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Short-Term Hypergravity-Induced Changes in Growth, Photo synthetic Parameters, and Assessment of Threshold Values in Wheat (Triticum aestivum L.)

Data publikacji: 13 Apr 2022
Tom & Zeszyt: Tom 10 (2022) - Zeszyt 1 (January 2022)
Zakres stron: 10 - 17
Informacje o czasopiśmie
License
Format
Czasopismo
eISSN
2332-7774
Pierwsze wydanie
30 Jan 2019
Częstotliwość wydawania
2 razy w roku
Języki
Angielski
INTRODUCTION

Plants can respond to many abiotic stress conditions, such as temperature, drought, salinity, heavy metals, and so on in several ways. It has been hypothesized that, for almost every biological system there exists a threshold for physiological response and behavior, above or below which the responses are significantly affected. Identifying potential threshold values in plants is important as it indicates their sustainability in extreme abiotic environments, and significant changes in plant growth and development may occur around this value. For instance, the water potential threshold that started to negatively affect the rice growth was observed to be between −0.046 and −0.056 MPa (Santos et. al., 2018). Plants subjected to mild heat stress (1°C to 4°C above optimal growth temperature) had reduced yield (Timlin et al., 2006; Tesfaendrias et al., 2010); however, more intense heat stress (generally greater than 4°C above optimum) resulted in severe yield loss extending to complete crop failure (Ghosh et al., 2000; Tesfaendriasetal., 2010). The optimum temperature range in citrus (Citrus sinensis L. Osbeck) is 22°C–27°C, and temperatures greater than 30°C increased significant fruit drop (Cole and McCloud, 1985).

Gravity, a constant abiotic physical factor on Earth, plays a very important role in functioning of many biological systems such as bacteria, plants, animal, etc. Recent advances in space and gravitational biology have shown that an alteration in the gravity value above or below Earth's gravity (1 g) produces measurable changes in biological systems. Indeed, it is well documented that microgravity has positive effects while hypergravity has negative effects on plant growth and development (Waldron and Brett, 1990; Hoson et al., 1996; Jagtap et al., 2011; Vidyasagar et al., 2014). Although several studies have been conducted on ground-based low gravity (simulated microgravity), the use of plant systems for studies under a higher range of hypergravity conditions is limited, which may be due to the negative impact of high g forces on plants. Efforts have been made to calculate the threshold of gravi response for unicellular organisms such flagellates, ciliates, etc. (Häder et al., 2005), but the threshold values of hypergravity effects for multicellular organisms such as plants were not reported clearly. The understanding and assessment of the threshold value of hypergravity in plants is important, as it would provide the lower and upper limit of the g-value where the change in plant growth and development are more prominent.

Higher-range g forces retarded growth and development in plants as seen from earlier reports, for example, pea seedlings when centrifuged at 140×g, 370×g, and 1,050×g for 5 days (Waldron and Brett, 1990), cress hypocotyls at 35×g, and 135×g for 12 hours (Hoson et al. 1996), azuki bean epicotyls at 30×g and 300×g for 10 hours (Soga et al., 1999), Arabidopsis thaliana at 300×g for 24 hours (Nakabayashi et al., 2006). An increase in the content of cell wall polysaccharides due to hypergravity exposure was observed in cress hypocotyls (Hoson et al., 1996) and in azuki bean epicotyls (Soga et al., 1999a). The elongation growth and lignin deposition in secondary cell walls of the Arabidopsis thaliana (L.) grown for three days after exposure to hypergravity of 300 g for 24 hours suggest the role of mechanoreceptors in hyper gravity-induced lignin deposition in secondary cell walls (Tamaoki et al., 2006). The loss of starch and soluble carbohydrates during seed development was found to be accelerated due to hyper gravity (Musgrave et al., 2009). Thus, different plants were exposed to different hypergravity levels (selection of g-value unclear) and effects were studied. Despite adequate information available onthe effects of hyper gravity on plant growth and development, much less is known about photosynthetic parameters such as the rate of photosynthesis, stomatal conductance, the rate of transpiration, and intracellular CO2 concentration that plays an important role in driving photosynthesis. In addition, the information on hypergravity-induced changes in chlorophyll fluorescence parameters characterized by the Kautsky fluorescence induction curve (photochemical activity of PS II) is limited. Only few reports have documented the effects of hypergravity on photosynthetic and chlorophyll fluorescence parameters; however, these studies were not aimed at threshold values (Vidyasagar et al., 2014; Takemura et al., 2017). This could be due to the negative impact of hypergravity on plant growth and development, which might have discouraged researchers from extending hypergravity studies for understanding photosynthesis.

