Globally rice (
Oryza sativa L.) is a major food crop, for production and consumption, comparable to other food crops like wheat
(Todaka et al., 2015). In 2013, rice cultivation was recorded from 124 countries around the world andproduction stood at 745 million tons (FAOSTAT). In a recent report
(Dar et al., 2020) the effect of drought on food security has been reviewed in Eastern India. Rice acts as a source of staple food for more than three billion people and served as a source of daily calorie intake
(Khush, 2005). In rice, both reductions of growth and yield loss occurred due to the effect of drought
(Basu et al., 2016). In the farming of rice, water is a necessity which again is a highly limited resource
(Wang et al., 2012). Rice is very sensitive to drop in soil water content and also requires plenty of water for production compared to other cereal crops, normally 3,000 to 5,000 liters of water, are required for 1 kg of rice seeds production which is much higher than wheat and others crops
(Singh et al., 2002). Drought is the meteorological event, which implies the absence of rainfall for a period of time, long enough to cause moisture depletion in soil and water deficit with a decrease of water potential in plant tissues
(Kramer, 1980). The rice ecosystem mostly suffers from drought at the time of flowering stage in both upland and lowland
(Mishra and Chaturvedi, 2018). In rice, drought stress affects in various ways during rice production, which globally affects almost 23 million hectares of rice field, which are rain fed
(Serraj et al., 2011). Lacks of proper water supply to the root, high transpiration rates are the main reason of drought stress and it effects growth, development and ultimately the yield
(Pandey and Shukla, 2015). Being a water loving crop, rice production gets severely impaired by drought stress; a 15% to 50% yield loss has been noted depending on the vigour and period of stress given
(Srividhya et al., 2011). At the time of reproductive growth, a sharp decline in grain yield occurred when rice plant subjected to even moderate levels of drought stress
(Venuprasad et al., 2008). The yield of a grain crop is a function of the rate and duration of accumulation of dry weight in the economically valuable parts of the plant
(Rahman and Yoshida, 1985). Besides grain size, the duration and rate of grain filling also determine the final grain weight and thereby contribute greatly to grain productivity
(Takai et al., 2005). In two recent reports
(Berahim et al., 2021; Kumar et al., 2021) the effect of induced drought was studied on different yield related parameters along with stomatal performances. Four components contribute to potential rice grain yield that are grain weight, grain number per panicle, panicle number per plant andthe ratio of filled grains
(Sakamoto and Matsuoka, 2008). It has been documented that grain weight was largely determined by grain filling
(Wang et al., 2008). Rice grain filling is nothing but a process of starch accumulation, as starch contributes 80% to 90% of the final dry weight of brown rice
(Zhu et al., 2011). Grain filling is a process which occurs as a complex series of events, including the relocation of carbohydrates synthesized by photosynthetic organs and biosynthesis of starch from sucrose in the developing endosperm
(Peng et al., 2013). The main component of rice endosperm is starch and thus incomplete grain filling is generally due to defects in starch synthesis
(Zhu et al., 2011). In hybrid cultivars, the vital reason for fluctuation in grain yield is attributed to poor grain filling of the later-flowering spikelets of rice, which is itself is a serious problem
(Yang and Zhang, 2010). As a result of climate change, there is a possibility of reduction of yield, in a limited water resource
(Ray et al., 2015). In two independent studies
(Melandri et al., 2021 and
Panda et al., 2021) reported all the different mechanisms behind the drought tolerance in rice in details. A recent report made by
Kumar et al., (2020) showed that drought have a major role in quantity and chemistry of resistant starch content and Glycemic index of rice grain during development. Therefore, research on the grain filling in rice in response to stress is essential for us to increase our understanding to employ strategies to combat drought stress, through which grain weight can be enhanced, consequently increasing the grain yield per plant
(Peng et al., 2013). For that reason, basic requirement is to know the mechanism of drought tolerance potentiality of plant for better yield in limited rainfall
(Mostajeran and Rahimi, 2009). It can be achieved through development of short duration high yielding lines through breeding or transgenics, which may give better yield under environmental stress
(Singh et al., 2012). Considering this significant requirement and lacunae, an initiation was taken in present study where a detailed account has been taken on biochemical basis and mechanism of grain filling during developmental stages and how drought alter the grain filling mechanism. Finally, the possible management practices which can be employed to overcome the effect of drought on grain development stage have been discussed.
