins in plants, albeit frequently coupled to and in combination with protein ubiquitination (Bonifacino and Traub, 2003; Traub and Bonifacino, 2013). A very elegant mechanism combining these two modifications was recently demonstrated for the PM-localized IRON-REGULATED TRANSPORTER 1 (IRT1), where phosphorylation is triggered by direct metal binding to a histidine-rich stretch in the cytosolic domain of the transporter. This in turn facilitates recruitment of the IRT1 DEGRADATION FACTOR1 E3 ubiquitin ligase IDF1, allowing for the conclusion that protein phosphorylation seems to be a prior requirement for ubiquitination and both are needed for efficient endosomal sorting of IRT1 (Dubeaux et al., 2018).

The best documented post-translational modification for endocytosis of PM proteins in plants is ubiquitination. This reversible protein modification serves as a signal triggering endocytosis and consequent sorting for degradation, and thus plays a key role in directing the entry of PM proteins into the endosomal system (Clague et al., 2012; Piper et al., 2014; Dubeaux and Vert, 2017). Protein ubiquitination is catalyzed by a series of highly conserved enzymes: ubiquitin activating enzymes (E1), ubiquitin conjugating enzymes (E2), and ubiquitin ligases (E3), resulting in the formation of an isopeptide bond between the C-terminus of ubiquitin and the free amine of a lysine residue on the target protein (Vierstra, 2012; Callis, 2014; Piper et al., 2014). Ubiquitin conjugation is extraordinarily complex in plants, exemplified by more than 1500 E3 ubiquitin ligases, found in the model plant Arabidopsis, which confer target specificity for ubiquitination (Hua and Vierstra, 2011). Furthermore, different E3 ubiquitin ligases can target the same substrates, likely essential for the fine-tuning of protein function, as well as the same E3 ubiquitin ligase can ubiquitinate different proteins (Bueso et al., 2014; Irigoyen et al., 2014; Zhao et al., 2017; Fernandez et al., 2020)

Target proteins can be monoubiquitinated or poly-monoubiquitinated, where individual ubiquitin molecules are conjugated to cargo proteins or additional ubiquitin molecules are linked to an already attached ubiquitin to form chains. Different types of such polyubiquitin chains can form, depending on which lysine residues of the ubiquitin molecule are conjugated (Husnjak and Dikic, 2012). Two common forms are K48- and K63-linked ubiquitin chains, where the E2/E3 pairing determines substrate specificity and the type of chain linkage, although the same E3 may form different linkage types together with different E2s (Tomanov et al., 2014; Stewart et al., 2016). Ubiquitin binding domain (UBD)-containing proteins, which noncovalently associate with ubiquitin, are responsible for the decoding and translation of the ubiquitination code (Husnjak and Dikic, 2012). These ubiquitin receptors typically contain short amino acid stretches, lacking a strict consensus sequence, that display a low binding affinity toward ubiquitin (Husnjak and Dikic, 2012). Importantly, protein ubiquitination is a reversible process with de-ubiquitinating enzymes remodeling the ubiquitin code, contributing to the highly dynamic and reversible characteristics of endocytic trafficking decisions (Isono and Nagel, 2014). Ubiquitination of PM proteins, especially the addition of K63-linked polyubiquitin chains, serves as a signal for endocytosis and further sorting to the vacuole (Husnjak and Dikic, 2012; Romero-Barrios and Vert, 2018). This was shown for several different PM proteins like the iron transporter IRT1 (Dubeaux et al., 2018), the abscisic acid (ABA) receptors PYL4 and PYR1 (Bueso et al., 2014), and the auxin efflux facilitator PIN2 (Leitner et al., 2012b) as well as the brassinosteroid receptor BRI1 (Di Rubbo et al., 2013; Martins et al., 2015). Endocytic vesicles co-localize with K63-linked polyubiquitinated cargo (Johnson and Vert, 2016), and the molecular mechanisms driving endocytosis of such cargos are essentially conserved in plants. Nevertheless, some key players involved in this process appear plant-specific (Dubeaux and Vert, 2017; Gao et al., 2017; Schwihla and Korbei, 2020).

Recycling

After internalization from the cell surface, endocytosed vesicles deliver their content via fusion to the TGN/EE and the cargo proteins can either be recycled back to the PM or be further sorted to multi-vesicular bodies (MVBs) and on to the vacuole for degradation (Paez Valencia et al., 2016). The recycling machinery includes small GTPases and their regulators as well as the retromer complex, while the Endosomal Sorting Complex Required for Transport (ESCRT) machinery is in charge of sorting PM proteins to their degradation (Buono et al., 2017; Isono and Kalinowska, 2017; Rodriguez-Furlan et al., 2019). PM proteins can be recycled back to the PM by being actively diverted from the default vacuolar degradation pathway at the TGN/EE. Plants do not seem to have endosomes dedicated specifically to a recycling pathway, but this rather involves components of the TGN/EE and potentially early stages of the MVBs (Robinson and Neuhaus, 2016).

Degradative sorting

Proteins destined for degradation are not recycled back to the PM, but internalized into the intraluminal vesicles (ILVs) of the MVBs (Otegui, 2018). The signal that marks PM proteins for degradation is ubiquitination, and the ESCRT machinery is thought to exclusively capture ubiquitinated membrane cargoes and sort them into ILVs of MVBs (Shields and Piper, 2011; Dubeaux and Vert, 2017). MVBs originate from the TGN/EE in a process that requires the ESCRT machinery for ILV formation and annexins for releasing MVBs to fuse with the vacuole, whereupon ILVs and their cargo is degraded (Paez Valencia et al., 2016; Isono and Kalinowska, 2017; Cui et al., 2018; Figure 1).

Figure 1

The endosomal protein degradation system of plants. Continuous endocytosis from the PM to the TGN/EE occurs. PM protein monoubiquitination promotes endocytosis and K63-linked polyubiquitination promotes further transport to the vacuole via the concatenated ILVs of MVBs. This step involves ESCRT components. TOLs and SH3P2 fulfill ubiquitin-recognizing functions at the PM, possibly guiding K63-linked ubiquitinated cargo to the endosomal membrane and interacting with/recruiting ESCRT-I subunits. At the endosomal membrane, FYVE1/FREE1 and ALIX show interaction with ubiquitin. This reveals a complex network of several possible ubiquitin receptors in the ESCRT-mediated degradation pathway.

Abbildung 1. Das endosomale Proteinabbausystem von Pflanzen. Kontinuierliche Endozytose erfolgt von der PM zum TGN/EE. Mono-ubiquitinierung von PM-Proteinen fördert die Endozytose und K63-verknüpfte Poly-ubiquitinierung den Weitertransport in die Vakuole über die „concatenated ILVs” der MVBs. An diesem Schritt sind ESCRT-Komponenten beteiligt. TOLs und SH3P2 fungieren als Ubiquitin-rezeptoren an der PM und leiten -gemeinsam mit ESCRT-I Untereinheiten- K63-verknüpfte ubiquitinierte Proteine zur endosomalen Membran. An der endosomalen Membran interagieren FYVE1/FREE1 und ALIX mit Ubiquitin und fungieren somit als zusätzliche Ubiquitinrezeptoren im endosomalen Transport und Abbau von PM-Proteinen.

ESCRT machinery

The ESCRT machinery is a conserved, multi-subunit membrane remodeling complex. It functions in the formation of membrane invaginations, which bud away from the cytoplasm, followed by scission. This stepwise process, performed by protein complexes termed ESCRT-0 to ESCRT-III and accessory components, acts in the recognition, concentration, and sequestering of cargo into the ILVs of MVBs and membrane-deforming events (Henne et al., 2011; Paez Valencia et al., 2016; Gao et al., 2017; Isono and Kalinowska, 2017).

The ESCRT-0 complex is required for the initial targeting and concentration of ubiquitinated cargo and further recruits ESCRT-I, to which it passes on the cargo (Hurley, 2010). The ESCRT-I then recruits the ESCRT-II to the endosomes and the presence of both complexes induces invagination of the limiting membrane toward the endosomal lumen (Hurley and Hanson, 2010). ESCRT-I and -II complexes might also act in parallel to cluster ubiquitinated cargo for internalization (Hurley, 2008; Hurley and Ren, 2009). ESCRT-II then recruits and possibly activates the ESCRT-III complex, which consists of small soluble subunits that assemble into higher-ordered multimers on endosomal membranes (Teo et al., 2004). Once the ESCRTs are assembled, the ubiquitin molecule is removed from the cargo proteins by deubiquitinating enzymes, while an AAA ATPase recycles ESCRT-III back into its monomeric form (Babst et al., 1998). The recruitment and activity of the AAA ATPase is mediated by ESCRT-III–related proteins (Gatta and Carlton, 2019).

In yeast/mammals, the ESCRT-0 complex is made up of two subunits and found at the EEs and the PM (Raiborg and Stenmark, 2009; Henne et al., 2011), where it appears to preassemble with cargoes to enhance the sorting efficiency without affecting vesicle formation per se (Mayers et al., 2013). The ESCRT-0 associates preferentially with K63-linked ubiquitin chains (Nathan et al., 2013), and some subunits can recruit deubiquitinating enzymes, permitting for adjustments in cargo ubiquitination, which enforces the decision if the cargo is to be recycled or degraded (Raiborg and Stenmark, 2009). While the other ESCRT machinery complexes are ubiquitous in eukaryotes and presumably ancient in origin, the ESCRT-0 might represent a more recent addition, not found in plant genomes. The TOM1 protein family represents a family of proteins sharing the same tandem array of domains, the VHS (Vps27/Hrs/Stam) and GAT domains as the ESCRT-0 (Winter and Hauser, 2006; Mosesso et al., 2019). Furthermore, it functions either in parallel, as in mammals (Wang et al., 2010), or alternatively, as in amoeba (Blanc et al., 2009), to the ESCRT-0 complex. TOM1L1 has also been proposed to package ubiquitinated PM proteins into CCVs (Liu et al., 2009). TOM1 is widely conserved in eukaryotes, and from its phylogenetic distribution, it is likely to have been either replaced or perhaps supplemented by the ESCRT-0 in opisthokonts (Herman et al., 2011). As plants do not have canonical ESCRT-0 components, they rely on other proteins to initially recognize ubiquitinated cargo at the PM (Mosesso et al., 2019). Potential candidates that substitute for this complex are from the conserved target of myb1 (TOM1)-like (TOL) protein family (Winter and Hauser, 2006; Schwihla and Korbei, 2020).

The A. thaliana TOL protein family has a domain organization similar to the ESCRT-0 and consists of nine proteins (TOL1–9), several of which have been demonstrated to be essential for vacuolar targeting and subsequent degradation of ubiquitinated PM proteins (Korbei et al., 2013; Moulinier-Anzola et al., 2020; Figure 1). TOLs bind ubiquitin with a preference toward K63-linked ubiquitin chains and participate in the early endocytic trafficking of membrane(-associated) proteins destined for degradation (Moulinier-Anzola et al., 2020), such as the auxin efflux facilitator PIN2, the syntaxin KNOLLE (Korbei et al., 2013), and the borate transporter BOR1 (Yoshinari et al., 2018). A higher-order quintuple tol mutant plant line has a severe and pleiotropic phenotype involving not only mislocalization of specific PM proteins (Korbei et al., 2013), but also a general defect in the degradation of ubiquitinated proteins (Moulinier-Anzola et al., 2020). TOL proteins function as ubiquitin receptors in the initial steps of the ESCRT pathway as they interact with the ESCRTI component VACUOLAR PROTEIN SORTING 23A (VPS23A), thus connecting the TOLs to the ESCRT machinery (Moulinier-Anzola et al., 2020). Function and localization of TOL6 are influenced by ubiquitination, which could assist in the fine-tuning of the interplay between protein recycling and downregulation (Moulinier-Anzola et al., 2020). TOLs can therefore be considered as a plant-specific substitute of ESCRT-0, functioning as multivalent ubiquitin-binding complexes and promoting cargo delivery to the vacuole (Sauer and Friml, 2014; Mosesso et al., 2019; Schwihla and Korbei, 2020).

The ESCRT-I complex, which in yeast/mammals forms a hetero-tetrameric complex containing one copy of each of the subunits (Schuh and Audhya, 2014), is responsible for binding ubiquitinated cargo and ESCRT-0 subunits (Bache et al., 2003). Arabidopsis contains two isoforms of each of the subunits VPS23 (ELC/VPS23A and VPS23B), VPS28 (VPS28-1 and VPS28-2), and VPS37 (VPS37-1 and VPS37-2), but no Mvb12-like protein (Winter and Hauser, 2006; Leung et al., 2008). Arabidopsis VPS23A, which participates in cell division and trichome development, is able to bind to ubiquitin and associate with VPS37 and VPS28 to form a putatively intact plant ESCRT-I complex (Spitzer et al., 2006).