Therefore, in addition to growth, the photosynthetic and chlorophyll fluorescence parameters were also considered to assess the threshold values of hypergravity in wheat (Triticum aestivumL) in this study. The study of the threshold value of high g on growth and photosynthetic parameters will not only give us an idea about the response of these parameters under high g but also will indicate the optimum range of high g for future studies.

MATERIALS AND METHODS
Hypergravity Treatment

Wheat seeds (Triticum aestivum L.) of variety Lok-1 were procured from Sheti Udyog Bhandar, Swargate, Pune. Noninfected (no black spots) and matured seeds of uniform size were selected for each experiment. Seeds were surface-sterilized with 0.5% (w/v) fungicide (Uthane M-45 manufactured by United Phosphorus Limited), washed four to five times with distilled water to remove traces of fungicide and imbibed in distilled water for 24 hours. After immersion, eight seeds were suspended in a test tube containing 1 ml distilled water. The seeds suspended in test tubes were exposed to hypergravity at 25 °C in dark condition using a high-speed centrifuge machine which offers acceleration profiles of selected steps (Model: Superspin RV/FM with rotor radius ~6 cm manufactured by Plasto Craft Industries, Pvt. Ltd. Mumbai, India). The time of exposure was kept constant for 10 minutes, and hypergravity values varied from 200 g, 400 g, 600 g, 800 g, and 1,000 g. After exposure to higher g, seeds were sow non 0.8% (w/v) agar gel under normal gravity (1 g) and light intensity of 15 μmolm−2s−1 for 16D / 8N cycle in the month of March with ambient environmental conditions, i.e., temperatures of 30 ± 2 °C and relative humidity of 40 ± 5%. Seeds suspended in similar test tubes containing 1 ml distilled water kept at 25 °C without exposure to higher g acted as control. All the measurements were carried out on the fifth day after sowing.

Growth

Growth parameters such as shoot length, root length, fresh shoot weight, and fresh root weight of five-day-old seedlings raised from controls and hypergravity-exposed seeds were measured.

Measurement of photosynthesis parameters

On the fifth day, seedlings were taken out of the 0.8% (w/v) agar gel, and shoots were removed for measurement of the photosynthesis parameters. The shoots were immediately placedin the leaf cuvette (PLC4-B) for the measurement of photosynthesis parameters, i.e., the rate of photosynthesis (PN) in μmol m−2 s−1, the transpiration rate (Evap) in mmol m−2 s−1, the stomatal conductance (GS) in mmol m−2 s−1, and the intracellular CO2 concentration (Cint) in μmol mol−1 by using the TPS-2 portable photosynthesis system (PP Systems, USA).

Measurement of chlorophyll fluorescence parameters (Kautsky curve)

Chlorophyll fluorescence has been routinely used for many years to monitor the photosystem II (PSII) behavior of plants noninvasively (Strasser et al., 1995; Baker and Rosenqvist, 2004). For the recording of chlorophyll fluorescence, a portable instrument Handy PEA (Plant Efficiency Analyser, Hansatech Instruments, Kings Lynn, UK) was used. Shoots from five–day-old seedlings raised from control and hypergravity-treated seeds were isolated and immediately enclosed in leaf clips for 10 minutes of adaptation to darkness. After 10 minutes, a single strong 1 second light pulse (3,500 μmolm−2s−1) was applied to the shoots with the help of three light-emitting diodes (650 nm). The fast fluorescence kinetics (Fo to Fm) was recorded for 10 μs to 1 second both for the controls and the hypergravity-treated seedlings. The analysis of the chlorophyll fluorescence parameters was done using the Kautsky fluorescence induction curve labeled as O-J-I-P (Strasser et al., 1995; Prakash et al., 2003; Toth et al., 2007; Okukaroumet al., 2007; Xia et al., 2019). Using the OJIP test, minimal fluorescence (Fo), variable fluorescence (Fv), maximal fluorescence (Fm), maximum quantum efficiency of PSII photochemistry (Fv/Fm), performance index (PI), and area above the curve were obtained.

