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MAIN CONCLUSION: Stomatal traits in rice genotypes affect water use efficiency. Low-frequency small-size stomata correlate with whole plant efficiency, while low-frequency large-size stomata show intrinsic efficiency and responsiveness to vapour pressure deficit. Leaf surface and the patterning of the epidermal layer play a vital role in determining plant growth. While the surface helps in determining radiation interception, epidermal pattern of stomatal factors strongly regulate gas exchange and water use efficiency (WUE). This study focuses on identifying distinct stomatal traits among rice genotypes to comprehend their influence on WUE. Stomatal frequency ranged from 353 to 687 per mm2 and the size varied between 128.31 and 339.01 µm2 among 150 rice germplasm with significant variability in abaxial and adaxial surfaces. The cumulative water transpired and WUE determined at the outdoor phenomics platform, over the entire crop growth period as well as during specific hours of a 24 h-day did not correlate with stomatal frequency nor size. However, genotypes with low-frequency and large-size stomata recorded higher intrinsic water use efficiency (67.04 µmol CO2 mol-1 H2O) and showed a quicker response to varying vapour pressure deficit that diurnally ranged between 0.03 and 2.17 kPa. The study demonstrated the role of stomatal factors in determining physiological subcomponents of WUE both at single leaf and whole plant levels. Differential expression patterns of stomatal regulatory genes among the contrasting groups explained variations in the epidermal patterning. Increased expression of ERECTA, TMM and YODA genes appear to contribute to decreased stomatal frequency in low stomatal frequency genotypes. These findings underscore the significance of stomatal traits in breeding programs and strongly support the importance of these genes that govern variability in stomatal architecture in future crop improvement programs.
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Genotipo , Oryza , Hojas de la Planta , Estomas de Plantas , Transpiración de Plantas , Agua , Oryza/genética , Oryza/fisiología , Oryza/crecimiento & desarrollo , Estomas de Plantas/fisiología , Estomas de Plantas/genética , Agua/metabolismo , Hojas de la Planta/genética , Hojas de la Planta/fisiología , Hojas de la Planta/crecimiento & desarrollo , Hojas de la Planta/anatomía & histología , Transpiración de Plantas/fisiología , Presión de VaporRESUMEN
Water-saving attempts for rice cultivation often reduce yields. Maintaining productivity under drought is possible when rice genotypes are bred with improved metabolism and spikelet fertility. Although attempts have been made to introgress water mining and water use efficiency traits, combining acquired tolerance traits (ATTs), that is, specific traits induced or upregulated to better tolerate severe stress, appears equally important. In our study, we screened 90 rice germplasm accessions that represented the molecular and phenotypic variations of 851 lines of the 3 K rice panel. Utilising phenomics, we identified markers linked to ATTs through association analysis of over 0.2 million SNPs derived from whole-genome sequences. Propensity to respond to 'induction' stress varied significantly among genotypes, reflecting differences in cellular protection against oxidative stress. Among the ATTs, the hydroxyl radical and proline contents exhibited the highest variability. Furthermore, these significant variations in ATTs were strongly correlated with spikelet fertility. The 43 significant markers associated with ATTs were further validated using a different subset of contrasting genotypes. Gene expression studies and metabolomic profiling of two well-known contrasting genotypes, APO (tolerant) and IR64 (sensitive), identified two ATT genes: AdoMetDC and Di19. Our study highlights the relevance of polyamine biosynthesis in modulating ATTs in rice. Genotypes with superior ATTs and the associated markers can be effectively employed in breeding rice varieties with sustained spikelet fertility and grain yield under drought.
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Oryza , Oryza/genética , Oryza/metabolismo , Sequías , Genotipo , Agua/metabolismo , MetabolomaRESUMEN
Mild stresses induce "acquired tolerance traits" (ATTs) that provide tolerance when stress becomes severe. Here, we identified the genetic variability in ATTs among a panel of rice germplasm accessions and demonstrated their relevance in protecting growth and productivity under water-limited conditions. Diverse approaches, including physiological screens, association mapping and metabolomics, were adopted and revealed 43 significant marker-trait associations. Nontargeted metabolomic profiling of contrasting genotypes revealed 26 "tolerance-related-induced" primary and secondary metabolites in the tolerant genotypes (AC-39000 and AC-39020) compared to the susceptible one (BPT-5204) under water-limited condition. Metabolites that help maintain cellular functions, especially Calvin cycle processes, significantly accumulated more in tolerant genotypes, which resulted in superior photosynthetic capacity and hence water use efficiency. Upregulation of the glutathione cycle intermediates explains the ROS homeostasis among the tolerant genotypes, maintaining spikelet fertility, and grain yield under stress. Bioinformatic dissection of a major effect quantitative trait locus on chromosome 8 revealed genes controlling metabolic pathways leading to the production of osmolites and antioxidants, such as GABA and raffinose. The study also led to the identification of specific trait donor genotypes that can be effectively used in translational crop improvement activities.
