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Article

Exogenous Foliar Application of Glycine Betaine to Alleviate Water Deficit Tolerance in Two Indica Rice Genotypes under Greenhouse Conditions

by
Rujira Tisarum
1,
Cattarin Theerawitaya
1,
Thapanee Samphumphung
1,
Teruhiro Takabe
2 and
Suriyan Cha-um
1,*
1
National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Pathum Thani 12120, Thailand
2
Research Institute, Meijo University, Nagoya 468-8502, Japan
*
Author to whom correspondence should be addressed.
Agronomy 2019, 9(3), 138; https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy9030138
Submission received: 3 February 2019 / Revised: 25 February 2019 / Accepted: 15 March 2019 / Published: 18 March 2019
(This article belongs to the Special Issue Roles of Glycine Betaine in Improving Plant Abiotic Stress Resistance)
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Versions Notes

Abstract

:
The aim of this investigation was to enhance overall growth, yield attributes as well as physio-biochemical adaptive strategies by exogenous foliar application of glycine betaine (GlyBet) in two rice varieties against water deficit stress under greenhouse conditions. Rice crop cvs. RD43 (low amylose content) and SPR1 (high amylose content) grown in clay pots containing garden soil until booting stage were chosen as the test plant material, sprayed by 0 (control) or 100 mM GlyBet and subsequently subjected to: MWD (mild water deficit by 8 d water withholding; 24.80% SWC; Soil water content) or SWD (severe water deficit by 14 d water withholding; 13.63% SWC) or WW (well-watered conditions or control). Free proline content in cv. RD43 was rapidly increased in relation to the degree of water deficit and suppressed by exogenous GlyBet, while free proline in cv. SPR1 was lower than cv. RD43. Overall growth performances and yield traits in both cultivars under MWD were maintained by exogenous application of GlyBet; however, these parameters declined under SWD even after the GlyBet application. Degradation of photosynthetic pigments and chlorophyll fluorescence in pretreated GlyBet plants under SWD were prevented, resulting in elevated net photosynthetic rate (Pn). Interestingly, Pn was very sensitive parameter that sharply declined under SWD in both RD43 and SPR1 genotypes. Positive relationships between physio-morphological and biochemical changes in rice genotypes were demonstrated with high correlation co-efficiency. Based on the key results, it is concluded that foliar GlyBet application may play an important role in drought-tolerant enhancement in rice crops.

1. Introduction

Rice is an important carbohydrate source for the world population with nearly 3 billion people consuming rice as a staple food, especially in Asia [1]. In fact, rice cultivation consumes about 24%–30% of fresh water resources in its whole life cycle. Water-saving strategies and improved varieties with high water use efficiency [2] have been developed [3,4,5]. In the world, 79 million ha cultivation of low land rice provides 75% of the world’s rice production [6]. In Asia, paddy fields (40%–46% of irrigated area) have been known to consume 2- to 3-fold the volumes of the fresh water used by other crops [7]. A water shortage in the irrigated paddy fields is evidently observed, depending upon the high evaporation rate or the limiting fresh water supply, resulting in reduced productivity [8,9,10,11,12]. Drought stress as a consequence of climate change in rainfed areas is a major constraint to high productivity [13,14,15].
A large number of anti-drought agents, i.e., compatible solutes (GlyBet, proline, trehalose) and plant growth regulators (gibberellic acid, paclobutrazol, cytokinins, salicylic acid) are investigated for the amelioration of the drought stress [16,17,18,19]. GlyBet is a member of quaternary ammonium compounds, and a neutral compatible solute that plays a key role in cellular osmotic adjustment, maintaining the organelles (mitochondria, chloroplasts) and water-use efficiency in the plants under water deficit [20,21]. Rice crop has been reported as a GlyBet non-accumulator plant with a very low amount of GlyBet [<1 μmol g−1 dry weight (DW)] [22]. However, overexpression of GlyBet biosynthesis-related genes, i.e., CMO (choline monooxygenase) and BADH (betaine aldehyde dehydrogenase) in rice crop has improved abiotic tolerance in the plant [23,24,25]. Alternatively, exogenous application of GlyBet in the rice crop has been well established to improve plant growth, development and yield traits under drought stress [26,27,28]. For example, exogenous foliar of 100 mM GlyBet in Pathumthani 1 (PT1), a drought-sensitive cultivar for water deficit alleviation (physiological adaptation, growth retention and yield stabilization, has been published [27]. The uptake, translocation and accumulation of GlyBet by exogenous application have been reported in several other plant species as well [29,30,31,32]. In addition, regulation of antioxidative defense mechanisms and their physiological adaptation in rice crops to cope with drought stress using GlyBet seed priming has also been well investigated [26]. Consequently, the role of GlyBet in physiological and biochemical adaptation processes and hormonal regulation against a drought situation has been well studied [20,33]. However, information regarding the endogenous proline regulation in drought-stressed plants pretreated with GlyBet, especially in different rice genotypes, is limited.
Recently, a released rice variety, RD43 (SPR99007-22-1-2-2-1 registered by the Rice Department, Thailand, 5 October 2010) with medium glycemic index and low amylose content [34] and irrigated lowland variety, Suphan Buri 1 (SPR1; SPRLR85163-5-1-1-2 registered by the Rice Department, Thailand, 28 October 1993) with high amylose content [35,36] were selected to be tested for water deficit-tolerant abilities using exogenous foliar GlyBet. These cultivars have been reported as moderately salt tolerant [37], however, there is no study in context with their drought tolerance efficiency. The objective of this study was to improve the overall growth and yield traits as well as physio-biochemical strategies by exogenous GlyBet application in the selected rice varieties under water deficit stress.

