Biomass partitioning is one of the pivotal determinants of crop growth management, which is influenced by environmental cues. Light and CO2 are the main drivers of photosynthesis and biomass production in plants. In this study, the effects of CO2 levels: ambient 400 ppm (a[CO2]) and elevated to 1,000 ppm (e[CO2]) and different light intensities (75, 150, 300, 600 μmol·m−2·s−1 photosynthetic photon flux density – PPFD) were studied on the growth, yield, and biomass partitioning in chrysanthemum plants. The plants grown at higher light intensity had a higher dry weight (DW) of both the vegetative and floral organs. e[CO2] diminished the stimulating effect of more intensive light on the DW of vegetative organs, although it positively influenced inflorescence DW. The flowering time in plants grown at e[CO2] and light intensity of 600 μmol·m−2·s−1 occurred earlier than that of plants grown at a[CO2]. An increase in light intensity induced the allocation of biomass to inflorescence and e[CO2] enhanced the increasing effect of light on the partitioning of biomass toward the inflorescence. In both CO2 concentrations, the highest specific leaf area (SLA) was detected under the lowest light intensity, especially in plants grown at e[CO2]. In conclusion, elevated light intensity and CO2 direct the biomass toward inflorescence in chrysanthemum plants.
- biomass allocation
- dry weight
- flowering time
- inflorescence characteristic
- water use efficiency
Chrysanthemum is a short-day flowering plant belonging to the Asteraceae family (Arora 2012). It is one of the most popular ornamental plants and the second economically important cut flower in the world (Teixeira da Silva 2004). It is also used as potted and landscape plant (Liu et al. 2010). The production of chrysanthemum is one of the most intensive and controlled horticultural production systems, requiring the control of several growing conditions (Machin 1996; Carvalho & Heuvelink 2001).
There is ample evidence that the quality, intensity, and duration of light influence photosynthesis, biomass accumulation, flowering time, and the quality in many horticultural crops (Van Ieperen 2012; Demotes-Mainard et al. 2016; Zheng et al. 2019). The effect of light intensity and quality on chrysanthemum has also been shown in previous reports (Cockshull & Hughes 1971; Wang et al. 2009; Dierck et al. 2017; Kumar et al. 2017; Nissim-Levi et al. 2019).
Photosynthesis saturation of C3 plants requires 800–1,000 ppm CO2 (Stitt 1991), while the ambient concentration (a[CO2]) is about 400 ppm, therefore, commercial producers elevate the CO2 level to improve crop biomass and productivity (Högy et al. 2009; Hasegawa et al. 2013) and to regulate the time of flowering (Reekie et al. 1994; López-Cubillos & Hughes 2016; Kobayasi et al. 2019). The elevation of CO2 is defined as “CO2 fertilization”; it has been shown to increase biomass by 50% in C3 plants (Prior et al. 2005), 35% in Crassulacean acid metabolism (CAM) plants (Drennan & Nobel 2000), and 12% in C4 plants (Poorter & Navas 2003). However, there are divergent reports on the effect of elevated CO2 concentration (e[CO2]) on different plant species (Croonenborghs et al. 2009). It was found that environmental factors, including nitrogen (Robinson et al. 2012) and other elements (De Graaff et al. 2006; Lotfiomran et al. 2016), temperature (Lee 2011; Madan et al. 2012; Kumari et al. 2019), water availability (Madhu & Hatfield 2015), air pollutants (Volin & Reich 1996), drought (Miranda-Apodaca et al. 2018), and light (Kerstiens 2001; Pérez-López et al. 2015) determine the magnitude of plant response to e[CO2]. Naing et al. (2016) suggested an interaction between supplemental lighting and e[CO2] of the rose, and reported that the greatest increase in growth rate was achieved when e[CO2] was applied together with additional lightning (Naing et al. 2016). The same results were also obtained in the growth of seedlings and the yield of tomatoes and peppers by both e[CO2] and higher light intensity (Fierro et al. 1994). However, there is a lack of information regarding biomass partitioning under simultaneous increase in light intensity and CO2 fertilization. Therefore, this research aimed to investigate the interactive effects of light intensity and e[CO2] on growth, flowering, and biomass partitioning of chrysanthemum to achieve high-quality flowering in a shorter time.