Statistical analysis

The data presented in this research paper gives the mean values of three sets of experiments with n=8 for each set. All the data were analyzed by using ANOVA with significance levels *p<0.05, **p<0.01, and ***p<0.001, NS means no significant difference.

RESULTS
Growth

The images of five-day-old shoots raised from controls and higher g-treated seeds are shown in Figure 1. No statistically significant difference was observed between controls and 200 g. The significant decrease in growth parameters such as shoot length (SL), root length (RL), fresh shoot weight (FSW), and fresh root weight (FRW), was observed in hypergravity-treated seeds from 400 g to 1,000 g. The decrease in shoot length and root length was 30% at 400 g and 90% at 1,000 g. The decrease in FSW and FRW was 19% at 400 g and 80 % at 1,000 g(Table 1).

Figure 1

Shoots extracted from five-day-old wheat seedlings raised from control and hypergravity treated seeds.

Photosynthesis parameters

The photosynthesis parameters, i.e., the rate of photosynthesis (PN) and intracellular CO2 concentration (Cint) were significantly decreased in five-day-old seedlings raised from hypergravity-exposed seeds compared with controls (Figure 2). At 400 g, the percentage decrease in the rate of photosynthesis (PN) and intracellular CO2 concentration (Cint) was found to be 38% and 20% while at 1,000 g, it was 84% and 40%, respectively. However, there was no significant change observed at 200 g for these two parameters compared to control. The transpiration rate (Evap) and stomatal conductance (Gs) parameters were slightly decreased, though not significant, in all the hypergravity-exposed samples except 200 g as compared with controls.

Figure 2

Photosynthesis parameters such as (a) rate of photosynthesis (PN), (b) intracellular CO2 concentration (Cint), (c) transpiration rate (Evap), and (d) stomatal conductance (Gs) in five-day-old seedlings raised from controls and hypergravity-exposed seeds.

Kautsky fluorescence induction curves

The Kautsky fluorescence induction curves for five days old seedlings raised from control and hypergravity exposed seeds are shown in Figure 3. The fluorescence intensity of Kautsky induction curves decreased with increase in value of hypergravity from 400 g to 1,000 g compared with controls.

Figure 3

Kautsky fluorescence induction curves for control and hypergravity samples (Set 1: Control, Set 2: 200 g, Set 3: 400 g, Set 4: 600 g, Set 5: 800 g and Set 6: 1,000 g) obtained from Handy PEA instrument.

The area above the fluorescence OJIP curve between Fo and Fm decreased with an increase in g-value as compared with controls (Table 2). The decrease in area was 6% at 400 g and 43% at 1,000 g. However, at 200 g fluorescence intensity and area above OJIP curve remain unchanged.

Chlorophyll fluorescence parameters

The performance index (PI) showed a significant fall in five-day-old seedlings ranging from 400 g to 1,000 g as compared with controls (Table 1) except at 200 g. The percentage fall in PI was 9% at 400 g and 33% at 1,000 g. No change in the ratio Fv/Fm, i.e., maximal photochemical efficiency of PSII, was observed in hypergravity samples as compared with controls.

DISCUSSION

The effects of short-term hypergravity exposure on growth, photosynthetic and chlorophyll fluorescence parameters in wheat seedlings raised from hypergravity-exposed seeds were investigated to understand the threshold response of the effects of hypergravity. The significant reduction in growth begins at 400 g and declined to its maximum at 1,000 g. The rate of reduction was found to be 10% more pronounced in seedling length as compared with its weight. The reduction in growth is consistent with the previous studies on various vascular plants such as peas, azuki beans, cress, etc., due to long-term moderate exposure to hypergravity (Hoson et al., 1996; Waldron and Brett, 1990; Soga et al., 1999; Takemura et al., 2017). The decrease in cell wall extensibility (Hoson et al. 1996) or lower enzyme activity (Vidyasagar et al., 2014) could be the possible reasons for the observed decrease in growth as reported earlier.