2. Materials and Methods

2.1. Plant Material, Exogenous Glybet Foliar and Water Deficit Treatments

Seeds of two rice genotypes, ‘Rice Department #43 or RD43’ (low glycemic index) and ‘Suphan Buri 1 or SPR1’ (high amylose content) obtained from the Pathumthani Rice Research Center, Thailand, were used as test materials. Two-week-old seedlings of rice were transplanted into clay pots (ø = 20 cm) containing 2 kg garden soil (Electroconductivity (EC) = 2.687 dS m−1; pH = 5.5; organic matter = 10.36%; total nitrogen = 0.17%; total phosphorus = 0.07%; total potassium = 1.19%). The transplanted seedlings were incubated in a greenhouse under 500−1000 μmol m−2 s−1 photosynthetic photon flux density with a 10 h d−1 photoperiod, 25–37 °C ambient temperature and 50%–85% relative humidity, until booting stage. Rice plants were treated with 0 (water) and 100 mM foliar spray of GlyBet (Betaine; 50 mL plant−1). Thereafter, 3 sets of drought treatment were set up. These included: well-watered condition (WW; 44.02% soil water content (SWC)), mild water deficit condition (MWD; 24.80% SWC) by withholding water for 8 days, and severe water deficit condition (SWD; 13.63% SWC) by withholding water for 14 days, (Figure S1). In addition, the relative humidity and air temperature during the water withholding period were recorded using a data logger (MicroLogPROII, Fourtec-Fourier Technologies Ltd., Rosh Ha’ayin, Israel) (Figure S2). Shoot height, number of leaves, number of tillers and flag leaf area in each treatment were measured. In addition, panicle weight (PW), panicle length (PL), seed fertility (SF) and hundred grain weight (HGW) at the time of harvest were also recorded.

2.2. Proline Quantification

Free proline in the flag leaf tissues of each treatment, collected at 0, 2, 4, 6, 8, and 14 days after water withholding and 3-days re-watering (recovery), was analyzed according to the method of Bates et al. [38]. Fifty milligrams of fresh material were ground with liquid nitrogen in a mortar. The homogenate powder was mixed with 1 mL of aqueous sulfosalicylic acid (3%, w/v) and filtered through filter paper (Whatman #1, Sigma-Aldrich, Darmstadt, Germany). The extracted solution was reacted with an equal volume of glacial acetic acid and ninhydrin reagent (1.25 mg ninhydrin in 30 mL of glacial acetic acid and 20 mL of 6 M H3PO4) and incubated at 95 °C for 1 h. The reaction was terminated by placing the container in an ice bath. The reaction mixture was mixed vigorously with 2 mL of toluene. After cooling to 25 °C, the chromophore was measured at 520 nm by spectrophotometer (HACH DR/4000; Model 48,000, HACH Company, Loveland, CO, USA) using L-proline as a calibration standard.

2.3. Plant Physiological Assay

Chlorophyll a (Chla), chlorophyll b (Chlb), and total chlorophyll (TC) content in the flag leaf tissues were analyzed according to the method of Shabala et al. [39]. One hundred milligrams of leaf tissue were homogenized in a glass vial with 10 mL of 99.5% acetone, and blended using a homogenizer. The glass vials were sealed with Parafilm® to prevent evaporation, and then stored at 4 °C for 48 h. Chla and Chlb concentrations were measured at 662 nm and 644 nm, respectively, using an ultraviolet–visible (UV–VIS) spectrophotometer (DR6000™ UV-VIS Spectrophotometer, HACH®, Loveland, CO, USA) against acetone (99.5%) as a blank.
Chlorophyll fluorescence emission was measured from the adaxial surface of flag leaf using a fluorescence monitoring system (model FMS 2; Hansatech Instruments Ltd., Norfolk, UK) in the pulse amplitude modulation mode [40]. A leaf, kept in dark for 30 min was initially exposed to the modulated measuring beam of a far-red light (LED; Light emitted diode source) with typical peak at wavelength of 735 nm. Original (F0) and maximum (Fm) fluorescence yields were measured under weak modulated red light (<85 μmol m−2 s−1) with 1.6 s pulses of saturating light (>1500 μmol m−2 s−1 PPFD; Photosynthetic photon flux density) and calculated using FMS software for Windows®. The variable fluorescence yield (Fv) was calculated using the equation: Fv = Fm − F0. The ratio of variable to maximum fluorescence (Fv/Fm) was calculated as the maximum quantum yield of PSII photochemistry. The photon yield of PSII (ΦPSII) in the light was calculated as: PSII = (Fm‘ − F)/Fm‘ after 45 s of illumination, when steady state was achieved [41].
Net photosynthetic rate (Pn; μmol m−2 s−1) was measured using a portable photosynthesis system with an infrared gas analyzer (Model LI 6400, LI-COR® Inc., Lincoln, NE, USA). Pn parameter was measured by continuously monitoring the content of the air entering and exiting in the IRGA headspace chamber, according to Cha-um et al. [42].

2.4. Plant Morphological Characterization and Yield Traits

Shoot height, number of leaves, number of tillers and flag leaf area in each treatment were measured. In addition, panicle weight (PW), panicle length (PL), seed fertility (SF) and hundred grain weight (HGW) at the time of harvest were also recorded.

2.5. Statistical Analysis

The experiment was arranged as 3 × 2 factorial in a completely randomized design (CRD) with six replicates (n = 6) for each treatment. The mean values from six treatments were compared using Tukey’s HSD (Honestly significant difference) and analyzed by SPSS software (version 11.5 for Window®, SPSS Inc., Chicago, IL, USA). In addition, the relationships between physiological and morphological characters were validated using Pearson’s correlation co-efficiency method.