Rooted cuttings (~9 cm stem length with 3–4 leaves) of cut chrysanthemum (
A combination of 3:1 red and blue light-emitting diodes (LEDs) with peaks at 600–685 nm for red and 415–500 nm for blue LEDs was used for application of different light intensities in the growth chambers. These LED light panels (24 W, Iran Grow Light) were used to limit the production of heat by the light sources. The same combination of red and blue LEDs was used in all the growth chambers, since based on the previous reports they are the main light spectra for photosynthesis and growth of plants. The photo-period was set at 12 h/12 h light/dark periods.
To supply high CO2 concentration, a CO2 cylinder that was equipped with a manometer, electric valve, and the digital timer was used. The cylinder outlet pressure was adjusted thrice using a pressure gauge connected to a timer resulting in injecting the CO2 into the air every 2 min, and the CO2 concentration was recorded using a CO2 sensor equipped with a data logger (Trotec, BZ30, Germany).
After three months of plant growth at different light intensity and CO2 concentration, growth and morphological characteristics, such as leaf and inflorescence number, fresh and dry weights (DWs) of above-ground parts and roots, were analyzed. The specific leaf area (SLA) of each plant was calculated using the following equation:
The flowering time was recorded based on the emergence of flower buds. The accumulation of biomass in the various plant organs was calculated by the DW measured at the end of the production cycle. To do so, plants were harvested, the different parts were separated, and, after measuring the fresh weight, their DWs were recorded after reaching a constant weight for 3 days at 80 °C. Measurements included final dry weight of organs including leaf, stem, inflorescence, and root.
To determine the water use efficiency (WUE), the total amount of water consumed by the plants during the growth period was recorded. Under greenhouse conditions, the relationship between soil water evaporation and plant transpiration is inseparable (Ma et al. 2013). In our experiment, the total amount of water consumed by the plants was measured by subtracting the amount of water evaporated from the substrate in the absence of plants from the amount of water used for irrigation (Polley et al. 1996). To schedule the proper time and amount of water, irrigation was applied when 30% of water was taken from the pots.
This value was represented by “easily obtained water” (the amount of water retained by the fully irrigated substrate following 24 h). The soil was irrigated when the soil water content was lower than the amount of easily obtained water. WUE was calculated as the ratio of DW of the above-ground parts (including stem, leaf, inflorescence, and flowers) to the amount of water that was taken by the plants.
Six plants were used as six replicates in each treatment. Each plant was taken as an independent replicate. The data were subjected to two-way analysis of variance (ANOVA) and Duncan's test was used as a post-test; p > 0.05 was considered as not significant.
The DW of the above-ground parts increased gradually with increasing the light intensity in plants grown at a[CO2]. Plants grown at 600 μmol·m−2·s−1 showed the maximum DW of above-ground parts. These plants had four times higher DW of aboveground parts than those obtained in plants grown at 75 μmol·m−2·s−1 (Fig. 1A). In e[CO2], there was a more than twofold increase in DW of aboveground parts of plants grown at 600 μmol·m−2·s−1 compared to DW of above-ground parts of the plants grown at lower light intensity.
Increase in light intensity resulted in a gradual increase in leaf DW and in the number of leaves only in plants grown at a[CO2]. The maximum leaf DW and the number of leaves were obtained in plants grown at 600 μmol·m−2·s−1. In these plants, there were three times higher leaf DW and five times more leaves than those in plants grown at 75 μmol·m−2·s−1. However, e[CO2] eliminated the stimulating effect of increasing light intensity on the studied parameters (Fig. 1B–C).
The SLA of plants grown at 75 μmol·m−2·s−1 and exposed to e[CO2] was significantly higher than SLA of plants exposed to higher light intensities irrespective of CO2 level (Fig. 1D). At light intensities higher than 75 μmol·m−2·s−1, there was no significant difference among the light intensity or CO2 level.
A drastic increase in the DW of the roots was observed with the increase in the light intensity from 75 to 600 μmol·m−2·s−1. The DW of the roots of plants grown at 600 μmol·m−2·s−1 was more than 13 times higher than those grown at 75 μmol·m−2·s−1 and a[CO2] and 5 times higher at e[CO2]. Also, a drastic reduction in the DW of the roots was observed in plants grown at intensity of 300 μmol·m−2·s−1 and e[CO2] comparing with plants grown at a[CO2] (Figs. 2A and 3).
The inflorescence DW increased with increasing light intensity; although at a[CO2], no differences were found between 75 and 150 as well as between 300 and 600 μmol·m−2·s−1. At e[CO2], plants grown at 600 μmol·m−2·s−1 had the highest DW of inflorescence. The DW inflorescence of these plants was 14 times higher than the inflorescence DW of plants grown at 75 μmol·m−2·s−1 and in e[CO2] and 35 times higher when the plants were grown in a[CO2] (Fig. 2B). In plants grown at 600 μmol·m−2·s−1, exposure to e[CO2] resulted in approximately three times higher inflorescence DW than in the plants grown at a[CO2].