Photosynthesis is one of the major physiological processes in plants and is highly sensitive to changes in environmental conditions. Intracellular CO2 is one of the important factors that determine plants ability to perform photosynthetic assimilation. In the present study, it was found that intracellular CO2 concentration (Cint) gradually decreased from 400 g to 1,000 g. The significant decrease in rate of photosynthesis (PN) was also observed from 400 gupto 1,000 g. The observed lower rate of photosynthesis in hypergravity samples compared with control could be due to the relatively reduced availability of Cint (Tominaga et al., 2018). The reduced availability of CO2 could be attributed to decrease in stomatal conductance (Gs), i.e., the ability of the stomatal pore to release water vapor from the leaf to the atmosphere and allow CO2 to enter from the atmosphere. The decrease in stomatal conductance may also cause a decline in the transpiration rate (Farquhar and Sharkey, 1982; Jeanguenin et al., 2017). In addition to the above argument, contributions from other factors such as reductions in chlorophyll content (Vidyasagar et al., 2014) and changes in chloroplast size (Takemura et al., 2017) might also be responsible for the reduced rate of photosynthesis in the present study.

Chlorophyll fluorescence gives the information about change in the efficiency of photochemistry of photosystem II (Maxwell and Johnson, 2000). The fluorescence curve starts from minimal fluorescence Fo (O) to maximal fluorescence Fm (P) via two intermediate steps J and I with respect to time. This entire curve divides into three phases: O-J, J-I and I-P (Figure 4). As seen from the results, the initial minimal level of fluorescence Fo (fluorescence origin) was found to be same for the controls as for all the hypergravity samples(Figure 3). This indicates that all the PSII reaction centers were in open state and the first stable electron acceptor of PSII called QA oxidized equally in control as well as in all hypergravity samples. However, the maximal fluorescence (Fm) value was found to be reduced in hypergravity samples (Figure 3). Maximal fluorescence is observed when all the reaction centers are closed and QA is fully reduced. This, in turn, is governed by the relative rates of PSII photochemistry and oxidation of plastoquinol by electron transfer to photosystem I (PSI). The area above the chlorophyll fluorescence curve between Fo and Fm is proportional to the pool size of the electron acceptors QA on the reducing side of PSII. It can beseen from Figure 3 that the average area above the Kautsky curve gradually decreased for the hypergravity samples ranging from 400 g to 1,000 g. The decrease in the Fm value in the hypergravity samples (Figure 3), as QA was not fully reduced, possibly indicates an imbalance between the rate of PSII photochemistry and plastoquinol oxidation with an increase in the g-value from 400 g to 1,000 g. The important parameter of chlorophyll fluorescence, the performance index (PI), indicating plant vitality under stress decreased from 400 g to 1,000 g. The decrease in PI could be a consequence of reduced reaction center density or declined trapping efficiency and electron transfer efficiency (Tripathy et al., 1996; Stribet and Govindjee, 2011).

Figure 4

A typical Kautsky fluorescence induction curve adapted from Strasser et al. 1995; Xia et al., 2019.

The present study has revealed that when seeds were exposed to a short duration of 10 minutes, the reduction of growth, photosynthetic and chlorophyll fluorescence parameters started at 400 g and was at the maximum at 1,000 g. This indicates that 400 g may be considered as a lower threshold and 1,000 g a higher threshold of hypergravity for growth, as well as photosynthetic and chlorophyll fluorescence parameters in wheat (Figure 5). The value of hypergravity at which these effects have just started can be termed the lower threshold g (THL-g) while at which these effects are at the maximum can be termed the higher threshold g (THH-g).

Figure 5

Schematic diagram showing the declined effect on growth and photosynthesis in response to the stimulus of hypergravity. Average percentage decrease in growth (values in red) and rate of photosynthesis, PN (values in green) with an increase in hypergravity (g) value as compared with control in wheat with ambient environmental conditions, i.e., temperature 30 ± 2°C, relative humidity 40 ± 5%. THL and THH indicate the lower threshold and the higher threshold at 400 g and 1,000 g, respectively.