3. Results and Discussion

3.1. Free Proline Accumulation Pattern under Water Deficit Conditions

At booting stage, free proline in the flag leaf of indica rice cv. RD43 was increased in relation to the degree of water deficit and the maximum value obtained was 120.94 (29.14 folds high over well watering) and 172.32 μmol g−1 FW (56.68-fold high over well watering) in MWD and SWD, respectively. The content declined by re-watering in the recovery process (Figure 1a). Similarly, free proline in cv. SPR1 under water deficit was accumulated by 1.80- and 20.93-fold in MWD and SWD, respectively, over WW conditions (Figure 1b). Interestingly, free proline accumulation rate in flag leaf of GlyBet-pretreated rice cvs. RD43 and SPR1 under water deficit declined when compared to untreated plants (Figure 1). Free proline was a major compatible solute in cv. RD43 to cope with water deficit stress, whereas this was not applicable in case of cv. SPR1, pointing towards the difference in their patterns of responses towards water deficit conditions (Figure 1). Moreover, free proline in GlyBet-pretreated rice cv. SPR1 under MWD was similar to that of well watering, and comparatively high under SWD (Figure 1b).
An exogenous GlyBet foliar application in rice crop for abiotic stress tolerance, i.e., drought [26,27] and salt [43,44,45] has been well explored. Endogenous levels of GlyBet in several organs of monocotyledonous plant species, maize [46] and wheat [47,48,49], is enriched by exogenous GlyBet dosage application, water withholding period and their interaction. In addition, GlyBet uptake and translocation in higher plants, tobacco [50], sunflower [51] and Carapa guianensis Aublet [32], under drought conditions has also been reported. In the present study, free proline in both RD43 and SPR1 cultivars was regulated by reduction in the degree of SWC and it was decreased by exogenous foliar GlyBet application. In papaya cv. BH-65, free proline in the leaves of 18 d water deficit stress was recorded to be the maximum, but it was subsequently decreased by re-watering and repressed by GlyBet pretreatment [52]. Similarly, free proline in tobacco cvs. DHJ5210 (drought tolerant) and ZY100 (drought-sensitive) under drought stress was down-regulated by 80 mM GlyBet application [50]. In 19 wheat genotypes, free proline and endogenous GlyBet levels in the drought-stressed plants treated with exogenous GlyBet application increased in both tillering and anthesis stages [49]. Free proline in GlyBet pretreated rice cv. PT1 [27], maize cvs. S911 and S9 [17], sunflower [53] and pea [54], under water deficit conditions was the maximum. Moreover, free proline in leaf and panicle tissues of drought stressed rice cv. Basmati-385, irrespective of GlyBet foliar spray, enriched compared to cv. KS-282 [28]. The major role of free proline enrichment in the drought stress tolerance via osmotic adjustment and antioxidant activities at the cellular levels has been well established [26,48,50,54].

3.2. Overall Growth Performances and Yield Traits

Shoot height in rice cv. RD43 under MWD and SWD without GlyBet treatment was significantly declined by 3.53% and 5.23% over well watering, respectively, whereas shoot height under SWD with GlyBet application dropped by 4.31% over well watering conditions. In contrast, shoot height in cv. SPR1 under SWD without GlyBet was expressively declined by 14.43% over well watering and improved on GlyBet foliar application (Table 1). The number of leaves in cvs. RD43 and SPR1 irrespective of GlyBet treatment under SWD were decreased. The number of tillers per clump in cvs. RD43 and SPR1 without GlyBet treatment under MWD and SWD were significantly reduced; however, those were elevated by exogenous GlyBet application (Table 1). Interestingly, number of tillers in cv. RD43 under SWD was strongly raised up by GlyBet application, although it declined by 21.77% in cv. SPR1 (Table 1). In addition, flag leaf area in cvs. RD43 and SPR1 without GlyBet treatment under SWD was declined by >50% over well watering. Flag leaf area was found to be a good indicator to identify the cv. RD43 as water deficit tolerant over cv. SPR1, as it showed the reduction by 38.55% under MWD and by 55.50% under SWD (Table 1).
In the present study, overall growth performance, i.e. shoot height, number of leaves, number of tillers and flag leaf area, in rice cvs. RD43 and SPR1 grown under MWD were strongly improved by exogenous GlyBet application. Under SWD, number of leaves in both cultivars was significantly dropped even after exogenous GlyBet application. In rice cv. PT1 (drought sensitive), shoot height in plants under water deficit was deteriorated by 11.47% over the control, whereas it was maintained by 100 mM GlyBet foliar application (4.09% reduction of control) [27]. In tobacco, shoot height in cvs. DHJ5210 (drought-tolerant) and ZY100 (drought-sensitive) under drought stress was elevated by 80 mM GlyBet application [50]. In maize cultivars, Dongdan-60 and ND-95, shoot height and number of leaves under drought stress was elevated by GlyBet pretreatment and these traits in Dongdan-60 were more noticeable than in ND-95 [55]. In papaya cv. BH-65, the number of leaves was a very sensitive trait responding strongly to 18 d water deficit stress and declining by 65.27% to that of well watering (control), while it was improved by 50 mM GlyBet treatment (only 39.16% reduction to that of control) [52]. Moreover, plant height, number of leaves and leaf area of tomato cv. PS under drought stress (water withholding for 14 and 21d) were ameliorated by 10 mM GlyBet application [56].
Panicle weight of rice cv. SPR1 under MWD and SWD without GlyBet treatment was decreased by 28.92% and 63.45% over well watering, respectively. However, it declined by only 29.51% and 46.53%, respectively, in GlyBet-pretreated plants. In contrast, panicle weight of rice cv. RD43 under MWD was improved by GlyBet application; however, it was declined by 36.39% over well watering, when exposed to SWD (Table 2). Similarly, panicle length in cv. SPR1 under MWD and SWD without GlyBet pretreatment was decreased by 8.42% and 18.72%, respectively, over well watering, and decreased by 8.03% and 17.05%, respectively, over well watering in plants with GlyBet pretreatment. Interestingly, panicle length of cv. RD43 was strongly increased by foliar GlyBet application, leading to maintenance of the panicle weight and panicle length, especially under SWD (Table 1). Seed fertility in cv. SPR1 under MWD and SWD was significantly reduced by 30.37% and 74.96% over well watering. It was subsequently lifted-up by GlyBet pretreatment in cv. RD43 under MWD, whereas it declined by 33.14% under SWD with GlyBet pretreatment. Grain weight (100 grains) in cvs. SPR1 and RD43 under SWD without GlyBet application declined by 19.93% and 14.56% over the control, and it was strongly improved by GlyBet application (Table 2).
Panicle weight, panicle length, seed fertility and HGW in cv. RD43 under water deficit were better than those in cv. SPR1, and these were further improved by 100 mM GlyBet foliar application, especially under SWD. In rice cv. PT1 (drought sensitive), panicle length, panicle weight, seed fertility and HGW of GlyBet pretreated plants at booting stage under water deficit stress were significantly improved compared to untreated plants [27]. Likewise, number of seeds per panicle in 100 mM GlyBet pretreated rice cvs. KS-282 (coarse grain rice) and Basmati-385 (fine grain rice) under water deficit stress was greater than untreated plants [28]. Grain yield (g m−2) of 100 mM GlyBet foliar sprayed wheat genotypes under drought stress was strongly elevated compared to untreated plants [57]. Moreover, yield traits, cob length, number of kernels per row, number of kernels per cop and grain yield per plant in GlyBet-pretreated maize cvs. Dongdan-60 and ND-95 under drought conditions were also better compared to the plants without GlyBet application [55].