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Sequías , Oryza , Metabolómica , Oryza/metabolismo , Sitios de Carácter Cuantitativo/genética , Agua/metabolismoRESUMEN
Drought-induced abscisic acid (ABA) accumulation plays a key role in plant water relations by regulating stomatal movements. Although ABA helps in the survival of the plants, reduced carbon gain affects plant productivity. To improve crop productivity under mild drought stress conditions, it is necessary to manipulate ABA responses. Other research groups have used forward chemical genomics for the identification of ABA agonists and antagonists aiming to manipulate ABA biosynthesis and signalling. In the present study, we identified indolyl-ethyl amine and serotonin small molecules using a reverse chemical genomics approach, with these acting as potent inhibitors of ABA biosynthesis through transient regulation of bZIP23 transcription factor activity. In rice, wheat and soybean, each of the small molecules enhanced the germination of seeds, even in the presence of ABA. These molecules nullified the effect of ABA on intact and detached leaves, resulting in higher photosynthesis. Furthermore, these small molecules effectively reduced the transcription levels of bZIP23 targeting NCED4, PP2C49 and CO3 genes. Rice plants treated with the small molecules were found to have improved stomatal conductance, spikelet fertility and yield compared to untreated plants under mild drought stress conditions. Our results suggest that indolyl-ethyl amine and serotonin small molecules could be utilized to improve yield under mild drought conditions.
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Ácido Abscísico , Oryza , Ácido Abscísico/farmacología , Carbono , Sequías , Regulación de la Expresión Génica de las Plantas , Oryza/genética , Oryza/metabolismo , Fotosíntesis , Serotonina , Factores de Transcripción/genética , Agua/metabolismoRESUMEN
Drought significantly decreases crop productivity, especially in high water consuming crops like rice. Grain filling is one of the important critical growth phases in rice and drought during this phase leads to significant reduction in yield. In this study, a comparison was made between IR64 (drought susceptible) and Apo (drought tolerant) rice genotypes to capture the response to water limitation (50% field capacity (FC)) compared with the control (100%FC) during grain filling. Plants were grown in a high-throughput phenomics facility for precise imposition of moisture stress during grain filling. Apo performed better in water limited conditions with lower reduction of photosynthetic rate and maintenance of lower leaf temperature than IR64. Days from sowing to maturity, spikelet fertility and seed weight were more impeded by water limitation in IR64 than in Apo. Unlike Apo, IR64 did not show any decrease in transpiration rate at 50%FC compared with 100%FC. Metabolomic profiling of spikelets at grain filling showed distinct effects of water limitation on accumulation of metabolites, especially in Apo. Secondary metabolism, mainly the phenylpropanoid pathway involved in scavenging mechanisms, was upregulated in Apo. Accumulation of most amino acids was significantly higher in IR64 than in Apo. Due to higher rates of photosynthesis under stress, most carbohydrates accumulated more in Apo than in IR64 at 50%FC. Sucrose transporters were significantly upregulated in water limited conditions especially in Apo. Overall, thanks to higher source capacity, more source to sink transport and better scavenging, Apo showed a lower reduction in yield than IR64.
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Oryza , Grano Comestible , Genotipo , Metaboloma , Oryza/genética , AguaRESUMEN
Drought tolerance is governed by constitutive and acquired traits. Combining them has relevance for sustaining crop productivity under drought. Mild levels of stress induce specific mechanisms that protect metabolism when stress becomes severe. Here, we report a comparative assessment of "acquired drought tolerance (ADT)" traits in two rice cultivars, IR64 (drought susceptible) and Apo (tolerant), and a drought-tolerant wheat cultivar, Weebill. Young seedlings were exposed to progressive concentrations of methyl viologen (MV), a stress inducer, before transferring to a severe concentration. "Induced" seedlings showed higher tolerance and recovery growth than seedlings exposed directly to severe stress. A novel phenomic platform with an automated irrigation system was used for precisely imposing soil moisture stress to capture ADT traits during the vegetative stage. Gradual progression of drought was achieved through a software-controlled automated irrigation facility. This facility allowed the maintenance of the same level of soil moisture irrespective of differences in transpiration, and hence, this platform provided the most appropriate method to assess ADT traits. Total biomass decreased more in IR64 than in Apo. The wheat cultivar showed lower levels of damage and higher recovery growth even compared to Apo. Expression of ROS-scavenging enzymes and drought-responsive genes was significantly higher in Apo than in IR64, but differences were only marginal between Apo and Weebill. The wheat cultivar showed significantly higher stomatal conductance, carbon gain, and biomass than the rice cultivars, under drought. These differences in ADT traits between cultivars as well as between species can be utilised for improving drought tolerance in crop plants.