The number of inflorescences increased with increasing light intensity; this effect was more visible at a[CO2]. In plants grown at e[CO2], there was no significant difference between the number of inflorescences at 75, 150, and 300 μmol·m−2·s−1, while e[CO2] doubled the number of inflorescences in plants grown at 600 μmol·m−2·s−1 (Fig. 2C and 4).
The time of flowering was positively influenced by both the light intensity and the level of CO2. The number of days to flowering decreased gradually with increasing light intensity (Fig. 2D). The transition to the generative phase was accelerated (45% earlier) by increasing the light intensity from 75 to 600 μmol·m−2·s−1 in plants grown under a[CO2]. Enrichment with CO2 caused the further acceleration of flowering (53% earlier than at a[CO2]), by increasing the light intensity from 75 to 600 μmol·m−2·s−1 (Figs. 2D and 4).
The accumulation of biomass (stem, leaf, flower, and root) increased in proportion to the increasing light intensity. Comparison of biomass production under each of the light intensity showed that e[CO2] diminish the accumulation of biomass compared with a[CO2]. This effect was more pronounced with an increase in the light intensity from 75 to 300 μmol·m−2·s−1, which resulted in a 9% and 69% reduction in biomass of plants grown at 75 and 300 μmol·m−2·s−1, respectively (Fig. 5). These results indicate that plants grown under low light intensities respond better to e[CO2] and an increase in light intensity reduces the stimulating effect of CO2, which indicates resistance to the physiological effect of light on the accumulation of biomass (Fig. 5).
Both the increase in the light intensity and the CO2 level increased the share of biomass of inflorescence at the expense of the amount of leaf bio-mass (Fig. 6). As the light intensity increased, a gradual increase in the inflorescence was observed. The biomass of inflorescence of plants grown at 600 μmol·m−2·s−1 was about five times higher than that of plants grown at 75 μmol·m−2·s−1. In addition, the root biomass also increased with the increase in light intensity and the maximum root biomass was observed in plants grown at 600 μmol·m−2·s−1, showing a twice higher biomass accumulation compared with plants grown at 75 μmol·m−2·s−1 and at a[CO2]. In contrast, a downward trend in the leaves biomass was observed with increasing light intensity, which shows a reduction of leaf biomass by 47.35% in plants grown at 600 μmol·m−2·s−1 compared with those at 75 μmol·m−2·s−1 (Fig. 6). The biomass of inflorescence at the highest light intensity was three times greater than that of plants grown at 75 μmol·m−2·s−1, which is less than five times the increase at a[CO2] at the same light intensities (Fig. 6). An increase in root biomass in response to the increase in light intensity was not observed in plants grown at e[CO2] (Fig. 6). Moreover, at e[CO2], a drastic reduction of the leaf biomass of plants at 75 μmol·m−2·s−1 compared to plants grown at 600 μmol·m−2·s−1, was observed, showing a stronger reduction compared to the reduction of leaf biomass at the same light intensity and at a[CO2] (Fig. 6). Considering the influence of e[CO2] on the allocation of biomass at each light intensity, the biomass of inflorescences increased, and the biomass of leaves decreased with increasing CO2 concentration (Fig. 6).
Different light intensities and CO2 concentrations significantly affected WUE (Fig. 7). The WUE value increased 5 times and 4.7 times under a[CO2] and e[CO2], respectively, when light intensity increased from 75 μmol·m−2·s−1 to 600 μmol·m−2·s−1. Considering the impact of CO2 concentration regardless of light intensity, e[CO2] reduced the WUE value the strongest at 300 μmol·m−2·s−1 compared to other light intensities (Fig. 7).
In the present study, a positive effect of light intensity and increased level of CO2 on the dry weight of inflorescences was observed. This finding is in agreement with the results of a previous study on rose plants that showed an increase in fresh weight of inflorescences when the plants are ex-posed to a combination of e[CO2] and additional lighting (Naing et al. 2016). These authors postulated that an increase in water use efficiency enhanced the photosynthesis rate in the modified atmosphere and led to the provision of more carbo-hydrates utilized in flowering and flower development. Moreover, supplementary lightning increases the fresh weight of flowers by reducing the number of blind flowers in
In our experiment, the number of inflorescences increased with increasing light intensity under ambient CO2 level but CO2 elevation diminished the effect of higher light intensity. These results are in agreement with another study that showed the effect of e[CO2] and light intensity on the production and quality of flower stems in
In our research, an increase in light intensity and CO2 concentration accelerated flowering. In contrast, e[CO2] was reported to delay flowering in four short-day species, however, in long-day species flower bud initiation was promoted in response to e[CO2] (Reekie et al. 1994).