3.3. Physiological Changes and Relationships between Those Traits

Chla and Chlb contents in flag leaf of rice cv. RD43 without GlyBet pretreatment were sensitive to SWD, and decreased by 57.35% and 46.50% over the control (Table 3). Chla in flag leaf tissues of rice cv. RD43 without GlyBet pretreatment under MWD was degraded by 35.67% over control. Chla and Chlb contents in cv. SPR1 under SWD without GlyBet application were found to be minimum at 130.38 and 170.63 μg g−1 FW, respectively (Table 3). TC content in cv. RD43 without GlyBet pretreatment under SWD was significantly degraded by 51.13% (Figure 2a), as well as being lowest at 301.01 mg g−1 FW in cv. SPR1 under SWD (Figure 2b). Maximum quantum yield of PSII (Fv/Fm) and photon yield of PSII (ΦPSII) of rice crop cv. RD43 without GlyBet pretreatment under SWD were diminished by 46.53% and 49.04% over the control, whereas these were retained upon exogenous GlyBet application. Moreover, Fv/Fm and ΦPSII in cv. SPR1 without GlyBet pretreatment under SWD were reduced by 22.35% and 41.95% over control, respectively (Table 3). Interestingly, Fv/Fm in cv. SPR1 with GlyBet pretreatment under SWD declined by 11.49% over the control. Pn in rice cv. RD43 without GlyBet treatment under MWD, and SWD was reduced by 31.63% and 80.73% over the control, respectively; but it was elevated upon GlyBet pretreatment, especially under MWD (Figure 2c). However, Pn in cv. SPR1 was sharply declined when subjected to SWD in both with (77.68% reduction over control) or without (85.82% reduction over control) GlyBet application (Figure 2d). Positive relationships between Chla content and Fv/Fm in cv. RD43 (r2 = 0.6456; Figure 3a) and SPR1 (r2 = 0.7568; Figure 3b), and between TC content and ΦPSII in cv. RD43 (r2 = 0.5354; Figure 3c) and SPR1 (r2 = 0.5665; Figure 3d) were demonstrated. Moreover, positive relationships between ΦPSII and Pn in cv. RD43 (r2 = 0.8941; Figure 4a) and SPR1 (r2 = 0.7298; Figure 4b) as well as Pn and panicle weight in cv. RD43 (r2 = 0.9682; Figure 4c) and SPR1 (r2 = 0.9332; Figure 4d) were also established.
The reduction rate of chlorophyll pigments, i.e. Chla, Chlb and TC, in crop species depends on the degree of water deficit, GlyBet application, drought tolerant abilities and their interaction [27,55]. SPAD (Konica Minolta Chlorophyll Meter SPAD 502 PLUS) value or chlorophyll content in flag leaf of wheat was maintained in cv. HF9703 (drought tolerant) better than in cv. SN215953 (drought-sensitive) when subjected to drought stress [47]. In addition, similar results in cotton [19] and tobacco [50] have been established. Consequently, Fv/Fm and ΦPSII in rice cvs. RD43 and SPR1 under SWD without GlyBet were sharply diminished and strongly improved by GlyBet pretreatment. In PT1 rice, Fv/Fm and ΦPSII in flag leaf tissues were very sensitive to severe water deficit (25% soil water content) and diminished by 41.42% and 42.49% over the control, respectively, but promoted by exogenous GlyBet pretreatment, resulting in maintained Pn [27]. In wheat cvs. HF9703 (drought-tolerant) and SN215953 (drought-sensitive), the diminishing rate of Fv/Fm depended on their drought-tolerant abilities, intensity of drought stress, as well as strongly being enhanced by GlyBet application [48]. Moreover, ΦPSII in tobacco cvs. DHJ5210 (drought-tolerant) and ZY100 (drought-sensitive) under drought stress conditions was retained in GlyBet treated plants [50]. Under SWD, Pn was a sensitive parameter in rice crop cvs. RD43 (80.73% reduction) and SPR1 (85.82% reduction) but it was stabilized in 100 mM GlyBet pretreated plants. Similar results of Pn stabilization under drought stress using exogenous GlyBet application in papaya [52], tobacco [50], cotton [19], and wheat [47] have been reported. In addition, a positive relation between physiological data and panicle weight of rice cvs. RD43 and SPR1 was validated. In an earlier study, relationships between Chla and Fv/Fm (r2 = 0.74), TC and ΦPSII (r2 = 0.72), Fv/Fm and Pn (r2 = 0.82), Pn and panicle weight (r2 = 0.67) in GlyBet pretreated rice (cv. PT1) under water deficit have been established [27]. Likewise, positive relations between TC and ΦPSII (r2 = 0.91), photochemical quenching (qP) and Pn (r2 = 0.64), Pn and plant dry weight (r2 = 0.75) in GlyBet-pretreated rice (cv. KDML105) under salt stress have been validated [58].

4. Conclusions

Overall growth performances, yield attributes, physio-biochemical responses in indica rice cvs. RD43 and SPR1 coping with water deficit conditions, especially severe water deficit were ameliorated by 100 mM GlyBet foliar application at the booting stage. Under severe water deficit, chlorophyll pigments, chlorophyll fluorescence and net photosynthetic rate in 100 mM GlyBet-pretreated plants were maintained, leading to them retaining overall growth performances and yield traits. Foliar GlyBet application may play an important role as a simple short-gun technique for drought-tolerant improvement in the rice crop.

Supplementary Materials

The following are available online at https://0-www-mdpi-com.brum.beds.ac.uk/2073-4395/9/3/138/s1, Figure S1: Soil water content in the soil substrate after water withholding period and re-watering treatments, Figure S2: Relative humidity and air temperature of environmental conditions in whole experiment of present study.