The ESCRT-II, which has a pivotal role in linking the upstream ubiquitin-binding ESCRT complexes to the downstream ESCRT-III complex, is a Y-shaped heteromer of the subunits Vps22, Vps25, and Vps36 (Hurley, 2010). In A. thaliana, all ESCRT-II subunits are present as single-copy genes (Winter and Hauser, 2006; Leung et al., 2008; Richardson et al., 2011). The rice OsVPS22 gene encodes a functional VPS22 homolog, where vps22 mutants exhibit seedling lethality. Nevertheless, potential defects in endosomal sorting remain to be determined (Zhang et al., 2013). VPS36, which may form a putative ESCRT-II complex together with VPS22 and VPS25, is critical for embryo and seedling development and regulates vacuole biogenesis as well as endosomal sorting to the vacuole of several PM proteins (Wang et al., 2017).

ESCRT-III does not contain any known UBDs, and thus is unlikely to recognize ubiquitinated cargoes. Instead, ESCRT-III is essential for membrane scission during sorting of the endocytic cargo into ILVs (Henne et al., 2012). In contrast to the models proposed for animal systems, plant ILVs were shown to form networks of concatenated vesicles instead of individual vesicles in the lumen of the MVB. These networks remain connected by narrow bridges, thus trapping the cargo. The potential role of the ESCRT-III is to act as a diffusion barrier to prevent escape of the cargos destined for degradation (Buono et al., 2017). Consistent with this key function, overexpression of dominant negative alleles of ESCRT-III core subunits results in defects in MVB biogenesis and vacuolar degradation of PM proteins (Cai et al., 2014). Ultimately VPS4/SKD1, an ortholog of yeast/mammalian AAA ATPase, hydrolyzes ATP, leading to the disassembly of the ESCRT-III complex, allowing for recycling of the subunits. This is an essential step for the completion of the membrane scission and the formation of ILVs and, furthermore, for the MVBs to fuse with the vacuole/lysosomes (Hurley, 2010; Schuh and Audhya, 2014). All core subunits of the conserved ESCRT-III machinery have two homologs in Arabidopsis, with the exception of VPS2, which has three (Winter and Hauser, 2006; Cai et al., 2014). Nevertheless, only VPS2.1, which binds deubiquitinating enzymes, appears to function as a typical ESCRT-III subunit (Katsiarimpa et al., 2011). There is only one Arabidopsis VPS4/SKD1 homolog named SKD1 (Haas et al., 2007).

A further protein interacting with the ESCRT-III is ALIX, which also interacts with ESCRT-I subunits, therefore having the potential to link ESCRT-I and ESCRT-III (Bissig and Gruenberg, 2014). ALIX binds ubiquitin, specifically K63-linked ubiquitin chains (Dowlatshahi et al., 2012), suggesting it may function as a ubiquitin receptor for protein sorting into MVBs (Pashkova et al., 2013). Similar functions have been attributed to Arabidopsis ALIX (Figure 1), which furthermore is indispensable for plant growth and development as well as vacuole and MVB biogenesis (Cardona-Lopez et al., 2015; Kalinowska et al., 2015).

Plant genomes encode unique ESCRT components with limited sequence similarities to mammalian/yeast subunits, which interact with known ESCRT subunits to regulate endocytic sorting processes. The SH3 DOMAIN-CONTAINING PROTEIN 2 (SH3P2; Figure 1) has been implicated in vacuolar trafficking of ubiquitinated cargoes as it localizes to CCVs and binds K63-linked ubiquitin chains, VPS23A, and deubiquitinating enzymes (Kolb et al., 2015; Nagel et al., 2017). FYVE 1 (Fab 1, YOTB, Vac 1, and EEA1)/FREE1 (FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1) localizes to MVBs and binds ubiquitin, interacts with SH3P2, both VPS23 subunits, and is incorporated into the ESCRT-III complex (Barberon et al., 2014; Gao et al., 2014; Kolb et al., 2015; Belda-Palazon et al., 2016; Figure 1). It is essential for ILV formation, vacuolar biogenesis, autophagic degradation, seedling development, and localization and degradation of PM proteins and cytosolic ABA receptors (Barberon et al., 2014; Gao et al., 2014; Kolb et al., 2015; Belda-Palazon et al., 2016).

The high number of plant-specific factors, next to the conserved canonical trafficking machinery responsible for transporting PM proteins destined for degradation, reflects the need of plants to precisely adjust the abundance of their PM proteins in order to be able to respond quickly and accurately to their surroundings. Furthermore, some ESCRT subunits, as, for example, the TOL proteins, have undergone drastic gene expansions (Gao et al., 2017; Cui et al., 2018; Mosesso et al., 2019; Vietri et al., 2020). Thus, to fully understand plant adaptation mechanisms, deciphering the molecular mechanisms underlying the regulation of ESCRT-dependent degradation of ubiquitinated PM proteins is crucial.

While it is evident that the ESCRT machinery participates in virtually every aspect of plant growth and development, its contribution to mediating adaptive responses to environmental stimuli appears remarkable. Specifically, a variety of loci associated with ESCRT-mediated sorting have been linked to often times highly defined aspects of higher plants’ responses to biotic as well as abiotic stress conditions. Prominent examples are the ESCRT-I subunits, where a double mutant line (vps28-2 vps37-1) displays reduced endosomal sorting of a pathogen-related receptor. This plant line thus shows impaired immune responses against bacterial pathogens, although its development is otherwise normal, suggesting functional redundancy with the other isoforms (Spallek et al., 2013). Apart from that, a Zea mays ortholog of the AAA ATPase SKD1 is not essential for plant survival, but was demonstrated to be upregulated by salt or drought stress (Xia et al., 2013), and appears to be critical for adequate responses to both biotic and abiotic stresses (Wang et al., 2014, 2015). Recently, several components of the ESCRT machinery have been shown to play a critical role in the ABA signaling pathway, which is also reflected in a higher drought tolerance of their respective loss-of-function mutants (Belda-Palazon et al., 2016; Yu et al., 2016; Garcia-Leon et al., 2019). The ESCRT-I subunit VPS23A, for example, influences the stability and subcellular localization of ABA receptors by affecting their endosomal trafficking to the vacuole for degradation (Yu et al., 2016). Thus, the core function of the ESCRT machinery is essential in plant development, but diversification and redundancies within the subunits might contribute to and play an important role in adaptation processes.

Drought stress

Among the abiotic and biotic stressors, drought conditions receive particular attention as one of the most important factors that limit crop production on a global scale (Gupta et al., 2020). Drought stress restricts many aspects of plant growth and development from plant height to root morphogenesis (Gray and Brady, 2016). Thus, water represents a limiting factor for crop production in agriculture, aggravated further by current signs of climate change, which represents a serious threat for a sustainable supply with staple food (Nuccio et al., 2018; Osmolovskaya et al., 2018; Bertolino et al., 2019). Plants in their natural environment have evolved strategies to cope with limited water supply, which is reflected in a spectrum of mechanisms resulting in an increased tolerance to drought. A plant's approach to cope with such limitations involves either drought escape, which allows plants to complete their life cycle before the onset of drought, drought avoidance, antagonizing enhanced water loss, or drought tolerance characterized by (oftentimes long-term) osmotic adjustments (Zhang, 2007; Osmolovskaya et al., 2018; VanWallendael et al., 2019). However, water shortage beyond a critical threshold level will inevitably result in irreversible tissue damage together with major effects on photosynthesis, respiration, and nutrient uptake (Zhu, 2002; Osmolovskaya et al., 2018). These effects are linked to drought-related aberrations in stomata function, interfering with gas exchange, thus leading to dramatic consequences for crop plants (Zhu, 2002; Bertolino et al., 2019).

Plants carefully protect their cells from dehydration, coordinated by the phytohormone ABA, which rapidly accumulates in plants in response to drought/dehydration stress. This is accomplished by an array of ABA-mediated responses, such as stomatal closure to limit water loss and the production of protective metabolites (Yamaguchi-Shinozaki and Shinozaki, 2006; Gomez-Cadenas et al., 2015). Apart from that, ABA influences adaptive growth responses, including the control of seed germination as well as overall plant organ growth (Cutler et al., 2010; Finkelstein, 2013; Nakashima and Yamaguchi-Shinozaki, 2013). These latter ABA responses impact on plant morphogenesis as a result of an intimate interplay with responses triggered by additional growth regulators. Auxin, for example, is indispensable for root morphogenesis and functions as a key regulator of root system architecture (Lavenus et al., 2013). Ongoing research, unraveling the mechanisms of ABA–auxin crosstalk in the regulation of root growth, thus produces essential insights into the interplay between stress responses and morphogenetic signaling events and how they jointly control adaptive responses (Xie et al., 2021).

TOLs function in the modulation of hormonal pathways

Members of the TOL protein family function in the first steps in the ESCRT-mediated degradation of ubiquitinated PM-associated proteins (Korbei et al., 2013; Moulinier-Anzola et al., 2020). Nevertheless, the precise function of the individual TOLs in this enlarged protein family is not yet described. There are apparent functional redundancies within members of the TOL family, as Arabidopsis single knockout plant lines show no obvious phenotype, while a higher-order mutant exhibits severe pleiotropic defects (Korbei et al., 2013). These severe developmental aberrations could be associated with defects in the recognition and further endocytic sorting for degradation of ubiquitinated membrane cargo, underlining the central role of TOLs in the regulation of plant morphogenesis (Korbei et al., 2013). Phytohormones require stringent modulation of their signaling at transcriptional, translational, and post-translational levels. Intercellular hormone transport and perception is centered around PM-localized proteins, the abundance and localization of which define the magnitude of hormonal responses (Benjamins and Scheres, 2008; Cutler et al., 2010). Protein ubiquitination and the consequential endocytic sorting play a fundamental role in controlling the function of regulators of phytohormone signaling components to adjust and eventually cease pathways (Luschnig and Vert, 2014; Yu and Xie, 2017).

PIN2, an intrinsic PM protein required for directional cellular efflux of the phytohormone auxin, represents an excellent example for such regulation (Gallei et al., 2020; Konstantinova et al., 2021). This protein is modified by K63-linked ubiquitin chains in dependence of RING DOMAIN LIGASE (RGLG)-type E3 ubiquitin ligases, as such ubiquitination acts as a principal signal for PIN2 endocytosis (Leitner et al., 2012a, 2012b). This is underlined by the expression analyses of mutant pin2 alleles, in which a constitutively ubiquitinated PIN2 was found to be endocytosed and degraded in the vacuole, whereas a ubiquitination-deficient pin2K-R allele, in which multiple lysines in the PIN2 open reading frame were replaced by arginines, failed to be degraded in the vacuole (Leitner et al., 2012b). Furthermore, a PIN2–ubiquitin fusion protein, which otherwise got constitutively endocytosed and sorted to the vacuole, was retained at the PM in the root meristem cells of a quintuple tol mutant line, indicating that TOLs are important in the initial recognition and sorting of PIN2 for degradation (Korbei et al., 2013). These and further results established TOLs being responsible for initiating the vacuolar sorting of PIN2 via the ESCRT pathway (Korbei et al., 2013; Moulinier-Anzola et al., 2020).

As higher-order tol mutants show a defect in the degradation of ubiquitinated PM proteins (Korbei et al., 2013; Moulinier-Anzola et al., 2020), the degradation of proteins involved in the control of ABA signaling and/or homeostasis may also be affected in these mutants. ABA responses have been intimately connected to ubiquitination and the resulting vacuolar sorting of several ABA signaling components (Yu and Xie, 2017). This was shown in recent studies on the ABA receptors, for which ubiquitination has been demonstrated to take place in the nucleus, the cytosol, as well as at the PM (Bueso et al., 2014; Irigoyen et al., 2014; Li et al., 2016; Zhao et al., 2017; Fernandez et al., 2020). Members of the RING FINGER OF SEED LONGEVITY 1 (RSL1)/RING FINGER ABA-RELATED (RFA) family of E3 ubiquitin ligases show distinct functions in these processes. RFA1 and RFA4, which reside in the nucleus and cytosol, ubiquitinate and cause the degradation of PYL4 via the 26S proteasome (Fernandez et al., 2020), whereas the ubiquitination of PYL4 at the PM is catalyzed by RSL1 (Bueso et al., 2014), resulting in PYL4 sorting into the vacuole for degradation (Belda-Palazon et al., 2016; Yu et al., 2016; Garcia-Leon et al., 2019). It is not entirely resolved how these differing locations of the PYR/PYL/RCAR receptors impact on ABA signaling and subsequent responses (Rodriguez et al., 2014; Diaz et al., 2016). Nevertheless, it is now becoming evident that non-redundant pathways controlling protein stability either via K48-or K63-linked polyubiquitination modulate ABA responsiveness via control of protein half-life (Yu et al., 2016). Involvement of the ESCRT machinery in ABA signal modulation was evidenced by the physical interaction of PYR/PYL/RCAR receptors with the ESCRT-I subunits FYVE1/FREE1 and VPS23A in vesicle-like structures, and weak fyve1 and vps23a mutants displayed increased sensitivity to ABA (Belda-Palazon et al., 2016; Yu et al., 2016). ALIX was also shown to physically interact with and mediate trafficking of PYR/PYL/RCAR receptors for degradation in the vacuole (Garcia-Leon et al., 2019). Thus, a specific role for a subset of TOLs or the other ESCRT components VPS23A, ALIX, and FREE/FYVE1 in the control of ABA signaling might be brought about by modifications in ABA responsiveness via reversible adjustments in the abundance or subcellular distribution of ABA signaling elements.