Leaf DW was affected by both CO2 concentration and light intensity, so that the leaf DW increased with increasing light intensity in plants that were exposed to a[CO2], while under e[CO2] the positive effect of light intensity was eliminated. There is controversy with previous reports investigating the effects of e[CO2] on the growth of different plant species. For instance, the treatment of lettuce with e[CO2] reduced fresh weight, while application of e[CO2] together with complementary nutrients led to an increase in fresh weight compared to control plants (Croonenborghs et al. 2009; Miyagi et al. 2017).
The number of leaves per plant increased significantly by exposure to higher light intensities under a[CO2], while e[CO2] antagonistically interacted with light intensity in this regard. Notably, under e[CO2], no significant difference was observed in the number of leaves depending on light intensities. This suggests that e[CO2] inhibits the positive effect of high light intensity on leaf production. In line with our results, a 23% reduction in the number of leaves have been reported in soybean; however, the effect of e[CO2] on the number of leaves depended on the plant growth stage (Madhu & Hatfield 2015).
SLA value increased at e[CO2] and 75 μmol·m−2·s−1, but no significant effect was detected under higher light intensities. It has been reported that SLA decreased in response to e[CO2] in the four dominant Quercus species (Chae et al. 2016) as well as in other species (Poorter & Navas 2003; Ainsworth & Long 2005), while the positive effect of e[CO2] and the temperature on the leaf area was recorded in
At both CO2 concentrations, higher light intensities increased the root DW, but the enhancing effect of light intensity on roots decreased at elevation of CO2 level. Similarly, a positive effect of light intensity on root growth was demonstrated in
In contrast, increasing CO2 has been reported to reduce root/shoot ratio in
The results of our study showed that with increasing light intensity, the DW of the above-ground parts increased at both a[CO2] and e[CO2] levels, but at all light intensities, lower values of DW were obtained at higher CO2 level. The positive effect of e[CO2] on the above-ground biomass production and its negative effect on the grain yield were reported in wheat (Högy et al. 2009). Dry matter accumulation was increased by exposure to higher light intensity in either a[CO2] or e[CO2], but higher total biomass production in a[CO2] indicates a repressive effect of e[CO2] on dry matter accumulation. It has been shown that e[CO2] increases biomass production of rye, wheat,
The biomass partitioning to different plant organs depends on species, ontogeny, and the environment surrounding the plant (Poorter & Nagel 2000). Our study showed that distribution of biomass to different plant parts depends on light intensity and CO2 concentrations. In the perennial herb,
WUE was also affected by both CO2 concentration and the light intensity. By increasing light intensity, WUE increased more in plants grown at a[CO2], showing that CO2 enrichment and higher light intensity have a synergistic effect on WUE. The enhancing effect of increased light intensity on WUE was also demonstrated in pepper (Pan et al. 2020), lettuce (Esmaili et al. 2020), and wheat (Yi et al. 2020). In the case of lettuce, there was also an improvement in WUE by exposing the plants to a higher light intensity and enriching CO2 up to threshold levels (Esmaili et al. 2020). However, the declining impact of CO2 on WUE is in contradiction with previous reports on pigeon pea (Sreeharsha et al. 2015; Zhang et al. 2018). These contradictions in describing the interaction effect of light intensity and e[CO2] require further investigation.
Light intensity and concentration of CO2 had considerable effect on the growth and reproduction of chrysanthemum. The plants grown at higher light intensities and ambient CO2 were characterized with higher dry weight of vegetative organs and total biomass while having a lower dry weight of the inflorescences. The CO2 increased to 1,000 ppm reduced the positive effect of light on the dry weight of vegetative organs; however, its opposite effect was observed on dry weight of inflorescence, suggesting that at a higher CO2 level, biomass tends to be shifted toward inflorescence compared to vegetative organs. In addition, flowering was accelerated at higher CO2 and higher light intensities. The increase in light intensity favors the allocation of biomass to the inflorescence and elevation of CO2, enhancing the increasing effect of light on partitioning of biomass to the inflorescence. Overall, our study provides insight into the role of light intensity and CO2 concentration on vegetative and generative growth of chrysanthemum.