Author Contributions

R.T. performed the physiological assay; C.T. performed the biochemical assay; T.S. performed morphological and yield attributes; T.T. performed the experiment layout consultation and manuscript preparation; S.C. conceived and designed the experiments. All authors were responsible for manuscript writing. All authors read and approved the final manuscript.

Funding

This research was funded by National Science and Technology Development Agency (NSTDA grant number P-18-51456).

Acknowledgments

The authors would like to sincerely thank National Science and Technology Development Agency (NSTDA grant number P-18-51456), Thailand, for funding support.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Brar, D.S.; Singh, K.; Khush, G.S. Frontiers in Rice Breeding. In The Future Rice Strategy for India; Academic Press: Cambridge, MA, USA, 2017; pp. 137–160. [Google Scholar]
  2. Mottaleb, K.A.; Rejesus, R.M.; Murty, M.V.R.; Mohanty, S.; Li, T. Benefits of development and dissemination of climate-smart rice: Ex ante impact assessment of drought-tolerant rice in South Asia. Mitig. Adapt. Strat. Glob. Chang. 2017, 22, 879–901. [Google Scholar] [CrossRef]
  3. Bouman, B.A.M.; Humphreys, E.; Toung, T.P.; Barker, R. Rice and water. Adv. Agron. 2007, 92, 187–237. [Google Scholar]
  4. Smith, M.L.; Mohanty, R.K. Monsoon, rice production, and urban growth: The microscale management of ‘too much’ water. Holocene 2018, 28, 1325–1333. [Google Scholar] [CrossRef]
  5. Wu, S.J.; Chiueh, Y.W.; Hsu, C.T. Modeling risk analysis for rice production due to agro-climate change and uncertainty in irrigated water. Paddy Water Environ. 2018, 16, 35–53. [Google Scholar] [CrossRef]
  6. Maclean, J.L.; Dawe, D.; Hardy, B.; Hettle, G.P. Rice Almanac; International Rice Research Institute: Los Baños, Philippines, 2002; p. 253. [Google Scholar]
  7. Tuong, T.P.; Bouman, B.A.M.; Mortimer, M. More rice, less water–integrated approaches for increasing water productivity in irrigated rice-based system in Asia. Plant Prod. Sci. 2005, 8, 231–241. [Google Scholar] [CrossRef]
  8. Tuong, T.P.; Bouman, B.A.M. Rice production in water-scarce environments. In Water Productivity in Agriculture: Limits and Opportunities for Improvement; Kijne, J.W., Baker, R., Molden, D., Eds.; CAB International: Wallingford, UK, 2003; pp. 53–67. [Google Scholar]
  9. Kummu, M.; Guillaume, J.H.A.; de Moel, H.; Eisner, S.; Flörke, M.; Porkka, M.; Siebert, S.; Veldkamp, T.I.E.; Ward, P.J. The world’s road to water scarcity: Shortage and stress in the 20th century and pathways towards sustainability. Sci. Rep. 2016, 6, 38495. [Google Scholar] [CrossRef]
  10. Jiang, S.; Wang, J.; Zhao, Y.; Shang, Y.; Gao, X.; Li, H.; Wang, Q.; Zhu, Y. Sustainability of water resources for agriculture considering grain production, trade and consumption in China from 2004 to 2013. J. Clean. Prod. 2017, 149, 1210–1218. [Google Scholar] [CrossRef]
  11. van Oort, P.A.J.; Zwart, S.J. Impacts of climate change on rice production in Africa and causes of simulated yield changes. Glob. Chang. Biol. 2017, 24, 1029–1045. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Prabnakorn, S.; Maskey, S.; Suryadi, F.X.; de Fraiture, C. Rice yield in response to climate trends and drought index in the Mun River Basin, Thailand. Sci. Total Environ. 2018, 621, 108–119. [Google Scholar] [CrossRef]
  13. Bandara, J.S.; Cai, Y. The impact of climate change on food crop productivity, food prices and food security in South Asia. Econ. Anal. Pol. 2014, 44, 451–465. [Google Scholar] [CrossRef]
  14. Li, T.; Angeles, O.; Radanielson, A.; Marcaida, M.; Manalo, E. Drought stress impacts of climate change on rainfed rice in South Asia. Clim. Chang. 2015, 133, 709–720. [Google Scholar] [CrossRef]
  15. Hayashi, K.; Llorca, L.; Rustini, S.; Setyanto, P.; Zaini, Z. Reducing vulnerability of rainfed agriculture through seasonal climate predictions: A case study on the rainfed rice production in Southeast Asia. Agric. Syst. 2018, 162, 66–76. [Google Scholar] [CrossRef]
  16. Shao, H.; Chen, X.-Y.; Chu, L.-Y.; Zhao, X.-N.; Wu, G.; Yuan, Y.-B.; Zhao, C.-X.; Hu, Z.-M. Investigation on the relationship of proline with wheat anti-drought under soil water deficits. Colloids Surf. B Biointerfaces 2006, 53, 113–119. [Google Scholar] [Green Version]
  17. Zhang, L.; Li, S.; Liang, Z. Differential plant growth and osmotic effects of two maize (Zea mays L.) cultivars to exogenous glycinebetaine application under drought stress. Plant Growth Regul. 2009, 58, 297–305. [Google Scholar]
  18. Ahanger, M.A.; Tyagi, S.R.; Wani, M.R.; Ahmad, P. Drought tolerance: Role of organic osmolytes, growth regulators, and mineral nutrients. In Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment; Ahmad, P., Wani, M.R., Eds.; Springer: New York, NY, USA, 2014; pp. 25–55. [Google Scholar]
  19. Ahmad, P.; Hameed, A.; Abd-Allah, E.F.; Sheikh, S.A.; Wani, M.R.; Rasool, S.; Jamsheed, S.; Kumar, A. Biochemical and molecular approaches for drought tolerance in plants. In Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment; Ahmad, P., Wani, M.R., Eds.; Springer: New York, NY, USA, 2014; pp. 1–29. [Google Scholar]
  20. Ashraf, M.; Foolad, M.R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 2007, 59, 206–216. [Google Scholar] [CrossRef]