Grain filling in rice
In rice, the flowering stage is vital, as it is the stage when the meiosis cell division starts andafter that panicle initiation starts from flag leaf
(Biswal and Kholi, 2013). Grain filling is mainly visible when a milky liquid fills the grains, this is the main reason for the increase of dry weight of the grain
(Zhang et al., 2012). Rice grain filling is a process of starch accumulation since starch contributes 80% to 90% of the final dry weight of an unpolished grain
(Duan and Sun, 2005). Initially from sucrose, biosynthesis of starch takes place in the developing endosperm which in turn determines grain yield and rice quality
(Zhu et al., 2011). Roles of several crucial enzymes have been documented in the pathway of starch synthesis and
(Tetlow et al., 2004); these are sucrose synthase (
SUS), UDP-glucose pyrophosphorylase (
UG Pase), ADP-glucose pyrophosphorylase (
AGPase) andstarch synthase. Among these
Sus3 is highly specific to the grain
(Huang et al., 1996). Starch synthase has been found to exist in two different forms and these are granule-bound starch synthase (
GBSS) and soluble starch synthase (
SSS)
(Zhu et al., 2011). GBSSI is also called Waxy (
Wx), both
Wx and
SSIIa are highly specific for grains
(Chen et al., 2012). Synthesis of amylopectin is more complicated than amylose and involves all four types of enzymes including AGPase,
SSS, Starch branching enzyme (
SBE) andstarch de branching enzyme (
DBE)
(Jeon et al., 2010). It was observed that after 3 days to 15 days from pollination, some phytohormones like Auxin, ABA and Zeatin concentrations notably increased
(Abu et al., 2012). Cytokinin levels in rice spikelets are significantly correlated with seed development
(Zhang et al., 2009). Negative correlation has been found between levels of ethylene in developing seeds and enzymatic activities linked with starch metabolism eventually leading to poor grain filling, for instance more ethylene levels in developing seeds leads to poor grain filling
(Zhang et al., 2009). A detailed description of the metabolic pathways associated with sucrose to starch conversion in developing grain particularly during grain filling stage was recently reported by
Jiang et al., (2021). Comparative genomics study through transcriptome profiling among two rice genotypes under mild drought during grain-filling stage was conducted by
Liang et al., (2021) and in a suppressed transgenic line of the
OsSYT-5 gene,
Shanmugam et al., (2021) reported the enhanced photosynthetic rate with reduced stomatal conductance and transpiration under water deficit condition. A diagrammatic flow chart describing the major biochemical pathways associated with grain filling in rice in described in Fig 1.
It was noted that when concentrations of ABA increased, transportation of sucrose into the grains got reduced which lowered the ability of grains to synthesize starch
(Bhatia and Singh 2002), surprisingly it was also seen that optimum concentrations of Abscisic acid (ABA) augmented SUS activity
(Tang et al., 2009). During embryo development, it was observed that enhanced Gibberellic acid (GA) concentrations at initial grain filling stages contributed significantly towards rapid enlargement of the embryo
(Yang et al., 2002).
Key changes during drought stress in rice
When drought occurs, usually plant growth rate reduced
(Zhu et al., 2004) and poor root development happens with reduced leaf surface
(Pandey and Shukla, 2015). Leaf rolling is a common phenomenon and it is used as a criterion for scoring drought tolerance
(Kadioglu and Terzi, 2007). As turgor pressure reduces under stress, cell growth severely decreases
(Taiz and Zeiger, 2006). Common effects of drought stress are mainly reduction of germination
(Swain et al., 2014), inhibition of plant height as well as growth
(Sokoto and Muhammod, 2014) and also reduction of panicle number
(Bunnag and Pongthai, 2013). Net photosynthesis
(Yang et al., 2014) and rate of transpiration are also affected by water stress
(Cabuslay et al., 2002) along with stomatal conductance
(Singh et al., 2013). It has been proved that drought affects efficiency of water utilization and reduces photosynthetic rate of rice plants.
(Yang et al., 2014). Drought reduces photosynthesis in flag leaf by inhibiting PSII activity
(Pieters and Souki, 2005). Rubisco enzyme activity sharply decreases during drought, which is the key enzyme of the Calvin cycle
(Zhou et al., 2007). Decrease in chlorophyll content has also been reported on drought stressed rice plants
(Maisura et al., 2014). A positive correlation is present between relative wWater content (RWC) and water use efficiency (WUE) during drought stress but transpiration rate has negative correlation with WUE
(Akram et al., 2013). In cytoplasm, several osmolyte accumulates for osmotic adjustment, among these proline was found to play a major role in drought stress tolerance mechanism
(Pandey and Shukla, 2015). It was observed that accumulation of soluble sugars was also induced during drought
(Maisura et al., 2014). Proline acts as an osmolyte and it helps for better maintenance and also imparts drought tolerance
(Vajrabhaya et al., 2001). Some positively charged molecules like Polyamines (PAs) are also involved in the response to drought
(Calzadilla et al., 2014). Reactive oxygen species (ROS) generation is a common phenomenon in response to drought stress
(Faize et al., 2011), which includes super oxide radical and others free radicals like hydrogen peroxide and several forms of singlet oxygen. In plants, ROS generation is the main reason for protein, nucleic acid damage and also lipid peroxidation
(Pandey et al., 2015). Up-regulation of 5000 genes and down-regulation of more than 6000 genes were observed in rice during drought period as reported
(Maruyama et al., 2014). Up regulation of
DREB transcription factors in response to drought also play major role in ABA-independent pathway, particularly two transcription factors,
OsDREB2A and
OsDREB2B expression are in high levels during water stress
(Matsukura et al., 2010). The
OREB1bZIP-type transcription factor also regulates the ABA-dependent pathway in rice
(Hong et al., 2011). A summary on overall impact of drought stress on rice plant is presented in Fig 2.