Next to the regulation of auxin homeostasis (Korbei et al., 2013), TOLs could therefore also be relevant for the perception and/or downstream interpretation of signals triggered by ABA, potentially via affecting the half-life of proteins involved in the control of ABA signaling and/or homeostasis (Korbei et al., 2013; Moulinier-Anzola et al., 2020). Thus, it will be essential to decipher if TOL proteins function in modulating the ABA pathway in plants to elucidate, in addition to their general role in the endosomal degradation pathway, if and how TOLs play a more differentiated role in ABA signaling.

Overall plant performance can be considered as a product of signaling pathways defining plant morphogenesis and stress tolerance under favorable and comparably adverse growth conditions (Nuccio et al., 2018; VanWallendael et al., 2019). TOL substrate specificity and activity in the control of protein turnover positions members of this protein family at the intersection of these antagonistically acting growth determinants. Understanding TOL function in further detail is thus likely to result in important insights into the mechanisms by which plants define the trade-off between stress tolerance and plant performance under highly volatile environmental conditions (Maggio et al., 2018).

Future perspectives

In summary, these observations led to a working hypothesis in which elevated tolerance to abiotic stressors such as drought may be due to increased ABA receptor activity caused by mis-functioning members of the ESCRT machinery like potentially also the TOLs. On the other hand, root development, a process coordinated by auxin, also affects plant tolerance to abiotic stresses, including drought (Uga et al., 2013). Thus, in a tol mutant plant line, where the turnover of auxin efflux facilitators is affected, this could be important for the appropriate modulation of auxin homeostasis.

Understanding the genes responsible for modulating the responses to phytohormones, as key mediators of plant responses to drought stress, could be a great approach to maintain as well as improve the productivity of crop plants. Enhanced drought tolerance without affecting further phenotypic traits represents a highly desirable agronomic trait (Waltz, 2014). Nevertheless, such plant lines have to be subjected to extensive phenotypic analysis. Basic growth parameters, including plant and organ shape/size, root architecture, and flowering time, have to be assessed carefully, as well as the plant responses to further environmental parameters, including light quantity/quality, variable temperatures, and additional abiotic stresses as well as responses to selected pathogens. These experiments should reveal potential trade-offs in overall plant development as a consequence of the enhanced drought tolerance (Nuccio et al., 2018; Vaidya et al., 2019).

In the light of recent climate extremes, it appears imperative to generate novel crop varieties that are well adapted to adverse environmental conditions and devoid of undesirable side effects affecting overall plant fitness and/or crop yield. Green biotechnology tried to address this issue, aiming at the generation of less drought-responsive crop varieties, by exploiting a range of different approaches. Different from labor-intense and time-consuming standard breeding strategies, solutions offered by biotechnology most often involve the generation of “conventional” genetically modified organisms (GMOs), utilizing the overexpression or silencing of determinants of drought responses in plants. An alternative to these rather blunt approaches is offered by a combination of knowledge obtained in the model plant A. thaliana and revolutionary precision breeding strategies that became accessible with the establishment of the CRISPR/Cas9 gene editing system. This technique shall be exploited for the introduction of point mutations into soybean ESCRT orthologs of Glycine max (soybean), followed by an in-depth analysis of the resulting genetic varieties, with a particular emphasis on drought tolerance phenotypes. As the acceptance for precision breeding in Europe is still nominal, once such a proof of principle has been provided, corresponding genetic variations need to be obtained from soybean germplasm collections (https://www.soybase.org/soynews/newsview.php). Soybeans play an increasing role in providing a sustainable protein supply in Europe, particularly Austria with its long tradition in soybean cultivation that was launched at the BOKU already in 1878 (Haberlandt, 1878). Thus, generation of drought-tolerant soybean varieties can be considered a succession of a long-standing line of research at this university, connecting conventional breeding approaches with state-of-the-art genome editing techniques employed for the sake of sustainable agronomic applicability.

Figure 1

The endosomal protein degradation system of plants. Continuous endocytosis from the PM to the TGN/EE occurs. PM protein monoubiquitination promotes endocytosis and K63-linked polyubiquitination promotes further transport to the vacuole via the concatenated ILVs of MVBs. This step involves ESCRT components. TOLs and SH3P2 fulfill ubiquitin-recognizing functions at the PM, possibly guiding K63-linked ubiquitinated cargo to the endosomal membrane and interacting with/recruiting ESCRT-I subunits. At the endosomal membrane, FYVE1/FREE1 and ALIX show interaction with ubiquitin. This reveals a complex network of several possible ubiquitin receptors in the ESCRT-mediated degradation pathway.Abbildung 1. Das endosomale Proteinabbausystem von Pflanzen. Kontinuierliche Endozytose erfolgt von der PM zum TGN/EE. Mono-ubiquitinierung von PM-Proteinen fördert die Endozytose und K63-verknüpfte Poly-ubiquitinierung den Weitertransport in die Vakuole über die „concatenated ILVs” der MVBs. An diesem Schritt sind ESCRT-Komponenten beteiligt. TOLs und SH3P2 fungieren als Ubiquitin-rezeptoren an der PM und leiten -gemeinsam mit ESCRT-I Untereinheiten- K63-verknüpfte ubiquitinierte Proteine zur endosomalen Membran. An der endosomalen Membran interagieren FYVE1/FREE1 und ALIX mit Ubiquitin und fungieren somit als zusätzliche Ubiquitinrezeptoren im endosomalen Transport und Abbau von PM-Proteinen.
The endosomal protein degradation system of plants. Continuous endocytosis from the PM to the TGN/EE occurs. PM protein monoubiquitination promotes endocytosis and K63-linked polyubiquitination promotes further transport to the vacuole via the concatenated ILVs of MVBs. This step involves ESCRT components. TOLs and SH3P2 fulfill ubiquitin-recognizing functions at the PM, possibly guiding K63-linked ubiquitinated cargo to the endosomal membrane and interacting with/recruiting ESCRT-I subunits. At the endosomal membrane, FYVE1/FREE1 and ALIX show interaction with ubiquitin. This reveals a complex network of several possible ubiquitin receptors in the ESCRT-mediated degradation pathway.Abbildung 1. Das endosomale Proteinabbausystem von Pflanzen. Kontinuierliche Endozytose erfolgt von der PM zum TGN/EE. Mono-ubiquitinierung von PM-Proteinen fördert die Endozytose und K63-verknüpfte Poly-ubiquitinierung den Weitertransport in die Vakuole über die „concatenated ILVs” der MVBs. An diesem Schritt sind ESCRT-Komponenten beteiligt. TOLs und SH3P2 fungieren als Ubiquitin-rezeptoren an der PM und leiten -gemeinsam mit ESCRT-I Untereinheiten- K63-verknüpfte ubiquitinierte Proteine zur endosomalen Membran. An der endosomalen Membran interagieren FYVE1/FREE1 und ALIX mit Ubiquitin und fungieren somit als zusätzliche Ubiquitinrezeptoren im endosomalen Transport und Abbau von PM-Proteinen.

Arora, D. and D. Van Damme (2021): Motif-based endomembrane trafficking. Plant Physiology 32(11): 3388–3407. AroraD. Van DammeD. 2021 Motif-based endomembrane trafficking Plant Physiology 32 11 3388 3407 10.1093/plphys/kiab077815406733605419 Search in Google Scholar

Babst, M., Wendland, B., Estepa, E.J. and S.D. Emr (1998): The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. The EMBO Journal 17, 2982–2993. BabstM. WendlandB. EstepaE.J. EmrS.D. 1998 The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function The EMBO Journal 17 2982 2993 10.1093/emboj/17.11.298211706389606181 Search in Google Scholar

Bache, K.G., Raiborg, C., Mehlum, A. and H. Stenmark (2003): STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. The Journal of Biological Chemistry 278, 12513–12521. BacheK.G. RaiborgC. MehlumA. StenmarkH. 2003 STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes The Journal of Biological Chemistry 278 12513 12521 10.1074/jbc.M21084320012551915 Search in Google Scholar

Barberon, M., Dubeaux, G., Kolb, C., Isono, E., Zelazny, E. and G. Vert (2014): Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proceedings of the National Academy of Sciences of the United States of America 111, 8293–8298. BarberonM. DubeauxG. KolbC. IsonoE. ZelaznyE. VertG. 2014 Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis Proceedings of the National Academy of Sciences of the United States of America 111 8293 8298 10.1073/pnas.1402262111405056224843126 Search in Google Scholar

Belda-Palazon, B., Rodriguez, L., Fernandez, M.A., Castillo, M.C., Anderson, E.A., Gao, C., Gonzalez-Guzman, M., Peirats-Llobet, M., Zhao, Q., De Winne, N., Gevaert, K., De Jaeger, G., Jiang, L., Leon, J., Mullen, R.T. and P.L. Rodriguez (2016): FYVE1/FREE1 Interacts with the PYL4 ABA Receptor and Mediates its Delivery to the Vacuolar Degradation Pathway. The Plant Cell 28(9): 2291–2311. Belda-PalazonB. RodriguezL. FernandezM.A. CastilloM.C. AndersonE.A. GaoC. Gonzalez-GuzmanM. Peirats-LlobetM. ZhaoQ. De WinneN. GevaertK. De JaegerG. JiangL. LeonJ. MullenR.T. RodriguezP.L. 2016 FYVE1/FREE1 Interacts with the PYL4 ABA Receptor and Mediates its Delivery to the Vacuolar Degradation Pathway The Plant Cell 28 9 2291 2311 10.1105/tpc.16.00178505979527495812 Search in Google Scholar

Benjamins, R. and B. Scheres (2008): Auxin: the looping star in plant development. Annual Review of Plant Biology 59, 443–465. BenjaminsR. ScheresB. 2008 Auxin: the looping star in plant development Annual Review of Plant Biology 59 443 465 10.1146/annurev.arplant.58.032806.10380518444904 Search in Google Scholar

Bertolino, L.T., Caine, R.S. and J.E. Gray (2019): Impact of Stomatal Density and Morphology on Water-Use Efficiency in a Changing World. Frontiers in Plant Science 10, 225. BertolinoL.T. CaineR.S. GrayJ.E. 2019 Impact of Stomatal Density and Morphology on Water-Use Efficiency in a Changing World Frontiers in Plant Science 10 225 10.3389/fpls.2019.00225641475630894867 Search in Google Scholar

Bissig, C. and J. Gruenberg (2014): ALIX and the multivesicular endosome: ALIX in Wonderland. Trends in Cell Biology 24, 19–25. BissigC. GruenbergJ. 2014 ALIX and the multivesicular endosome: ALIX in Wonderland Trends in Cell Biology 24 19 25 10.1016/j.tcb.2013.10.00924287454 Search in Google Scholar

Blanc, C., Charette, S.J., Mattei, S., Aubry, L., Smith, E.W., Cosson, P. and F. Letourneur (2009): Dictyostelium Tom1 participates to an ancestral ESCRT-0 complex. Traffic 10, 161–171. BlancC. CharetteS.J. MatteiS. AubryL. SmithE.W. CossonP. LetourneurF. 2009 Dictyostelium Tom1 participates to an ancestral ESCRT-0 complex Traffic 10 161 171 10.1111/j.1600-0854.2008.00855.x19054384 Search in Google Scholar

Bonifacino, J.S. and L.M. Traub (2003): Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annual Review of Biochemistry 72, 395–447. BonifacinoJ.S. TraubL.M. 2003 Signals for sorting of transmembrane proteins to endosomes and lysosomes Annual Review of Biochemistry 72 395 447 10.1146/annurev.biochem.72.121801.16180012651740 Search in Google Scholar

Bueso, E., Rodriguez, L., Lorenzo-Orts, L., Gonzalez-Guzman, M., Sayas, E., Munoz-Bertomeu, J., Ibanez, C., Serrano, R. and P.L. Rodriguez (2014): The single-subunit RING-type E3 ubiquitin ligase RSL1 targets PYL4 and PYR1 ABA receptors in plasma membrane to modulate abscisic acid signaling. The Plant Journal: for Cell and Molecular Biology 80, 1057–1071. BuesoE. RodriguezL. Lorenzo-OrtsL. Gonzalez-GuzmanM. SayasE. Munoz-BertomeuJ. IbanezC. SerranoR. RodriguezP.L. 2014 The single-subunit RING-type E3 ubiquitin ligase RSL1 targets PYL4 and PYR1 ABA receptors in plasma membrane to modulate abscisic acid signaling The Plant Journal: for Cell and Molecular Biology 80 1057 1071 10.1111/tpj.1270825330042 Search in Google Scholar