  21. Kurepin, L.; Ivanov, A.G.; Zaman, M.; Pharis, R.P.; Allakhverdiev, S.I.; Hurry, V.; Hüner, N.P.A. Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth. Res. 2015, 126, 221–235. [Google Scholar] [CrossRef]
  22. Rathinasabapathi, R.; Gage, D.A.; Mackill, D.J.; Hanson, A.W. Cultivated and wild rice do not accumulate glycinebetaine due to deficiencies in two biosynthetic steps. Crop Sci. 1993, 33, 534–538. [Google Scholar] [CrossRef]
  23. Kishitani, S.; Takanami, T.; Suzuki, M.; Oikawa, M.; Yokoi, S.; Ishitani, M.; Alvarez-Nakase, A.M.; Takabe, T. Compatibility of glycinebetaine in rice plants: Evaluation using transgenic rice plants with a gene for peroxisomal betaine aldehyde dehydrogenase from barley. Plant Cell Environ. 2000, 23, 107–114. [Google Scholar] [CrossRef]
  24. Shirasawa, K.; Takabe, T.; Takabe, T.; Kishitani, S. Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann. Bot. 2006, 98, 565–571. [Google Scholar] [CrossRef]
  25. Soren, K.R.; Ali, K.; Tyagi, V.; Tyagi, A. Recent advances in molecular breeding of drought tolerance in rice (Oryza sativa L.). Indian J. Biotechnol. 2010, 9, 233–251. [Google Scholar]
  26. Farooq, M.; Basra, S.M.A.; Wahid, A.; Cheema, Z.A.; Cheema, M.A.; Khaliq, A. Physiological role of exogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). J. Agron. Crop Sci. 2008, 194, 325–333. [Google Scholar] [CrossRef]
  27. Cha-um, S.; Samphumphuang, T.; Kirdmanee, C. Glycinebetaine alleviates water deficit stress in indica rice using proline accumulation, photosynthetic efficiencies, growth performances and yield attributes. Aust. J. Crop Sci. 2013, 7, 213–218. [Google Scholar]
  28. Jalal-ud-Din; Khan, S.U.; Khan, A.; Naveed, S. Effect of exogenously applied kinetin and glycinebetaine on metabolic and yield attributes of rice (Oryza sativa L.) under drought stress. Emir. J. Food Agric. 2015, 27, 75–81. [Google Scholar] [CrossRef]
  29. Mäkelä, P.; Peltonen-Sainio, P.; Jokinen, K.; Pehu, E.; Setälä, H.; Hinkkanen, R.; Somersalo, S. Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Sci. 1996, 121, 221–223. [Google Scholar] [CrossRef]
  30. Agboma, P.C.; Sinclair, T.R.; Jokinen, K.; Peltonen-Sainio, P.; Pehu, E. An evaluation of the effect of exogenous glycinebetaine on the growth and yield of soybean: Timing of application, watering regimes and cultivars. Field Crop Res. 1997, 54, 51–64. [Google Scholar] [CrossRef]
  31. Xing, W.; Rajashekar, C.B. Alleviation of water stress in beans by exogenous glycine betaine. Plant Sci. 1999, 148, 185–195. [Google Scholar] [CrossRef]
  32. Cruz, F.J.R.; Castro, G.L.S.; Silva Júnior, D.D.; Festucci-Buselli, R.A.; Pinheiro, H.A. Exogenous glycine betaine modulates ascorbate peroxidase and catalase activities and prevent lipid peroxidation in mild water-stressed Carapa guianensis plants. Photosynthetica 2013, 51, 102–108. [Google Scholar] [CrossRef]
  33. Kurepin, L.V.; Ivanov, A.G.; Zaman, M.; Pharis, R.P.; Hurry, V.; Hüner, N.P.A. Interaction of glycine betaine and plant hormones: Protection of the photosynthetic apparatus during abiotic stress. In Photosynthesis, Structures, Mechanisms and Applications; Hou, H.J.M., Najafpour, M.M., Moore, G.F., Allakhverdiev, S.I., Eds.; Springer International Publishing: New York, NY, USA, 2017; pp. 185–202. [Google Scholar]
  34. Wasusun, A.; Wongpiyachon, S.; Songchitsomboon, S.; Sukviwat, W.; Maneenin, P.; Pakkethaiti, S. Rice variety RD43: Medium glycemic index rice for niche market. Thai Rice Res. J. 2017, 8, 45–53. [Google Scholar]
  35. Suwannaporn, P.; Pitiphunpong, S.; Champangern, S. Classification of rice amylose content by discriminant analysis of physicochemical properties. Starch 2007, 59, 171–177. [Google Scholar] [CrossRef]
  36. Pengkumsri, N.; Chaiyasut, C.; Saenjum, C.; Sirilun, S.; Peerajan, S.; Suwannalert, P.; Sirisattha, S.; Sivamaruthi, B.S. Physicochemical and antioxidative properties of black, brown and red rice varieties of northern Thailand. Food Sci. Technol. 2015, 35, 331–338. [Google Scholar] [CrossRef] [Green Version]
  37. Pongprayoon, W.; Tisarum, R.; Theerawitaya, C.; Cha-um, S. Evaluation and clustering on salt-tolerant ability in rice genotypes (Oryza sativa L. subsp. indica) using multivariate physiological indices. Physiol. Mol. Biol. Plant 2019. [Google Scholar] [CrossRef]
  38. Bates, L.S.; Waldren, R.P.; Teare, I.D. Rapid determination of free proline for water-stress studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
  39. Shabala, S.N.; Shabala, S.I.; Martynenko, A.I.; Babourina, O.; Newman, I.A. Salinity effect on bioelectric activity growth, Na+ accumulation and chlorophyll fluorescence of maize leaves: A comparative survey and prospects for screening. Aust. J. Plant Physiol. 1998, 25, 609–616. [Google Scholar] [CrossRef]
  40. Loggini, B.; Scartazza, A.; Brugnoli, E.; Navari-Izzo, F. Antioxidant defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol. 1999, 119, 1091–1100. [Google Scholar] [CrossRef]
  41. Maxwell, K.; Johnson, G.N. Chlorophyll fluorescence-a practical guide. J. Exp. Bot. 2000, 51, 659–668. [Google Scholar] [CrossRef]
  42. Cha-um, S.; Supaibulwatana, K.; Kirdmanee, C. Glycinebetaine accumulation, physiological characterizations and growth efficiency in salt-tolerant and salt-sensitive lines of indica rice (Oryza sativa L. ssp. indica) in response to salt stress. J. Agron. Crop Sci. 2007, 193, 157–166. [Google Scholar]