Impact of drought on grains filling
Three phases during rice plant development that have an impact on grain yield are: Vegetative, reproductive and ripening stages in which drought conditions cause spikelet sterility and unfilled grains
(Ndjiondjop et al., 2010). It was found that drought stress impaired seed germination and early seedling growth, reduced plant growth and development in the vegetative phase, delayed flowering at the reproductive phase anddecreased the rate of grain filling
(Ndjiondjop et al., 2010). Due to water stress, photosynthesis in leaf and flag leaf gets reduced which affects grain filling and which results in low yield in rice
(Pandey and Shukla, 2015). During drought stress, reduction of seeds setting was observed with grain size and weight, due to spikelet sterility
(Raman et al., 2012). During booting stage, drought stress can effect in various ways
(Pantuwan et al., 2002), like floret initiation is interrupted by flowering in terminal periods, resulting in slow grain filling and spikelet sterility, eventually causing low grain weight and as a consequence of which poor paddy yield
(Pandey and Shukla, 2015). Reduction in grain yield due to drought occurs probably by decreased grain filling period
(Shahryari et al., 2008) along with disruption of leaf and gas exchange properties and the most important grain filling, source and sink translocation also gets affected due to drought stress
(Farooq et al., 2009). Water stress can decrease pollen viability by degrading starch of pollen, as result of which pollens grains fail to fertilize the egg
(Liu et al., 2006). Sterile panicles increase due to drought in booting phase
(Pantuwan et al., 2002) and mild drought in grain filling stage can decrease yield upto 14.7%
(Cai et al., 2006), whereas upto 52% yield loss was observed due to severe drought during grain filling
(Yambao and Ingraml, 1988). In drought stressed tice plants, it was observed that ethylene concentration increases in the rice grain at the early grain-filling stage but decreases during grain development
(Yang et al., 2004). Significant yield devastation occurred when water stress was perceived during flowering stage
(Yang et al., 2004). Since drought can directly affect flowering, it also results in abortion of flower and one of the major causes for unfilled grain formation and grain abscission
(Hsiao et al., 1976). High percentages of unfilled grains were also noted due to drought during reproductive growth stage
(Davatgar et al., 2009). This happens because of reduction of assimilate translocation towards tiller of the plant
(Rahman et al., 2002). Key enzymes which played an important role in active grain filling process includes enzymes like invertases, sucrose synthase, ADP glucose pyrophosphorylase (AGPase) andstarch synthase as well as the starch branching and the debranching enzymes all of which are affected by drought stress
(Sheoran and Saini, 1996). Delayed in flowering time due to water stress was found to be closely associated with filling of grains that ultimately hampered the crop yielding
(Pantuwan et al., 2002).
Management of drought stress for better grains filling and yield
Management through transgenic rice
One of the modern management strategies for drought stress is the development of transgenic rice. In such transgenic rice, over expression of
OsDREB2A and
OsDREB2B genes have been found to increase drought tolerance
(Cui et al., 2011). ROS accumulation and its subsequent modulation by manganese superoxide dismutase, an anti-oxidant enzyme encoded by transgenic rice plants over expressing the gene
mnSOD have resulted in superior osmotic tolerance
(Wang et al., 2005). Several traits of rice which include spikelet fertility, grain filling and major yield traits like panicle number per plant, grain number per plant can be achieved through cultivation of transgenic rice plants over expressing
NAC5 (Jeong et al., 2013). Drought tolerant transgenic rice plants over expressing
OsOAT have also increased heading than normal rice, in response to drought during panicle heading stage
(You et al., 2012). In transgenic rice, it was seen that grain yield was high through high grain filling during drought condition in field on the time of heading and this was observed as a result of over expression of
AP37 gene along with other transcription factor,
AP2/ERF (Oh et al., 2009). Improvement of drought tolerance by silencing OsSYT
-5 gene has been reported by
Shanmugam et al., (2021).
Management through hybridization
The first step towards development of drought tolerant crop plants is the identification of genetic variation responsible for drought resistance (DR) but improvement of such desirable DR attributes in crop plants is a critical challenge for plant breeders and crop physiologists since the drought resistance involves a complex genetic trait with multiple pathways
(Basu et al., 2016). Drought management is possible through development of short cycle hybrid rice, with very fast reproductive cycle and which are able to produce seeds before on set of drought stress
(Yue et al., 2006). Farming of such short duration cultivars is effective as it has short grain filling period and these rice lines possessing various adaptive mechanisms which helps to escape terminal drought occurring during the reproductive stage. Hybrid rice with long flag leaf has great positive impact on yield under drought stress
(Kumar et al., 2021). Hybrid varieties can tolerate drought by controlling stomatal opening and water conduction in root by producing Spermidine (SPD)
(Berahim et al., 2021).
An overview on general approach of drought stress management in rice is presented in Fig 3.