Buono, R.A., Leier, A., Paez-Valencia, J., Pennington, J., Goodman, K., Miller, N., Ahlquist, P., Marquez-Lago, T.T. and M.S. Otegui (2017): ESCRT-mediated vesicle concatenation in plant endosomes. The Journal of Cell Biology 216, 2167–2177. BuonoR.A. LeierA. Paez-ValenciaJ. PenningtonJ. GoodmanK. MillerN. AhlquistP. Marquez-LagoT.T. OteguiM.S. 2017 ESCRT-mediated vesicle concatenation in plant endosomes The Journal of Cell Biology 216 2167 2177 10.1083/jcb.201612040549662128592443 Search in Google Scholar

Cai, Y., Zhuang, X.H., Gao, C.J., Wang, X.F. and L.W. Jiang (2014): The Arabidopsis Endosomal Sorting Complex Required for Transport III Regulates Internal Vesicle Formation of the Prevacuolar Compartment and Is Required for Plant Development. Plant Physiology 165, 1328–1343. CaiY. ZhuangX.H. GaoC.J. WangX.F. JiangL.W. 2014 The Arabidopsis Endosomal Sorting Complex Required for Transport III Regulates Internal Vesicle Formation of the Prevacuolar Compartment and Is Required for Plant Development Plant Physiology 165 1328 1343 10.1104/pp.114.238378408134024812106 Search in Google Scholar

Callis, J. (2014): The ubiquitination machinery of the ubiquitin system. The Arabidopsis Book / American Society of Plant Biologists 12, e0174. CallisJ. 2014 The ubiquitination machinery of the ubiquitin system The Arabidopsis Book / American Society of Plant Biologists 12 e0174 10.1199/tab.0174419667625320573 Search in Google Scholar

Cardona-Lopez, X., Cuyas, L., Marin, E., Rajulu, C., Irigoyen, M.L., Gil, E., Puga, M.I., Bligny, R., Nussaume, L., Geldner, N., Paz-Ares, J. and V. Rubio (2015): ESCRT-III-Associated Protein ALIX Mediates High-Affinity Phosphate Transporter Trafficking to Maintain Phosphate Homeostasis in Arabidopsis. The Plant Cell 27, 2560–2581. Cardona-LopezX. CuyasL. MarinE. RajuluC. IrigoyenM.L. GilE. PugaM.I. BlignyR. NussaumeL. GeldnerN. Paz-AresJ. RubioV. 2015 ESCRT-III-Associated Protein ALIX Mediates High-Affinity Phosphate Transporter Trafficking to Maintain Phosphate Homeostasis in Arabidopsis The Plant Cell 27 2560 2581 10.1105/tpc.15.00393481510526342016 Search in Google Scholar

Chen, X., Irani, N.G. J. and Friml (2011): Clathrin-mediated endocytosis: the gateway into plant cells. Current Opinion in Plant Biology 14, 674–682. ChenX. IraniN.G. FrimlJ. 2011 Clathrin-mediated endocytosis: the gateway into plant cells Current Opinion in Plant Biology 14 674 682 10.1016/j.pbi.2011.08.00621945181 Search in Google Scholar

Clague, M.J., Liu, H. S. and Urbe (2012): Governance of endocytic trafficking and signaling by reversible ubiquitylation. Developmental Cell 23, 457–467. ClagueM.J. LiuH. UrbeS. 2012 Governance of endocytic trafficking and signaling by reversible ubiquitylation Developmental Cell 23 457 467 10.1016/j.devcel.2012.08.01122975321 Search in Google Scholar

Cocucci, E., Aguet, F., Boulant, S. and T. Kirchhausen (2012): The first five seconds in the life of a clathrin-coated pit. Cell 150, 495–507. CocucciE. AguetF. BoulantS. KirchhausenT. 2012 The first five seconds in the life of a clathrin-coated pit Cell 150 495 507 10.1016/j.cell.2012.05.047341309322863004 Search in Google Scholar

Cui, Y., He, Y.L., Cao, W.H., Gao, J.Y. and L.W. Jiang (2018): The Multivesicular Body and Autophagosome Pathways in Plants. Frontiers in plant science 9. CuiY. HeY.L. CaoW.H. GaoJ.Y. JiangL.W. 2018 The Multivesicular Body and Autophagosome Pathways in Plants Frontiers in plant science 9 10.3389/fpls.2018.01837629902930619408 Search in Google Scholar

Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R. and S.R. Abrams (2010): Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651–679. CutlerS.R. RodriguezP.L. FinkelsteinR.R. AbramsS.R. 2010 Abscisic acid: emergence of a core signaling network Annual Review of Plant Biology 61 651 679 10.1146/annurev-arplant-042809-11212220192755 Search in Google Scholar

Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D. and K. Schumacher (2006): Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. The Plant Cell 18, 715–730. DettmerJ. Hong-HermesdorfA. StierhofY.D. SchumacherK. 2006 Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis The Plant Cell 18 715 730 10.1105/tpc.105.037978138364516461582 Search in Google Scholar

Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D. and J. Friml (2007): Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Current Biology : CB 17, 520–527. DhonuksheP. AnientoF. HwangI. RobinsonD.G. MravecJ. StierhofY.D. FrimlJ. 2007 Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis Current Biology : CB 17 520 527 10.1016/j.cub.2007.01.05217306539 Search in Google Scholar

Di Rubbo, S., Irani, N.G., Kim, S.Y., Xu, Z.Y., Gadeyne, A., Dejonghe, W., Vanhoutte, I., Persiau, G., Eeckhout, D., Simon, S., Song, K., Kleine-Vehn, J., Friml, J., De Jaeger, G., Van Damme, D., Hwang, I. and E. Russinova, (2013): The clathrin adaptor complex AP-2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis. The Plant Cell 25, 2986–2997. Di RubboS. IraniN.G. KimS.Y. XuZ.Y. GadeyneA. DejongheW. VanhoutteI. PersiauG. EeckhoutD. SimonS. SongK. Kleine-VehnJ. FrimlJ. De JaegerG. Van DammeD. HwangI. RussinovaE. 2013 The clathrin adaptor complex AP-2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis The Plant Cell 25 2986 2997 10.1105/tpc.113.114058378459323975899 Search in Google Scholar

Diaz, M., Sanchez-Barrena, M.J., Gonzalez-Rubio, J.M., Rodriguez, L., Fernandez, D., Antoni, R., Yunta, C., Belda-Palazon, B., Gonzalez-Guzman, M., Peirats-Llobet, M., Menendez, M., Boskovic, J., Marquez, J.A., Rodriguez, P.L. and A Albert (2016): Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling. Proceedings of the National Academy of Sciences of the United States of America 113, E396–405. DiazM. Sanchez-BarrenaM.J. Gonzalez-RubioJ.M. RodriguezL. FernandezD. AntoniR. YuntaC. Belda-PalazonB. Gonzalez-GuzmanM. Peirats-LlobetM. MenendezM. BoskovicJ. MarquezJ.A. RodriguezP.L. AlbertA 2016 Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling Proceedings of the National Academy of Sciences of the United States of America 113 E396 405 10.1073/pnas.1512779113472554026719420 Search in Google Scholar

Dowlatshahi, D.P., Sandrin, V., Vivona, S., Shaler, T.A., Kaiser, S.E., Melandri, F., Sundquist, W.I. and R.R. Kopito (2012): ALIX is a Lys63-specific polyubiquitin binding protein that functions in retrovirus budding. Developmental Cell 23, 1247–1254. DowlatshahiD.P. SandrinV. VivonaS. ShalerT.A. KaiserS.E. MelandriF. SundquistW.I. KopitoR.R. 2012 ALIX is a Lys63-specific polyubiquitin binding protein that functions in retrovirus budding Developmental Cell 23 1247 1254 10.1016/j.devcel.2012.10.023352277023201121 Search in Google Scholar

Dubeaux, G. and G. Vert (2017): Zooming into plant ubiquitin-mediated endocytosis. Current Opinion in Plant Biology 40, 56–62. DubeauxG. VertG. 2017 Zooming into plant ubiquitin-mediated endocytosis Current Opinion in Plant Biology 40 56 62 10.1016/j.pbi.2017.07.00528756333 Search in Google Scholar

Dubeaux, G., Neveu, J., Zelazny, E. and G. Vert (2018): Metal Sensing by the IRT1 Transporter-Receptor Orchestrates Its Own Degradation and Plant Metal Nutrition. Molecular Cell 69, 953–964 e955. DubeauxG. NeveuJ. ZelaznyE. VertG. 2018 Metal Sensing by the IRT1 Transporter-Receptor Orchestrates Its Own Degradation and Plant Metal Nutrition Molecular Cell 69 953 964 e955 10.1016/j.molcel.2018.02.00929547723 Search in Google Scholar

Fernandez, M.A., Belda-Palazon, B., Julian, J., Coego, A., Lozano-Juste, J., Inigo, S., Rodriguez, L., Bueso, E., Goossens, A. and P.L. Rodriguez (2020): RBR-Type E3 Ligases and the Ubiquitin-Conjugating Enzyme UBC26 Regulate Abscisic Acid Receptor Levels and Signaling. Plant Physiology 182, 1723–1742. FernandezM.A. Belda-PalazonB. JulianJ. CoegoA. Lozano-JusteJ. InigoS. RodriguezL. BuesoE. GoossensA. RodriguezP.L. 2020 RBR-Type E3 Ligases and the Ubiquitin-Conjugating Enzyme UBC26 Regulate Abscisic Acid Receptor Levels and Signaling Plant Physiology 182 1723 1742 10.1104/pp.19.00898714094931699847 Search in Google Scholar

Finkelstein, R. (2013): Abscisic Acid synthesis and response. The Arabidopsis Book / American Society of Plant Biologists 11, e0166. FinkelsteinR. 2013 Abscisic Acid synthesis and response The Arabidopsis Book / American Society of Plant Biologists 11 e0166 10.1199/tab.0166383320024273463 Search in Google Scholar

Gallei, M., Luschnig, C. and J. Friml (2020): Auxin signalling in growth: Schrodinger's cat out of the bag. Current Opinion in Plant Biology 53, 43–49. GalleiM. LuschnigC. FrimlJ. 2020 Auxin signalling in growth: Schrodinger's cat out of the bag Current Opinion in Plant Biology 53 43 49 10.1016/j.pbi.2019.10.00331760231 Search in Google Scholar

Gao, C., Zhuang, X., Shen, J. and L. Jiang (2017): Plant ESCRT Complexes: Moving Beyond Endosomal Sorting. Trends in Plant Science 22, 986–998. GaoC. ZhuangX. ShenJ. JiangL. 2017 Plant ESCRT Complexes: Moving Beyond Endosomal Sorting Trends in Plant Science 22 986 998 10.1016/j.tplants.2017.08.00328867368 Search in Google Scholar

Gao, C., Luo, M., Zhao, Q., Yang, R., Cui, Y., Zeng, Y., Xia, J. and L. Jiang (2014): A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Current Biology : CB 24, 2556–2563. GaoC. LuoM. ZhaoQ. YangR. CuiY. ZengY. XiaJ. JiangL. 2014 A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth Current Biology : CB 24 2556 2563 10.1016/j.cub.2014.09.01425438943 Search in Google Scholar

Garcia-Leon, M., Cuyas, L., El-Moneim, D.A., Rodriguez, L., Belda-Palazon, B., Sanchez-Quant, E., Fernandez, Y., Roux, B., Zamarreno, A.M., Garcia-Mina, J.M., Nussaume, L., Rodriguez, P.L., Paz-Ares, J., Leonhardt, N. and V. Rubio, (2019): Arabidopsis ALIX Regulates Stomatal Aperture and Turnover of Abscisic Acid Receptors. The Plant Cell 31, 2411–2429. Garcia-LeonM. CuyasL. El-MoneimD.A. RodriguezL. Belda-PalazonB. Sanchez-QuantE. FernandezY. RouxB. ZamarrenoA.M. Garcia-MinaJ.M. NussaumeL. RodriguezP.L. Paz-AresJ. LeonhardtN. RubioV. 2019 Arabidopsis ALIX Regulates Stomatal Aperture and Turnover of Abscisic Acid Receptors The Plant Cell 31 2411 2429 10.1105/tpc.19.00399679009631363038 Search in Google Scholar

Gatta, A.T. and J.G. Carlton (2019): The ESCRT-machinery: closing holes and expanding roles. Current Opinion in Cell Biology 59, 121–132. GattaA.T. CarltonJ.G. 2019 The ESCRT-machinery: closing holes and expanding roles Current Opinion in Cell Biology 59 121 132 10.1016/j.ceb.2019.04.00531132588 Search in Google Scholar