  43. Harinasut, P.; Tsutsui, K.; Takabe, T.; Nomura, M.; Takabe, T.; Kishitani, S. Exogenous glycinebetaine accumulation and increased salt tolerance in rice seedlings. Biosci. Biotechnol. Biochem. 1996, 60, 366–368. [Google Scholar] [CrossRef]
  44. Demiral, T.; Türkan, I. Exogenous glycinebetaine affects growth and proline accumulation and retards senescence in two rice cultivars under NaCl stress. Environ. Exp. Bot. 2006, 56, 72–79. [Google Scholar] [CrossRef]
  45. Cha-um, S.; Kirdmanee, C. Effect of glycinebetaine on proline, water use and photosynthetic efficiencies, and growth of rice seedlings under salt stress. Turk. J. Agric. For. 2010, 34, 517–527. [Google Scholar]
  46. El-Hendawy, S.E.; Kotab, M.A.; Al-Suhaibani, N.A.; Schmidhalter, U. Optimal coupling combinations between the irrigation rate and glycinebetaine levels for improving yield and water use efficiency of drip-irrigation maize grown under arid conditions. Agric. Water Manag. 2014, 140, 69–78. [Google Scholar] [CrossRef]
  47. Zhao, X.X.; Ma, Q.Q.; Liang, C.; Fang, Y.; Wang, Y.Q.; Wang, W. Effect of glycinebetaine on function of thylakoid membranes in wheat flag leaves under drought stress. Biol. Plant. 2007, 51, 584–588. [Google Scholar] [CrossRef]
  48. Ma, Q.Q.; Wang, W.; Li, Y.H.; Li, D.Q.; Zou, Q. Alleviation of photoinhibition in drought-stressed wheat (Triticumaestivum) by foliar-applied glycinebetaine. J. Plant Physiol. 2006, 163, 165–175. [Google Scholar] [CrossRef]
  49. Gupta, N.; Thind, S.K.; Bains, N.S. Glycine betaine application modifies biochemical attributes of osmotic adjustment in drought stressed wheat. Plant Growth Regul. 2014, 72, 221–228. [Google Scholar] [CrossRef]
  50. Ma, X.L.; Wang, Y.J.; Xie, S.L.; Wang, C.; Wang, W. Glycinebetaine application ameliorates negative effects of drought stress in tobacco. Russ. J. Plant Physiol. 2007, 54, 472–479. [Google Scholar] [CrossRef]
  51. Iqbal, N.; Ashraf, Y.; Ashraf, M. Modulation of endogenous levels of some key organic metabolites by exogenous application of glycine betaine in drought stressed plants of sunflower (Helianthus annuus L.). Plant Growth Regul. 2011, 63, 7–12. [Google Scholar] [CrossRef]
  52. Mahouachi, J.; Argamasilla, R.; Gómez-Cadenas, A. Influence of exogenous glycine betaine and abscisic acid on papaya in responses to water-deficit stress. J. Plant Growth Regul. 2012, 31, 1–10. [Google Scholar] [CrossRef]
  53. Hussain, M.; Malik, M.A.; Farooq, M.; Ashraf, M.Y.; Cheema, M.A. Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J. Agron. Crop Sci. 2008, 194, 193–199. [Google Scholar] [CrossRef]
  54. Osman, H.S. Enhancing antioxidant-yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Ann. Agric. Sci. 2015, 60, 389–402. [Google Scholar] [CrossRef]
  55. Anjum, S.A.; Farooq, M.; Wang, L.C.; Xue, L.L.; Wang, S.G.; Wang, L.; Zhang, S.; Chen, M. Gas exchange and chlorophyll synthesis of maize cultivars are enhanced by exogenously-applied glycinebetaine under drought conditions. Plant Soil Environ. 2011, 57, 326–331. [Google Scholar] [CrossRef] [Green Version]
  56. Rezaei, M.A.; Jokar, I.; Ghorbanli, M.; Kaviani, B.; Kharabian-Masouleh, A. Morpho-physiological improving effects of exogenous glycine betaine on tomato (Lycopersicum esculentum Mill.) cv. PS under drought stress conditions. Plant Omic 2012, 5, 79–86. [Google Scholar]
  57. Gupta, N.; Thind, S.K. Improving photosynthetic performance of bread wheat under field drought stress by foliar applied glycine betaine. J. Agric. Sci. Technol. 2015, 17, 75–86. [Google Scholar]
  58. Cha-um, S.; Supaibulwatana, K.; Kirdmanee, C. Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativa L. ssp. indica cv. KDML105) to salt stress by application of exogenous glycinebetaine and choline. J. Agron. Crop Sci. 2006, 192, 25–36. [Google Scholar] [CrossRef]
Agronomy 09 00138 g001 550
Figure 1. Free proline in two different rice genotypes, RD43 (a) and SPR1 (b), exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 0, 2, 4, 6, 8, 14 (water withholding), and 17 (recovery) days under greenhouse conditions. Error bars represent ± SE. Different letters in each bar represent significant difference at p ≤ 0.05 according to Tukey’s honest significant difference (HSD).
Figure 1. Free proline in two different rice genotypes, RD43 (a) and SPR1 (b), exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 0, 2, 4, 6, 8, 14 (water withholding), and 17 (recovery) days under greenhouse conditions. Error bars represent ± SE. Different letters in each bar represent significant difference at p ≤ 0.05 according to Tukey’s honest significant difference (HSD).
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Figure 2. Total chlorophyll content (a,b), and net photosynthetic rate (c,d) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions. Error bars represent ± standard error (SE). Different letters in each bar represent significant difference at p ≤ 0.05 according to Tukey’s HSD.
Figure 2. Total chlorophyll content (a,b), and net photosynthetic rate (c,d) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions. Error bars represent ± standard error (SE). Different letters in each bar represent significant difference at p ≤ 0.05 according to Tukey’s HSD.
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Figure 3. Relationships between chlorophyll a content (Chla) and maximum quantum yield of PSII (Fv/Fm) (a,b), and total chlorophyll content (TC) and photon yield of PSII (ΦPSII) (c,d) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions. Error bars represent ±SE.