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Plants have evolved several adaptive mechanisms to cope with water-limited conditions. While most of them are through constitutive traits, certain "acquired tolerance" traits also provide significant improvement in drought adaptation. Most abiotic stresses, especially drought, show a gradual progression of stress and hence provide an opportunity to upregulate specific protective mechanisms collectively referred to as "acquired tolerance" traits. Here, we demonstrate a significant genetic variability in acquired tolerance traits among rice germplasm accessions after standardizing a novel gradual stress progress protocol. Two contrasting genotypes, BPT 5204 (drought susceptible) and AC 39000 (tolerant), were used to standardize methodology for capturing acquired tolerance traits at seedling phase. Seedlings exposed to gradual progression of stress showed higher recovery with low free radical accumulation in both the genotypes compared to rapid stress. Further, the gradual stress progression protocol was used to examine the role of acquired tolerance at flowering phase using a set of 17 diverse rice genotypes. Significant diversity in free radical production and scavenging was observed among these genotypes. Association of these parameters with yield attributes showed that genotypes that managed free radical levels in cells were able to maintain high spikelet fertility and hence yield under stress. This study, besides emphasizing the importance of acquired tolerance, explains a high throughput phenotyping approach that significantly overcomes methodological constraints in assessing genetic variability in this important drought adaptive mechanism.
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[This corrects the article DOI: 10.3389/fchem.2018.00092.].
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Burgeoning population growth, industrial demand, and the predicted global climate change resulting in erratic monsoon rains are expected to severely limit fresh water availability for agriculture both in irrigated and rainfed ecosystems. In order to remain food and nutrient secure, agriculture research needs to focus on devising strategies to save water in irrigated conditions and to develop superior cultivars with improved water productivity to sustain yield under rainfed conditions. Recent opinions accruing in the scientific literature strongly favor the adoption of a "trait based" crop improvement approach for increasing water productivity. Traits associated with maintenance of positive tissue turgor and maintenance of increased carbon assimilation are regarded as most relevant to improve crop growth rates under water limiting conditions and to enhance water productivity. The advent of several water saving agronomic practices notwithstanding, a genetic enhancement strategy of introgressing distinct physiological, morphological, and cellular mechanisms on to a single elite genetic background is essential for achieving a comprehensive improvement in drought adaptation in crop plants. The significant progress made in genomics, though would provide the necessary impetus, a clear understanding of the "traits" to be introgressed is the most essential need of the hour. Water uptake by a better root architecture, water conservation by preventing unproductive transpiration are crucial for maintaining positive tissue water relations. Improved carbon assimilation associated with carboxylation capacity and mesophyll conductance is important in sustaining crop growth rates under water limited conditions. Besides these major traits, we summarize the available information in literature on classifying various drought adaptive traits. We provide evidences that Water-Use Efficiency when introgressed with moderately higher transpiration, would significantly enhance growth rates and water productivity in rice through an improved photosynthetic capacity.
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Membrane damage is a hallmark of both biotic and abiotic stress responses. The membrane determines the ability of a cell to sustain altered environmental conditions and hence can be used as a biomarker to assess stress-induced cell damage or death. We present an easy, quick, cost-effective, staining and spectrophotometric method to assess membrane stability of plant cells. In this method, Evan's blue, an azo dye, is used to assay for cell viability. More specifically, Evan's blue dye can penetrate through ruptured or destabilized membranes and stain cells. Thus, when plant cells are subjected to stress that compromises membrane integrity, the number of cells that are permeated by Evan's blue dye will be increased compared to control cells that are not stressed. In contrast, live, healthy cells that are capable of maintaining membrane integrity do not take up Evan's blue dye. Cells that have taken up Evan's blue dye will have an accumulation of a blue protoplasmic stain and these stained cells can be qualitatively documented under bright field microscopy with or without the use of a camera. Furthermore, the dye can be extracted from cells that are stained by Evan's blue dye and can be quantified spectrophotometrically. Using this analysis, the accumulation of dye in positively-stained cells correlates with the extent of cell membrane damage and thus the amount of cells that are stained with Evan's blue dye under various conditions can be used as an indicator of cellular stress.