Geldner, N. and S. Robatzek (2008): Plant receptors go endosomal: a moving view on signal transduction. Plant Physiology 147, 1565–1574. GeldnerN. RobatzekS. 2008 Plant receptors go endosomal: a moving view on signal transduction Plant Physiology 147 1565 1574 10.1104/pp.108.120287249260018678748 Search in Google Scholar

Gomez-Cadenas, A., Vives, V., Zandalinas, S.I., Manzi, M., Sanchez-Perez, A.M., Perez-Clemente, R.M. and V. Arbona (2015): Abscisic Acid: a versatile phytohormone in plant signaling and beyond. Current Protein and Peptide Science 16, 413–434. Gomez-CadenasA. VivesV. ZandalinasS.I. ManziM. Sanchez-PerezA.M. Perez-ClementeR.M. ArbonaV. 2015 Abscisic Acid: a versatile phytohormone in plant signaling and beyond Current Protein and Peptide Science 16 413 434 10.2174/138920371666615033013010225824385 Search in Google Scholar

Gray, S.B. and S.M. Brady (2016): Plant developmental responses to climate change. Developmental Biology 419, 64–77. GrayS.B. BradyS.M. 2016 Plant developmental responses to climate change Developmental Biology 419 64 77 10.1016/j.ydbio.2016.07.02327521050 Search in Google Scholar

Gupta, A., Rico-Medina, A. and A.I. Cano-Delgado (2020): The physiology of plant responses to drought. Science 368, 266–269. GuptaA. Rico-MedinaA. Cano-DelgadoA.I. 2020 The physiology of plant responses to drought Science 368 266 269 10.1126/science.aaz761432299946 Search in Google Scholar

Haas, T.J., Sliwinski, M.K., Martinez, D.E., Preuss, M., Ebine, K., Ueda, T., Nielsen, E., Odorizzi, G. and M.S. Otegui, (2007): The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. The Plant Cell 19, 1295–1312. HaasT.J. SliwinskiM.K. MartinezD.E. PreussM. EbineK. UedaT. NielsenE. OdorizziG. OteguiM.S. 2007 The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5 The Plant Cell 19 1295 1312 10.1105/tpc.106.049346191375017468262 Search in Google Scholar

Haberlandt, F. (1878). Die Sojabohne: Ergebnisse der Studien und Versuche über die Anbauwürdigkeit dieser neu einzuführenden Culturpflanze. (Gerold). HaberlandtF. 1878 Die Sojabohne: Ergebnisse der Studien und Versuche über die Anbauwürdigkeit dieser neu einzuführenden Culturpflanze Gerold Search in Google Scholar

Henne, W.M., Buchkovich, N.J. and S.D. Emr (2011): The ESCRT Pathway. Developmental Cell 21, 77–91. HenneW.M. BuchkovichN.J. EmrS.D. 2011 The ESCRT Pathway Developmental Cell 21 77 91 10.1016/j.devcel.2011.05.01521763610 Search in Google Scholar

Henne, W.M., Buchkovich, N.J., Zhao, Y. and S.D. Emr (2012): The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices. Cell 151, 356–371. HenneW.M. BuchkovichN.J. ZhaoY. EmrS.D. 2012 The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices Cell 151 356 371 10.1016/j.cell.2012.08.03923063125 Search in Google Scholar

Herman, E.K., Walker, G., van der Giezen, M. and J.B. Dacks (2011): Multivesicular bodies in the enigmatic amoeboflagellate Breviata anathema and the evolution of ESCRT 0. Journal of Cell Science 124, 613–621. HermanE.K. WalkerG. van der GiezenM. DacksJ.B. 2011 Multivesicular bodies in the enigmatic amoeboflagellate Breviata anathema and the evolution of ESCRT 0 Journal of Cell Science 124 613 621 10.1242/jcs.078436303137221266469 Search in Google Scholar

Hua, Z. and R.D. Vierstra (2011): The cullin-RING ubiquitin-protein ligases. Annual Review of Plant Biology 62, 299–334. HuaZ. VierstraR.D. 2011 The cullin-RING ubiquitin-protein ligases Annual Review of Plant Biology 62 299 334 10.1146/annurev-arplant-042809-11225621370976 Search in Google Scholar

Hurley, J.H. (2008): ESCRT complexes and the biogenesis of multivesicular bodies. Current Opinion in Cell Biology 20, 4–11. HurleyJ.H. 2008 ESCRT complexes and the biogenesis of multivesicular bodies Current Opinion in Cell Biology 20 4 11 10.1016/j.ceb.2007.12.002228206718222686 Search in Google Scholar

Hurley, J.H. (2010): The ESCRT complexes. Critical Reviews in Biochemistry and Molecular Biology 45, 463–487. HurleyJ.H. 2010 The ESCRT complexes Critical Reviews in Biochemistry and Molecular Biology 45 463 487 10.3109/10409238.2010.502516298897420653365 Search in Google Scholar

Hurley, J.H. and X. Ren (2009): The circuitry of cargo flux in the ESCRT pathway. The Journal of Cell Biology 185, 185–187. HurleyJ.H. RenX. 2009 The circuitry of cargo flux in the ESCRT pathway The Journal of Cell Biology 185 185 187 10.1083/jcb.200903013270036719380875 Search in Google Scholar

Hurley, J.H. and P.I. Hanson (2010): Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nature Reviews. Molecular cell biology 11, 556–566. HurleyJ.H. HansonP.I. 2010 Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nature Reviews Molecular cell biology 11 556 566 Search in Google Scholar

Husnjak, K. and I. Dikic (2012): Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annual Review of Biochemistry 81, 291–322. HusnjakK. DikicI. 2012 Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions Annual Review of Biochemistry 81 291 322 10.1146/annurev-biochem-051810-09465422482907 Search in Google Scholar

Inada, N. and T. Ueda (2014): Membrane trafficking pathways and their roles in plant-microbe interactions. Plant and Cell Physiology 55, 672–686. InadaN. UedaT. 2014 Membrane trafficking pathways and their roles in plant-microbe interactions Plant and Cell Physiology 55 672 686 10.1093/pcp/pcu04624616268 Search in Google Scholar

Irigoyen, M.L., Iniesto, E., Rodriguez, L., Puga, M.I., Yanagawa, Y., Pick, E., Strickland, E., Paz-Ares, J., Wei, N., De Jaeger, G., Rodriguez, P.L., Deng, X.W. and V. Rubio (2014): Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis. The Plant Cell 26, 712–728. IrigoyenM.L. IniestoE. RodriguezL. PugaM.I. YanagawaY. PickE. StricklandE. Paz-AresJ. WeiN. De JaegerG. RodriguezP.L. DengX.W. RubioV. 2014 Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis The Plant Cell 26 712 728 10.1105/tpc.113.122234396703524563205 Search in Google Scholar

Isono, E. and M.K. Nagel (2014): Deubiquitylating enzymes and their emerging role in plant biology. Frontiers in Plant Science 5, 56. IsonoE. NagelM.K. 2014 Deubiquitylating enzymes and their emerging role in plant biology Frontiers in Plant Science 5 56 10.3389/fpls.2014.00056392856624600466 Search in Google Scholar

Isono, E. and K. Kalinowska (2017): ESCRT-dependent degradation of ubiquitylated plasma membrane proteins in plants. Current Opinion in Plant Biology 40, 49–55. IsonoE. KalinowskaK. 2017 ESCRT-dependent degradation of ubiquitylated plasma membrane proteins in plants Current Opinion in Plant Biology 40 49 55 10.1016/j.pbi.2017.07.00328753460 Search in Google Scholar

Johnson, A. and G. Vert (2016): Unraveling K63 Polyubiquitination Networks by Sensor-Based Proteomics. Plant Physiology 171, 1808–1820. JohnsonA. VertG. 2016 Unraveling K63 Polyubiquitination Networks by Sensor-Based Proteomics Plant Physiology 171 1808 1820 10.1104/pp.16.00619493658627208306 Search in Google Scholar

Kalinowska, K., Nagel, M.K., Goodman, K., Cuyas, L., Anzenberger, F., Alkofer, A., Paz-Ares, J., Braun, P., Rubio, V., Otegui, M.S. and E. Isono (2015): Arabidopsis ALIX is required for the endosomal localization of the deubiquitinating enzyme AMSH3. Proceedings of the National Academy of Sciences of the United States of America 112, E5543–5551. KalinowskaK. NagelM.K. GoodmanK. CuyasL. AnzenbergerF. AlkoferA. Paz-AresJ. BraunP. RubioV. OteguiM.S. IsonoE. 2015 Arabidopsis ALIX is required for the endosomal localization of the deubiquitinating enzyme AMSH3 Proceedings of the National Academy of Sciences of the United States of America 112 E5543 5551 10.1073/pnas.1510516112460348726324913 Search in Google Scholar

Katsiarimpa, A., Anzenberger, F., Schlager, N., Neubert, S., Hauser, M.T., Schwechheimer, C. and E. Isono (2011): The Arabidopsis deubiquitinating enzyme AMSH3 interacts with ESCRT-III subunits and regulates their localization. The Plant Cell 23, 3026–3040. KatsiarimpaA. AnzenbergerF. SchlagerN. NeubertS. HauserM.T. SchwechheimerC. IsonoE. 2011 The Arabidopsis deubiquitinating enzyme AMSH3 interacts with ESCRT-III subunits and regulates their localization The Plant Cell 23 3026 3040 10.1105/tpc.111.087254318080821810997 Search in Google Scholar

Kim, J.H., Hilleary, R., Seroka, A. and S.Y. He (2021): Crops of the future: building a climate-resilient plant immune system. Current Opinion in Plant biology 60, 101997. KimJ.H. HillearyR. SerokaA. HeS.Y. 2021 Crops of the future: building a climate-resilient plant immune system Current Opinion in Plant biology 60 101997 10.1016/j.pbi.2020.101997818458333454653 Search in Google Scholar

Kleine-Vehn, J., Wabnik, K., Martiniere, A., Langowski, L., Willig, K., Naramoto, S., Leitner, J., Tanaka, H., Jakobs, S., Robert, S., Luschnig, C., Govaerts, W., Hell, S.W., Runions, J. and J. Friml (2011): Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Molecular Systems Biology 7, 540. Kleine-VehnJ. WabnikK. MartiniereA. LangowskiL. WilligK. NaramotoS. LeitnerJ. TanakaH. JakobsS. RobertS. LuschnigC. GovaertsW. HellS.W. RunionsJ. FrimlJ. 2011 Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane Molecular Systems Biology 7 540 10.1038/msb.2011.72326171822027551 Search in Google Scholar

Kolb, C., Nagel, M.K., Kalinowska, K., Hagmann, J., Ichikawa, M., Anzenberger, F., Alkofer, A., Sato, M.H., Braun, P. and E. Isono (2015): FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis. Plant Physiology 167, 1361–1373. KolbC. NagelM.K. KalinowskaK. HagmannJ. IchikawaM. AnzenbergerF. AlkoferA. SatoM.H. BraunP. IsonoE. 2015 FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis Plant Physiology 167 1361 1373 10.1104/pp.114.253377437815625699591 Search in Google Scholar

Konstantinova, N., Korbei, B. and C. Luschnig (2021): Auxin and Root Gravitropism: Addressing Basic Cellular Processes by Exploiting a Defined Growth Response. International Journal of Molecular Sciences 22. KonstantinovaN. KorbeiB. LuschnigC. 2021 Auxin and Root Gravitropism: Addressing Basic Cellular Processes by Exploiting a Defined Growth Response International Journal of Molecular Sciences 22 10.3390/ijms22052749796315633803128 Search in Google Scholar

Korbei, B. and C. Luschnig (2013): Plasma membrane protein ubiquitylation and degradation as determinants of positional growth in plants. Journal of Integrative Plant Biology 55, 809–823. KorbeiB. LuschnigC. 2013 Plasma membrane protein ubiquitylation and degradation as determinants of positional growth in plants Journal of Integrative Plant Biology 55 809 823 10.1111/jipb.1205923981390 Search in Google Scholar

Korbei, B., Moulinier-Anzola, J., De-Araujo, L., Lucyshyn, D., Retzer, K., Khan, M.A. and C. Luschnig (2013): Arabidopsis TOL Proteins Act as Gatekeepers for Vacuolar Sorting of PIN2 Plasma Membrane Protein. Current Biology : CB. Volume 23, Issue 24, Pages 2500–2505 KorbeiB. Moulinier-AnzolaJ. De-AraujoL. LucyshynD. RetzerK. KhanM.A. LuschnigC. 2013 Arabidopsis TOL Proteins Act as Gatekeepers for Vacuolar Sorting of PIN2 Plasma Membrane Protein Current Biology : CB 23 24 2500 2505 10.1016/j.cub.2013.10.03624316203 Search in Google Scholar