Figure 3. Relationships between chlorophyll a content (Chla) and maximum quantum yield of PSII (Fv/Fm) (a,b), and total chlorophyll content (TC) and photon yield of PSII (ΦPSII) (c,d) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions. Error bars represent ±SE.
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Figure 4. Relationships between photon yield of PSII (ΦPSII) and net photosynthetic rate (Pn) (a,b), and Pn and panicle weight (c,d) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions. Error bars represent ±SE.
Figure 4. Relationships between photon yield of PSII (ΦPSII) and net photosynthetic rate (Pn) (a,b), and Pn and panicle weight (c,d) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions. Error bars represent ±SE.
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Table
Table 1. Shoot height (SH), number of leaves (NL), number of tiller (NT) and flag leaf area (FLA) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions.
Table 1. Shoot height (SH), number of leaves (NL), number of tiller (NT) and flag leaf area (FLA) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions.
Water RegimesGlyBetRD43SPR1
SH (cm)NLNTFLA (mm2)SH (cm)NLNTFLA (mm2)
WW095.47a3.67a11.00a8158ab107.67a3.33a7.67a8647a
10096.28a3.50a10.00ab8865a105.05a3.17a7.67a10176a
MWD092.10b3.33a9.33b7183bc105.70a3.20a6.00b5314b
10093.17ab3.50a9.50b9393a107.88a3.27a6.33ab8695a
SWD090.48b2.00b9.00b3857d92.13c1.60b5.80b3848b
10092.13b2.67b9.33b6287c106.84a1.83b6.00b5962b
Significant level
Water ********nsns**
GlyBet nsnsns**********
Water×GlyBet nsnsnsns*****
ns, *, and ** represent not-significant, and significant difference at p ≤ 0.05 and p ≤ 0.01, respectively. Different letters in each column represent significant difference at p ≤ 0.05 according to Tukey’s HSD.
Table
Table 2. Panicle weight (PW), panicle length (PL), seed fertility (SF) and hundred grain weight (HGW) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) as well as recovery until harvesting stage under greenhouse conditions.
Table 2. Panicle weight (PW), panicle length (PL), seed fertility (SF) and hundred grain weight (HGW) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) as well as recovery until harvesting stage under greenhouse conditions.
Water RegimesGlyBetRD43SPR1
PW (g)PL (cm)SF (%)HGW(g)PW (g)PL (cm)SF (%)HGW (g)
WW03.63a27.91a66.18ab2.61a2.49a27.08ab70.34a2.66a
1003.49ab27.85a72.08a2.58a2.88a28.03a70.27a2.69a
MWD02.61c25.32b65.58ab2.56a1.77bc24.80cd48.98b2.58a
1003.13b 26.95ab69.25ab2.48a2.03b25.78bc55.83a2.55a
SWD01.22e20.82c26.84d2.23b0.91d22.01e17.61c2.13b
1002.22d25.50b48.19c2.54a1.54c23.25de31.86b2.58a
Significant level
Water ****************
GlyBet ****ns*********
Water×GlyBet ********nsns****
ns, *, and ** represent not-significant, and significant difference at p ≤ 0.05 and p ≤ 0.01, respectively. Different letters in each column represent significant difference at p ≤ 0.05 according to Tukey’s HSD.
Table
Table 3. Chlorophyll a (Chla; μg g−1 FW), chlorophyll b (Chlb; μg g−1 FW), maximum quantum yield of PSII (Fv/Fm) and photon yield of PSII (ΦPSII) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions.
Table 3. Chlorophyll a (Chla; μg g−1 FW), chlorophyll b (Chlb; μg g−1 FW), maximum quantum yield of PSII (Fv/Fm) and photon yield of PSII (ΦPSII) in two different rice genotypes, RD43 and SPR1, exogenously applied with (100 mM GlyBet) or without GlyBet, and subsequently subjected to well watering (WW) and water withholding for 8 (mild water deficit, MWD) and 14 days (severe water deficit, SWD) under greenhouse conditions.
Water RegimesGlyBetRD43SPR1
ChlaChlbFv/FmΦPSIIChlaChlbFv/FmΦPSII
WW0146.76a197.09a0.836a0.675b167.92ab195.04ab0.877a0.789a
100162.15a184.27a0.845a0.744a185.44a235.51a0.888a0.787a
MWD094.41b137.34ab0.813ab0.607b142.35b192.57ab0.827a0.780a
100126.62ab141.35ab0.879a0.724a170.18ab223.35a0.847a0.784a
SWD062.59c105.44b0.477b0.344d130.38b170.63b0.681c0.458b
100135.45ab149.70ab0.809ab0.453c153.79ab181.65ab0.786b0.786a
Significant level
Water ****************
GlyBet nsnsns**nsns*ns
Water×GlyBet *********
ns, *, and ** represent not-significant, and significant difference at p ≤ 0.05 and p ≤ 0.01, respectively. Different letters in each column represent significant difference at p ≤ 0.05 according to Tukey’s HSD.

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Tisarum, R.; Theerawitaya, C.; Samphumphung, T.; Takabe, T.; Cha-um, S. Exogenous Foliar Application of Glycine Betaine to Alleviate Water Deficit Tolerance in Two Indica Rice Genotypes under Greenhouse Conditions. Agronomy 2019, 9, 138. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy9030138

AMA Style

Tisarum R, Theerawitaya C, Samphumphung T, Takabe T, Cha-um S. Exogenous Foliar Application of Glycine Betaine to Alleviate Water Deficit Tolerance in Two Indica Rice Genotypes under Greenhouse Conditions. Agronomy. 2019; 9(3):138. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy9030138

Chicago/Turabian Style

Tisarum, Rujira, Cattarin Theerawitaya, Thapanee Samphumphung, Teruhiro Takabe, and Suriyan Cha-um. 2019. "Exogenous Foliar Application of Glycine Betaine to Alleviate Water Deficit Tolerance in Two Indica Rice Genotypes under Greenhouse Conditions" Agronomy 9, no. 3: 138. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy9030138

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