In our previous study, the reduction in growth parameters due to short-term hyper gravity were seen at 500 g and the maximum at 2,000 g in wheat (Vidyasagar et al., 2014). The difference in threshold g values between the present and the previous studies could be due to the difference in the environmental conditions, especially temperature (25°C and 30°C) and humidity (60% and 40%). Several alterations are possible in growth and developmental response under hypergravity due to the difference in the physiological state of the plants and environmental conditions during and/or after exposure as reported earlier (Tamaoki et al., 2006; Kozeko and Kordyum, 2009; Takemura et al., 2017), which may lead to a different threshold response. Further, it can be assumed that the protective layer (coating) of seeds might have opposed hypergravity below 400 g but failed to resist it at and above 400 g. It would be interesting to explore the threshold values of the effects of hyper gravity for different cereals display in g variation in the density of the seed coat. In addition, to find the exact threshold value of high g, we recommend that the acceleration steps in g-value should be as small as possible. Keeping this in mind, we hypothesize that, plants possess the threshold value of hyper gravity effects, which may vary depending upon the time of exposure, the sensitivity of seeds or seedlings to a given g-value, and the environmental conditions under which they are exposed to hypergravity and grown. We encourage future studies to investigate underlying the physiological mechanisms responsible for observed effects at threshold g-values.

CONCLUSIONS

The present study aimed to analyze the effects of short-term hyper gravity exposure ranging from 200 g to 1,000 g on plant growth and photosynthetic parameters and to assess threshold g-values at which these effects were observed. No significant change was seen at 200 g in terms of growth and photosynthetic parameters. However, a significant reduction in these parameters was observed from 400 g onward and found to be at the maximum at 1,000 g. This implies that plants do not perceive short-term exposure of 200 g as a stress and respond normally, while from 400 g onward, plants experience a stressful hyper gravity environment leading to the beginning of a reduction in growth and photosynthetic parameters. We therefore propose that short-term (10 minute) hypergravity at 400 g can be treated as a lower threshold and 1,000 g as higher threshold for wheat seeds when they are exposed and grown under the environmental conditions described above. The present study could help researchers to choose proper g-values to prevent excessive exposure of plants to hypergravity. According to the available literature, this is the first study to report the threshold values of short-term hypergravity for growth and photosynthetic parameters.

Figure 1

Shoots extracted from five-day-old wheat seedlings raised from control and hypergravity treated seeds.
Shoots extracted from five-day-old wheat seedlings raised from control and hypergravity treated seeds.

Figure 2

Photosynthesis parameters such as (a) rate of photosynthesis (PN), (b) intracellular CO2 concentration (Cint), (c) transpiration rate (Evap), and (d) stomatal conductance (Gs) in five-day-old seedlings raised from controls and hypergravity-exposed seeds.
Photosynthesis parameters such as (a) rate of photosynthesis (PN), (b) intracellular CO2 concentration (Cint), (c) transpiration rate (Evap), and (d) stomatal conductance (Gs) in five-day-old seedlings raised from controls and hypergravity-exposed seeds.

Figure 3

Kautsky fluorescence induction curves for control and hypergravity samples (Set 1: Control, Set 2: 200 g, Set 3: 400 g, Set 4: 600 g, Set 5: 800 g and Set 6: 1,000 g) obtained from Handy PEA instrument.
Kautsky fluorescence induction curves for control and hypergravity samples (Set 1: Control, Set 2: 200 g, Set 3: 400 g, Set 4: 600 g, Set 5: 800 g and Set 6: 1,000 g) obtained from Handy PEA instrument.

Figure 4

A typical Kautsky fluorescence induction curve adapted from Strasser et al. 1995; Xia et al., 2019.
A typical Kautsky fluorescence induction curve adapted from Strasser et al. 1995; Xia et al., 2019.

Figure 5

Schematic diagram showing the declined effect on growth and photosynthesis in response to the stimulus of hypergravity. Average percentage decrease in growth (values in red) and rate of photosynthesis, PN (values in green) with an increase in hypergravity (g) value as compared with control in wheat with ambient environmental conditions, i.e., temperature 30 ± 2°C, relative humidity 40 ± 5%. THL and THH indicate the lower threshold and the higher threshold at 400 g and 1,000 g, respectively.
Schematic diagram showing the declined effect on growth and photosynthesis in response to the stimulus of hypergravity. Average percentage decrease in growth (values in red) and rate of photosynthesis, PN (values in green) with an increase in hypergravity (g) value as compared with control in wheat with ambient environmental conditions, i.e., temperature 30 ± 2°C, relative humidity 40 ± 5%. THL and THH indicate the lower threshold and the higher threshold at 400 g and 1,000 g, respectively.

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