Lavenus, J., Goh, T., Roberts, I., Guyomarc’h, S., Lucas, M., De Smet, I., Fukaki, H., Beeckman, T., Bennett, M. and L. Laplaze (2013): Lateral root development in Arabidopsis: fifty shades of auxin. Trends in Plant Science 18, 450–458. LavenusJ. GohT. RobertsI. Guyomarc’hS. LucasM. De SmetI. FukakiH. BeeckmanT. BennettM. LaplazeL. 2013 Lateral root development in Arabidopsis: fifty shades of auxin Trends in Plant Science 18 450 458 10.1016/j.tplants.2013.04.00623701908 Search in Google Scholar

Leitner, J., Retzer, K., Korbei, B. and C. Luschnig (2012a): Dynamics in PIN2 auxin carrier ubiquitylation in gravity-responding Arabidopsis roots. Plant Signaling & Behavior 7, 1271–1273. LeitnerJ. RetzerK. KorbeiB. LuschnigC. 2012a Dynamics in PIN2 auxin carrier ubiquitylation in gravity-responding Arabidopsis roots Plant Signaling & Behavior 7 1271 1273 10.4161/psb.21715349341122902683 Search in Google Scholar

Leitner, J., Petrasek, J., Tomanov, K., Retzer, K., Parezova, M., Korbei, B., Bachmair, A., Zazimalova, E. and C. Luschnig (2012b): Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proceedings of the National Academy of Sciences of the United States of America 109, 8322–8327. LeitnerJ. PetrasekJ. TomanovK. RetzerK. ParezovaM. KorbeiB. BachmairA. ZazimalovaE. LuschnigC. 2012b Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth Proceedings of the National Academy of Sciences of the United States of America 109 8322 8327 10.1073/pnas.1200824109336143922556266 Search in Google Scholar

Leung, K.F., Dacks, J.B. and M.C. Field (2008): Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698–1716. LeungK.F. DacksJ.B. FieldM.C. 2008 Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage Traffic 9 1698 1716 10.1111/j.1600-0854.2008.00797.x18637903 Search in Google Scholar

Li, Y., Zhang, L., Li, D., Liu, Z., Wang, J., Li, X. and Y. Yang (2016): The Arabidopsis F-box E3 ligase RIFP1 plays a negative role in abscisic acid signalling by facilitating ABA receptor RCAR3 degradation. Plant Cell Environment 39, 571–582. LiY. ZhangL. LiD. LiuZ. WangJ. LiX. YangY. 2016 The Arabidopsis F-box E3 ligase RIFP1 plays a negative role in abscisic acid signalling by facilitating ABA receptor RCAR3 degradation Plant Cell Environment 39 571 582 10.1111/pce.1263926386272 Search in Google Scholar

Liu, D., Kumar, R., Claus, L.A.N., Johnson, A.J., Siao, W., Vanhoutte, I., Wang, P., Bender, K.W., Yperman, K., Martins, S., Zhao, X., Vert, G., Van Damme, D., Friml, J. and E. Russinova (2020): Endocytosis of BRASSINOSTEROID INSENSITIVE1 Is Partly Driven by a Canonical Tyr-Based Motif. The Plant Cell 32, 3598–3612. LiuD. KumarR. ClausL.A.N. JohnsonA.J. SiaoW. VanhoutteI. WangP. BenderK.W. YpermanK. MartinsS. ZhaoX. VertG. Van DammeD. FrimlJ. RussinovaE. 2020 Endocytosis of BRASSINOSTEROID INSENSITIVE1 Is Partly Driven by a Canonical Tyr-Based Motif The Plant Cell 32 3598 3612 10.1105/tpc.20.00384761030032958564 Search in Google Scholar

Liu, N.S., Loo, L.S., Loh, E., Seet, L.F. and W. Hong (2009): Participation of Tom1L1 in EGF-stimulated endocytosis of EGF receptor. The EMBO journal 28, 3485–3499. LiuN.S. LooL.S. LohE. SeetL.F. HongW. 2009 Participation of Tom1L1 in EGF-stimulated endocytosis of EGF receptor The EMBO journal 28 3485 3499 10.1038/emboj.2009.282275656719798056 Search in Google Scholar

Luschnig, C. and G. Vert (2014): The dynamics of plant plasma membrane proteins: PINs and beyond. Development 141, 2924–2938. LuschnigC. VertG. 2014 The dynamics of plant plasma membrane proteins: PINs and beyond Development 141 2924 2938 10.1242/dev.10342425053426 Search in Google Scholar

Maggio, A., Bressan, R.A., Zhao, Y., Park, J. and D.J. Yun (2018): It's Hard to Avoid Avoidance: Uncoupling the Evolutionary Connection between Plant Growth, Productivity and Stress “Tolerance”. International Journal of Molecular Sciences 19. MaggioA. BressanR.A. ZhaoY. ParkJ. YunD.J. 2018 It's Hard to Avoid Avoidance: Uncoupling the Evolutionary Connection between Plant Growth, Productivity and Stress “Tolerance” International Journal of Molecular Sciences 19 10.3390/ijms19113671627485430463352 Search in Google Scholar

Martins, S., Dohmann, E.M., Cayrel, A., Johnson, A., Fischer, W., Pojer, F., Satiat-Jeunemaitre, B., Jaillais, Y., Chory, J., Geldner, N. and G. Vert (2015): Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination. Nature Communications 6, 6151. MartinsS. DohmannE.M. CayrelA. JohnsonA. FischerW. PojerF. Satiat-JeunemaitreB. JaillaisY. ChoryJ. GeldnerN. VertG. 2015 Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination Nature Communications 6 6151 10.1038/ncomms7151471303225608221 Search in Google Scholar

Mayers, J.R., Wang, L., Pramanik, J., Johnson, A., Sarkeshik, A., Wang, Y., Saengsawang, W., Yates, J.R., 3rd and A. Audhya (2013): Regulation of ubiquitin-dependent cargo sorting by multiple endocytic adaptors at the plasma membrane. Proceedings of the National Academy of Sciences of the United States of America 110, 11857–11862. MayersJ.R. WangL. PramanikJ. JohnsonA. SarkeshikA. WangY. SaengsawangW. YatesJ.R.3rd AudhyaA. 2013 Regulation of ubiquitin-dependent cargo sorting by multiple endocytic adaptors at the plasma membrane Proceedings of the National Academy of Sciences of the United States of America 110 11857 11862 10.1073/pnas.1302918110371811223818590 Search in Google Scholar

McMahon, H.T. and E. Boucrot (2011): Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nature Reviews. Molecular Cell Biology 12, 517–533. McMahonH.T. BoucrotE. 2011 Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nature Reviews Molecular Cell Biology 12 517 533 Search in Google Scholar

Merlot, S., Mustilli, A.C., Genty, B., North, H., Lefebvre, V., Sotta, B., Vavasseur, A. and J. Giraudat (2002): Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. The Plant Journal : for Cell and Molecular biology 30, 601–609. MerlotS. MustilliA.C. GentyB. NorthH. LefebvreV. SottaB. VavasseurA. GiraudatJ. 2002 Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation The Plant Journal : for Cell and Molecular biology 30 601 609 10.1046/j.1365-313X.2002.01322.x12047634 Search in Google Scholar

Merlot, S., Leonhardt, N., Fenzi, F., Valon, C., Costa, M., Piette, L., Vavasseur, A., Genty, B., Boivin, K., Muller, A., Giraudat, J. and J. Leung (2007): Constitutive activation of a plasma membrane H(+)-ATPase prevents abscisic acid-mediated stomatal closure. The EMBO journal 26, 3216–3226. MerlotS. LeonhardtN. FenziF. ValonC. CostaM. PietteL. VavasseurA. GentyB. BoivinK. MullerA. GiraudatJ. LeungJ. 2007 Constitutive activation of a plasma membrane H(+)-ATPase prevents abscisic acid-mediated stomatal closure The EMBO journal 26 3216 3226 10.1038/sj.emboj.7601750191409817557075 Search in Google Scholar

Mosesso, N., Nagel, M.K. and E. Isono (2019): Ubiquitin recognition in endocytic trafficking - with or without ESCRT-0. Journal of Cell Science 132. MosessoN. NagelM.K. IsonoE. 2019 Ubiquitin recognition in endocytic trafficking - with or without ESCRT-0 Journal of Cell Science 132 10.1242/jcs.23286831416855 Search in Google Scholar

Moulinier-Anzola, J., De-Araujo, L. and B. Korbei (2014): Expression of Arabidopsis TOL genes. Plant Signaling & Behavior 9, e28667. Moulinier-AnzolaJ. De-AraujoL. KorbeiB. 2014 Expression of Arabidopsis TOL genes Plant Signaling & Behavior 9 e28667 10.4161/psb.2866725764436 Search in Google Scholar

Moulinier-Anzola, J., Schwihla, M., De-Araújo, L., Artner, C., Jörg, L., Konstantinova, N., Luschnig, C. and B. Korbei (2020): TOLs function as ubiquitin receptors in the early steps of the ESCRT pathway in higher plants. Molecular Plant (5):717–731 Moulinier-AnzolaJ. SchwihlaM. De-AraújoL. ArtnerC. JörgL. KonstantinovaN. LuschnigC. KorbeiB. 2020 TOLs function as ubiquitin receptors in the early steps of the ESCRT pathway in higher plants Molecular Plant 5 717 731 10.1016/j.molp.2020.02.01232087370 Search in Google Scholar

Murashige, T. and F. Skoog (1962): A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum 15, 473–497. MurashigeT. SkoogF. 1962 A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Physiologia Plantarum 15 473 497 10.1111/j.1399-3054.1962.tb08052.x Search in Google Scholar

Nagel, M.K., Kalinowska, K., Vogel, K., Reynolds, G.D., Wu, Z., Anzenberger, F., Ichikawa, M., Tsutsumi, C., Sato, M.H., Kuster, B., Bednarek, S.Y. and E. Isono (2017): Arabidopsis SH3P2 is an ubiquitin-binding protein that functions together with ESCRT-I and the deubiquitylating enzyme AMSH3. Proceedings of the National Academy of Sciences of the United States of America 114, E7197–E7204. NagelM.K. KalinowskaK. VogelK. ReynoldsG.D. WuZ. AnzenbergerF. IchikawaM. TsutsumiC. SatoM.H. KusterB. BednarekS.Y. IsonoE. 2017 Arabidopsis SH3P2 is an ubiquitin-binding protein that functions together with ESCRT-I and the deubiquitylating enzyme AMSH3 Proceedings of the National Academy of Sciences of the United States of America 114 E7197 E7204 10.1073/pnas.1710866114557683928784794 Search in Google Scholar

Nakashima, K. and K. Yamaguchi-Shinozaki (2013): ABA signaling in stress-response and seed development. Plant Cell Reports 32, 959–970. NakashimaK. Yamaguchi-ShinozakiK. 2013 ABA signaling in stress-response and seed development Plant Cell Reports 32 959 970 10.1007/s00299-013-1418-123535869 Search in Google Scholar

Narasimhan, M., Johnson, A., Prizak, R., Kaufmann, W.A., Tan, S., Casillas-Perez, B. and J. Friml (2020): Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants. Elife 9. NarasimhanM. JohnsonA. PrizakR. KaufmannW.A. TanS. Casillas-PerezB. FrimlJ. 2020 Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants Elife 9 10.7554/eLife.52067701260931971511 Search in Google Scholar

Nathan, J.A., Tae Kim, H., Ting, L., Gygi, S.P. and A.L. Goldberg (2013): Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? The EMBO journal 32, 552–565. NathanJ.A. Tae KimH. TingL. GygiS.P. GoldbergA.L. 2013 Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? The EMBO journal 32 552 565 10.1038/emboj.2012.354357913823314748 Search in Google Scholar

Nuccio, M.L., Paul, M., Bate, N.J., Cohn, J. and S.R. Cutler (2018): Where are the drought tolerant crops? An assessment of more than two decades of plant biotechnology effort in crop improvement. Plant Science 273, 110–119. NuccioM.L. PaulM. BateN.J. CohnJ. CutlerS.R. 2018 Where are the drought tolerant crops? An assessment of more than two decades of plant biotechnology effort in crop improvement Plant Science 273 110 119 10.1016/j.plantsci.2018.01.02029907303 Search in Google Scholar

Osmolovskaya, N., Shumilina, J., Kim, A., Didio, A., Grishina, T., Bilova, T., Keltsieva, O.A., Zhukov, V., Tikhonovich, I., Tarakhovskaya, E., Frolov, A. and L.A. Wess-johann (2018): Methodology of Drought Stress Research: Experimental Setup and Physiological Characterization. International Journal of Molecular Sciences 19. OsmolovskayaN. ShumilinaJ. KimA. DidioA. GrishinaT. BilovaT. KeltsievaO.A. ZhukovV. TikhonovichI. TarakhovskayaE. FrolovA. Wess-johannL.A. 2018 Methodology of Drought Stress Research: Experimental Setup and Physiological Characterization International Journal of Molecular Sciences 19 10.3390/ijms19124089632115330563000 Search in Google Scholar

Otegui, M.S. (2018): ESCRT-mediated sorting and intralumenal vesicle concatenation in plants. Biochemical Society transactions 46, 537–545. OteguiM.S. 2018 ESCRT-mediated sorting and intralumenal vesicle concatenation in plants Biochemical Society transactions 46 537 545 10.1042/BST2017043929666213 Search in Google Scholar

Paez Valencia, J., Goodman, K. and M.S. Otegui (2016): Endocytosis and Endosomal Trafficking in Plants. Annual Review of Plant Biology 67, 309–335. Paez ValenciaJ. GoodmanK. OteguiM.S. 2016 Endocytosis and Endosomal Trafficking in Plants Annual Review of Plant Biology 67 309 335 10.1146/annurev-arplant-043015-11224227128466 Search in Google Scholar

Pashkova, N., Gakhar, L., Winistorfer, S.C., Sunshine, A.B., Rich, M., Dunham, M.J., Yu, L. and R.C. Piper (2013): The yeast Alix homolog Bro1 functions as a ubiquitin receptor for protein sorting into multivesicular endosomes. Developmental Cell 25, 520–533. PashkovaN. GakharL. WinistorferS.C. SunshineA.B. RichM. DunhamM.J. YuL. PiperR.C. 2013 The yeast Alix homolog Bro1 functions as a ubiquitin receptor for protein sorting into multivesicular endosomes Developmental Cell 25 520 533 10.1016/j.devcel.2013.04.007375575623726974 Search in Google Scholar

Piper, R.C., Dikic, I. and G.L. Lukacs (2014): Ubiquitin-dependent sorting in endocytosis. Cold Spring Harbor perspectives in biology 6. PiperR.C. DikicI. LukacsG.L. 2014 Ubiquitin-dependent sorting in endocytosis Cold Spring Harbor perspectives in biology 6 10.1101/cshperspect.a016808394121524384571 Search in Google Scholar

Raiborg, C. and H. Stenmark (2009): The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445–452. RaiborgC. StenmarkH. 2009 The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins Nature 458 445 452 10.1038/nature0796119325624 Search in Google Scholar

Reynolds, G.D., Wang, C., Pan, J. and S.Y. Bednarek (2018): Inroads into Internalization: Five Years of Endocytic Exploration. Plant Physiology 176, 208–218. ReynoldsG.D. WangC. PanJ. BednarekS.Y. 2018 Inroads into Internalization: Five Years of Endocytic Exploration Plant Physiology 176 208 218 10.1104/pp.17.01117576181329074601 Search in Google Scholar

Richardson, L.G.L., Howard, A.S.M., Khuu, N., Gidda, S.K., McCartney, A., Morphy, B.J. and R.T. Mullen (2011): Protein–protein interaction network and sub-cellular localization of the Arabidopsis thaliana ESCRT machinery. Frontiers in Plant Science 2, 1–14. RichardsonL.G.L. HowardA.S.M. KhuuN. GiddaS.K. McCartneyA. MorphyB.J. MullenR.T. 2011 Protein–protein interaction network and sub-cellular localization of the Arabidopsis thaliana ESCRT machinery Frontiers in Plant Science 2 1 14 10.3389/fpls.2011.00020335572122639582 Search in Google Scholar

Robinson, D.G. and J.M. Neuhaus (2016): Receptor-mediated sorting of soluble vacuolar proteins: myths, facts, and a new model. Journal of Experimental Botany 67, 4435–4449. RobinsonD.G. NeuhausJ.M. 2016 Receptor-mediated sorting of soluble vacuolar proteins: myths, facts, and a new model Journal of Experimental Botany 67 4435 4449 10.1093/jxb/erw22227262127 Search in Google Scholar

Robinson, D.G., Jiang, L. and K. Schumacher (2008): The endosomal system of plants: charting new and familiar territories. Plant physiology 147, 1482–1492. RobinsonD.G. JiangL. SchumacherK. 2008 The endosomal system of plants: charting new and familiar territories Plant physiology 147 1482 1492 10.1104/pp.108.120105249261018678740 Search in Google Scholar

Robinson, M.S. (2015): Forty Years of Clathrin-coated Vesicles. Traffic 16, 1210–1238. RobinsonM.S. 2015 Forty Years of Clathrin-coated Vesicles Traffic 16 1210 1238 10.1111/tra.1233526403691 Search in Google Scholar

Rodriguez, L., Gonzalez-Guzman, M., Diaz, M., Rodrigues, A., Izquierdo-Garcia, A.C., Peirats-Llobet, M., Fernandez, M.A., Antoni, R., Fernandez, D., Marquez, J.A., Mulet, J.M., Albert, A. and P.L. Rodriguez (2014): C2-domain abscisic acid-related proteins mediate the interaction of PYR/PYL/RCAR abscisic acid receptors with the plasma membrane and regulate abscisic acid sensitivity in Arabidopsis. The Plant Cell 26, 4802–4820. RodriguezL. Gonzalez-GuzmanM. DiazM. RodriguesA. Izquierdo-GarciaA.C. Peirats-LlobetM. FernandezM.A. AntoniR. FernandezD. MarquezJ.A. MuletJ.M. AlbertA. RodriguezP.L. 2014 C2-domain abscisic acid-related proteins mediate the interaction of PYR/PYL/RCAR abscisic acid receptors with the plasma membrane and regulate abscisic acid sensitivity in Arabidopsis The Plant Cell 26 4802 4820 10.1105/tpc.114.129973431119525465408 Search in Google Scholar

Rodriguez-Furlan, C., Minina, E.A. and G.R. Hicks (2019): Remove, Recycle, Degrade: Regulating Plasma Membrane Protein Accumulation. The Plant Cell 31, 2833–2854. Rodriguez-FurlanC. MininaE.A. HicksG.R. 2019 Remove, Recycle, Degrade: Regulating Plasma Membrane Protein Accumulation The Plant Cell 31 2833 2854 10.1105/tpc.19.00433692500431628169 Search in Google Scholar

Romero-Barrios, N. and G. Vert (2018): Proteasome-independent functions of lysine-63 polyubiquitination in plants. The New Phytologist 217, 995–1011. Romero-BarriosN. VertG. 2018 Proteasome-independent functions of lysine-63 polyubiquitination in plants The New Phytologist 217 995 1011 10.1111/nph.1491529194634 Search in Google Scholar

Ron, M. and A. Avni (2004): The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. The Plant Cell 16, 1604–1615. RonM. AvniA. 2004 The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato The Plant Cell 16 1604 1615 10.1105/tpc.02247549004915155877 Search in Google Scholar

Sancho-Andres, G., Soriano-Ortega, E., Gao, C., Bernabe-Orts, J.M., Narasimhan, M., Muller, A.O., Tejos, R., Jiang, L., Friml, J., Aniento, F. and M.J. Marcote (2016): Sorting Motifs Involved in the Trafficking and Localization of the PIN1 Auxin Efflux Carrier. Plant Physiology 171, 1965–1982. Sancho-AndresG. Soriano-OrtegaE. GaoC. Bernabe-OrtsJ.M. NarasimhanM. MullerA.O. TejosR. JiangL. FrimlJ. AnientoF. MarcoteM.J. 2016 Sorting Motifs Involved in the Trafficking and Localization of the PIN1 Auxin Efflux Carrier Plant Physiology 171 1965 1982 10.1104/pp.16.00373493656827208248 Search in Google Scholar

Sandvig, K., Kavaliauskiene, S. and T. Skotland (2018): Clathrin-independent endocytosis: an increasing degree of complexity. Histochemistry and Cell Biology 150, 107–118. SandvigK. KavaliauskieneS. SkotlandT. 2018 Clathrin-independent endocytosis: an increasing degree of complexity Histochemistry and Cell Biology 150 107 118 10.1007/s00418-018-1678-5609656429774430 Search in Google Scholar

Sauer, M. and J. Friml (2014): Plant biology: gatekeepers of the road to protein perdition. Current Biology : CB 24, R27–29. SauerM. FrimlJ. 2014 Plant biology: gatekeepers of the road to protein perdition Current Biology : CB 24 R27 29 10.1016/j.cub.2013.11.01924405674 Search in Google Scholar

Schuh, A.L. and Audhya, A. (2014): The ESCRT machinery: from the plasma membrane to endosomes and back again. Critical Reviews in Biochemistry and Molecular Biology 49, 242–261. SchuhA.L. AudhyaA. 2014 The ESCRT machinery: from the plasma membrane to endosomes and back again Critical Reviews in Biochemistry and Molecular Biology 49 242 261 10.3109/10409238.2014.881777438196324456136 Search in Google Scholar

Schwihla, M. and B. Korbei (2020): The Beginning of the End: Initial Steps in the Degradation of Plasma Membrane Proteins. Frontiers in Plant Science 11, 680. SchwihlaM. KorbeiB. 2020 The Beginning of the End: Initial Steps in the Degradation of Plasma Membrane Proteins Frontiers in Plant Science 11 680 10.3389/fpls.2020.00680725369932528512 Search in Google Scholar

Shi, H., Chen, Y., Qian, Y. and Z. Chan (2015): Low Temperature-Induced 30 (LTI30) positively regulates drought stress resistance in Arabidopsis: effect on abscisic acid sensitivity and hydrogen peroxide accumulation. Frontiers in Plant Science 6, 893. ShiH. ChenY. QianY. ChanZ. 2015 Low Temperature-Induced 30 (LTI30) positively regulates drought stress resistance in Arabidopsis: effect on abscisic acid sensitivity and hydrogen peroxide accumulation Frontiers in Plant Science 6 893 10.3389/fpls.2015.00893461117526539205 Search in Google Scholar

Shields, S.B. and R.C. Piper (2011): How ubiquitin functions with ESCRTs. Traffic 12, 1306–1317. ShieldsS.B. PiperR.C. 2011 How ubiquitin functions with ESCRTs Traffic 12 1306 1317 10.1111/j.1600-0854.2011.01242.x317164621722280 Search in Google Scholar

Spallek, T., Beck, M., Ben Khaled, S., Salomon, S., Bourdais, G., Schellmann, S. and S. Robatzek (2013): ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLoS genetics 9, e1004035. SpallekT. BeckM. Ben KhaledS. SalomonS. BourdaisG. SchellmannS. RobatzekS. 2013 ESCRT-I mediates FLS2 endosomal sorting and plant immunity PLoS genetics 9 e1004035 10.1371/journal.pgen.1004035387322924385929 Search in Google Scholar

Spitzer, C., Schellmann, S., Sabovljevic, A., Shahriari, M., Keshavaiah, C., Bechtold, N., Herzog, M., Muller, S., Hanisch, F.G. and M. Hulskamp (2006): The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133, 4679–4689. SpitzerC. SchellmannS. SabovljevicA. ShahriariM. KeshavaiahC. BechtoldN. HerzogM. MullerS. HanischF.G. HulskampM. 2006 The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis Development 133 4679 4689 10.1242/dev.0265417090720 Search in Google Scholar

Stewart, M.D., Ritterhoff, T., Klevit, R.E. and P.S. Brzovic (2016): E2 enzymes: more than just middle men. Cell Research 26, 423–440. StewartM.D. RitterhoffT. KlevitR.E. BrzovicP.S. 2016 E2 enzymes: more than just middle men Cell Research 26 423 440 10.1038/cr.2016.35482213027002219 Search in Google Scholar

Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., Onouchi, H., Naito, S. and T. Fujiwara (2010): Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proceedings of the National Academy of Sciences of the United States of America 107, 5220–5225. TakanoJ. TanakaM. ToyodaA. MiwaK. KasaiK. FujiK. OnouchiH. NaitoS. FujiwaraT. 2010 Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways Proceedings of the National Academy of Sciences of the United States of America 107 5220 5225 10.1073/pnas.0910744107284193420194745 Search in Google Scholar

Teo, H., Perisic, O., Gonzalez, B. and R.L. Williams (2004): ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Developmental Cell 7, 559–569. TeoH. PerisicO. GonzalezB. WilliamsR.L. 2004 ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes Developmental Cell 7 559 569 10.1016/j.devcel.2004.09.00315469844 Search in Google Scholar

Tomanov, K., Luschnig, C. and A. Bachmair (2014): Ubiquitin Lys 63 chains - second-most abundant, but poorly understood in plants. Frontiers in Plant Science 5, 15. TomanovK. LuschnigC. BachmairA. 2014 Ubiquitin Lys 63 chains - second-most abundant, but poorly understood in plants Frontiers in Plant Science 5 15 10.3389/fpls.2014.00015390771524550925 Search in Google Scholar

Traub, L.M. (2009): Tickets to ride: selecting cargo for clathrin-regulated internalization. Nature Reviews. Molecular Cell Biology 10, 583–596. TraubL.M. 2009 Tickets to ride: selecting cargo for clathrin-regulated internalization. Nature Reviews Molecular Cell Biology 10 583 596 Search in Google Scholar

Traub, L.M. and J.S. Bonifacino (2013): Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harbor Perspectives in Biology 5, a016790. TraubL.M. BonifacinoJ.S. 2013 Cargo recognition in clathrin-mediated endocytosis Cold Spring Harbor Perspectives in Biology 5 a016790 10.1101/cshperspect.a016790380957724186068 Search in Google Scholar

Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., Kitomi, Y., Inukai, Y., Ono, K., Kanno, N., Inoue, H., Takehisa, H., Motoyama, R., Nagamura, Y., Wu, J., Matsumoto, T., Takai, T., Okuno, K. and M. Yano (2013): Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics 45, 1097–1102. UgaY. SugimotoK. OgawaS. RaneJ. IshitaniM. HaraN. KitomiY. InukaiY. OnoK. KannoN. InoueH. TakehisaH. MotoyamaR. NagamuraY. WuJ. MatsumotoT. TakaiT. OkunoK. YanoM. 2013 Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions Nature Genetics 45 1097 1102 10.1038/ng.272523913002 Search in Google Scholar

Vaidya, A.S., Helander, J.D.M., Peterson, F.C., Elzinga, D., Dejonghe, W., Kaundal, A., Park, S.Y., Xing, Z., Mega, R., Takeuchi, J., Khanderahoo, B., Bishay, S., Volkman, B.F., Todoroki, Y., Okamoto, M. and S.R. Cutler (2019): Dynamic control of plant water use using designed ABA receptor agonists. Science 366. VaidyaA.S. HelanderJ.D.M. PetersonF.C. ElzingaD. DejongheW. KaundalA. ParkS.Y. XingZ. MegaR. TakeuchiJ. KhanderahooB. BishayS. VolkmanB.F. TodorokiY. OkamotoM. CutlerS.R. 2019 Dynamic control of plant water use using designed ABA receptor agonists Science 366 10.1126/science.aaw884831649167 Search in Google Scholar

VanWallendael, A., Soltani, A., Emery, N.C., Peixoto, M.M., Olsen, J. and D.B. Lowry (2019): A Molecular View of Plant Local Adaptation: Incorporating Stress-Response Networks. Annual Review of Plant Biology 70, 559–583. VanWallendaelA. SoltaniA. EmeryN.C. PeixotoM.M. OlsenJ. LowryD.B. 2019 A Molecular View of Plant Local Adaptation: Incorporating Stress-Response Networks Annual Review of Plant Biology 70 559 583 10.1146/annurev-arplant-050718-10011430786237 Search in Google Scholar

Vierstra, R.D. (2012): The Expanding Universe of Ubiquitin and Ubiquitin-Like Modifiers. Plant Physiology 160, 2–14. VierstraR.D. 2012 The Expanding Universe of Ubiquitin and Ubiquitin-Like Modifiers Plant Physiology 160 2 14 10.1104/pp.112.200667344019822693286 Search in Google Scholar

Vietri, M., Radulovic, M. and H. Stenmark (2020): The many functions of ESCRTs. Nature reviews. Molecular Cell Biology 21, 25–42. VietriM. RadulovicM. StenmarkH. 2020 The many functions of ESCRTs. Nature reviews Molecular Cell Biology 21 25 42 Search in Google Scholar

Viotti, C., Bubeck, J., Stierhof, Y.D., Krebs, M., Langhans, M., van den Berg, W., van Dongen, W., Richter, S., Geldner, N., Takano, J., Jurgens, G., de Vries, S.C., Robinson, D.G. and K. Schumacher (2010): Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. The Plant Cell 22, 1344–1357. ViottiC. BubeckJ. StierhofY.D. KrebsM. LanghansM. van den BergW. van DongenW. RichterS. GeldnerN. TakanoJ. JurgensG. de VriesS.C. RobinsonD.G. SchumacherK. 2010 Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle The Plant Cell 22 1344 1357 10.1105/tpc.109.072637287974120435907 Search in Google Scholar

Waltz, E. (2014): Beating the heat. Nature Biotechnology 32, 610–613. WaltzE. 2014 Beating the heat Nature Biotechnology 32 610 613 10.1038/nbt.294825004222 Search in Google Scholar

Wang, F., Shang, Y.F., Fan, B.F., Yu, J.Q., and Z.X. Chen (2014): Arabidopsis LIP5, a Positive Regulator of Multivesicular Body Biogenesis, Is a Critical Target of Pathogen-Responsive MAPK Cascade in Plant Basal Defense. PLoS pathogens 10. WangF. ShangY.F. FanB.F. YuJ.Q. ChenZ.X. 2014 Arabidopsis LIP5, a Positive Regulator of Multivesicular Body Biogenesis, Is a Critical Target of Pathogen-Responsive MAPK Cascade in Plant Basal Defense PLoS pathogens 10 10.1371/journal.ppat.1004243409213725010425 Search in Google Scholar

Wang, F., Yang, Y., Wang, Z., Zhou, J., Fan, B.F. and Z.X. Chen (2015): A Critical Role of Lyst-Interacting Protein5, a Positive Regulator of Multivesicular Body Biogenesis, in Plant Responses to Heat and Salt Stresses. Plant Physiology 169, 497–+. WangF. YangY. WangZ. ZhouJ. FanB.F. ChenZ.X. 2015 A Critical Role of Lyst-Interacting Protein5, a Positive Regulator of Multivesicular Body Biogenesis, in Plant Responses to Heat and Salt Stresses Plant Physiology 169 497 +. 10.1104/pp.15.00518457739426229051 Search in Google Scholar

Wang, H.J., Hsu, Y.W., Guo, C.L., Jane, W.N., Wang, H., Jiang, L. and G.Y. Jauh (2017): VPS36-Dependent Multivesicular Bodies Are Critical for Plasmamembrane Protein Turnover and Vacuolar Biogenesis. Plant Physiology 173, 566–581. WangH.J. HsuY.W. GuoC.L. JaneW.N. WangH. JiangL. JauhG.Y. 2017 VPS36-Dependent Multivesicular Bodies Are Critical for Plasmamembrane Protein Turnover and Vacuolar Biogenesis Plant Physiology 173 566 581 10.1104/pp.16.01356521073627879389 Search in Google Scholar

Wang, T., Liu, N.S., Seet, L.F. and W. Hong (2010): The emerging role of VHS domain-containing Tom1, Tom1L1 and Tom1L2 in membrane trafficking. Traffic 11, 1119–1128. WangT. LiuN.S. SeetL.F. HongW. 2010 The emerging role of VHS domain-containing Tom1, Tom1L1 and Tom1L2 in membrane trafficking Traffic 11 1119 1128 10.1111/j.1600-0854.2010.01098.x20604899 Search in Google Scholar

Winter, V. and M.T. Hauser (2006): Exploring the ESCRTing machinery in eukaryotes. Trends in Plant Science 11, 115–123. WinterV. HauserM.T. 2006 Exploring the ESCRTing machinery in eukaryotes Trends in Plant Science 11 115 123 10.1016/j.tplants.2006.01.008286599216488176 Search in Google Scholar

Xia, Z.L., Wei, Y.Y., Sun, K.L., Wu, J.Y., Wang, Y.X. and K. Wu (2013): The Maize AAA-Type Protein SKD1 Confers Enhanced Salt and Drought Stress Tolerance in Transgenic Tobacco by Interacting with Lyst-Interacting Protein 5. PloS one 8. XiaZ.L. WeiY.Y. SunK.L. WuJ.Y. WangY.X. WuK. 2013 The Maize AAA-Type Protein SKD1 Confers Enhanced Salt and Drought Stress Tolerance in Transgenic Tobacco by Interacting with Lyst-Interacting Protein 5 PloS one 8 10.1371/journal.pone.0069787372215723894539 Search in Google Scholar

Xie, Q., Essemine, J., Pang, X., Chen, H., Jin, J. and W. Cai (2021): Abscisic Acid Regulates the Root Growth Trajectory by Reducing Auxin Transporter PIN2 Protein Levels in Arabidopsis thaliana. Frontiers in Plant Science 12. XieQ. EssemineJ. PangX. ChenH. JinJ. CaiW. 2021 Abscisic Acid Regulates the Root Growth Trajectory by Reducing Auxin Transporter PIN2 Protein Levels in Arabidopsis thaliana Frontiers in Plant Science 12 10.3389/fpls.2021.632676798291833763094 Search in Google Scholar

Yamaguchi-Shinozaki, K. and K. Shinozaki (2006): Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781–803. Yamaguchi-ShinozakiK. ShinozakiK. 2006 Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses Annual Review of Plant Biology 57 781 803 10.1146/annurev.arplant.57.032905.10544416669782 Search in Google Scholar

Yoshinari, A., Korbei, B. and J. Takano (2018): TOL proteins mediate vacuolar sorting of the borate transporter BOR1 in Arabidopsis thaliana. Soil Science and Plant Nutrition, 1–8. YoshinariA. KorbeiB. TakanoJ. 2018 TOL proteins mediate vacuolar sorting of the borate transporter BOR1 in Arabidopsis thaliana Soil Science and Plant Nutrition 1 8 10.1080/00380768.2018.1504322 Search in Google Scholar

Yu, F. and Q. Xie (2017): Non-26S Proteasome Endo-membrane Trafficking Pathways in ABA Signaling. Trends in Plant Science 22, 976–985. YuF. XieQ. 2017 Non-26S Proteasome Endo-membrane Trafficking Pathways in ABA Signaling Trends in Plant Science 22 976 985 10.1016/j.tplants.2017.08.00928919033 Search in Google Scholar

Yu, F., Lou, L., Tian, M., Li, Q., Ding, Y., Cao, X., Wu, Y., Belda-Palazon, B., Rodriguez, P.L., Yang, S. and Q. Xie (2016): ESCRT-I Component VPS23A Affects ABA Signaling by Recognizing ABA Receptors for Endosomal Degradation. Molecular Plant 9, 1570–1582. YuF. LouL. TianM. LiQ. DingY. CaoX. WuY. Belda-PalazonB. RodriguezP.L. YangS. XieQ. 2016 ESCRT-I Component VPS23A Affects ABA Signaling by Recognizing ABA Receptors for Endosomal Degradation Molecular Plant 9 1570 1582 10.1016/j.molp.2016.11.00227856401 Search in Google Scholar

Zhang, Q. (2007): Strategies for developing Green Super Rice. Proceedings of the National Academy of Sciences of the United States of America 104, 16402–16409. ZhangQ. 2007 Strategies for developing Green Super Rice Proceedings of the National Academy of Sciences of the United States of America 104 16402 16409 10.1073/pnas.0708013104203424617923667 Search in Google Scholar

Zhang, X.Q., Hou, P., Zhu, H.T., Li, G.D., Liu, X.G. and X.M. Xie (2013): Knockout of the VPS22 component of the ESCRT-II complex in rice (Oryza sativa L.) causes chalky endosperm and early seedling lethality. Molecular Biology Reports 40, 3475–3481. ZhangX.Q. HouP. ZhuH.T. LiG.D. LiuX.G. XieX.M. 2013 Knockout of the VPS22 component of the ESCRT-II complex in rice (Oryza sativa L.) causes chalky endosperm and early seedling lethality Molecular Biology Reports 40 3475 3481 10.1007/s11033-012-2422-123275199 Search in Google Scholar

Zhang, Y., Persson, S., Hirst, J., Robinson, M.S., van Damme, D. and C. Sanchez-Rodriguez (2015): Change your TPLATE, change your fate: plant CME and beyond. Trends in Plant Science 20, 41–48. ZhangY. PerssonS. HirstJ. RobinsonM.S. van DammeD. Sanchez-RodriguezC. 2015 Change your TPLATE, change your fate: plant CME and beyond Trends in Plant Science 20 41 48 10.1016/j.tplants.2014.09.00225278268 Search in Google Scholar

Zhao, J., Zhao, L., Zhang, M., Zafar, S.A., Fang, J., Li, M., Zhang, W. and X. Li (2017): Arabidopsis E3 Ubiquitin Ligases PUB22 and PUB23 Negatively Regulate Drought Tolerance by Targeting ABA Receptor PYL9 for Degradation. International Journal of Molecular Sciences 18. ZhaoJ. ZhaoL. ZhangM. ZafarS.A. FangJ. LiM. ZhangW. LiX. 2017 Arabidopsis E3 Ubiquitin Ligases PUB22 and PUB23 Negatively Regulate Drought Tolerance by Targeting ABA Receptor PYL9 for Degradation International Journal of Molecular Sciences 18 10.3390/ijms18091841561849028837065 Search in Google Scholar

Zhu, J.K. (2002): Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273. ZhuJ.K. 2002 Salt and drought stress signal transduction in plants Annual Review of Plant Biology 53 247 273 10.1146/annurev.arplant.53.091401.143329312834812221975 Search in Google Scholar

Articles recommandés par Trend MD

Planifiez votre conférence à distance avec Sciendo