Plant heat stress: Concepts directing future research Jagadish, S.V. Krishna; Way, Danielle A.; Sharkey, Thomas D.
Plant, cell & environment/Plant, cell and environment,
July 2021, Volume:
44, Issue:
7
Journal Article
Peer reviewed
Open access
Predicted increases in future global temperatures require us to better understand the dimensions of heat stress experienced by plants. Here we highlight four key areas for improving our approach ...towards understanding plant heat stress responses. First, although the term ‘heat stress’ is broadly used, that term encompasses heat shock, heat wave and warming experiments, which vary in the duration and magnitude of temperature increase imposed. A greater integration of results and tools across these approaches is needed to better understand how heat stress associated with global warming will affect plants. Secondly, there is a growing need to associate plant responses to tissue temperatures. We review how plant energy budgets determine tissue temperature and discuss the implications of using leaf versus air temperature for heat stress studies. Third, we need to better understand how heat stress affects reproduction, particularly understudied stages such as floral meristem initiation and development. Fourth, we emphasise the need to integrate heat stress recovery into breeding programs to complement recent progress in improving plant heat stress tolerance. Taken together, we provide insights into key research gaps in plant heat stress and provide suggestions on addressing these gaps to enhance heat stress resilience in plants.
Predicted increases in future global temperatures require us to better understand the dimensions of heat stress experienced by plants. Here we highlight four key areas for improving our approach towards understanding plant heat stress responses.
Nighttime warming poses a threat to global food security as it is driving yield declines worldwide, but our understanding of the physiological basis of this phenomenon remains very limited. ...Furthermore, it is often assumed that such declines are driven solely by increases in nighttime temperature (TNight). Here we argue that, in addition to temperature, increases in nighttime evaporative demand may ‘conspire’ to penalize yields and end-use quality traits. We propose an ecophysiological framework outlining the possible mechanistic basis of such declines in yield and quality. We suggest ways to use the proposed framework as a guide to future efforts aimed at alleviating productivity losses by integrating crop ecophysiology with modeling, breeding, and management.
Nighttime warming is reducing crop yields worldwide, threatening global food security.This phenomenon is more complex than may be assumed, likely to involve interaction between two driving forces: nighttime temperature and evaporative demand.The two conspire to limit carbon availability for yield and end-use quality traits while decreasing water use efficiency, potentially enhancing vulnerability to droughts.An ecophysiological framework is proposed as a guide to implement future research efforts to mitigate yield declines.Such efforts should integrate physiology with crop modeling, breeding, and management to identify sustainable pathways for mitigation as climate change intensifies.
Carbon loss under high night‐time temperature (HNT) leads to significant reduction in wheat yield. Growth chamber studies were carried out using six winter wheat genotypes, to unravel postheading HNT ...(23°C)–induced alterations in carbon balance, source‐sink metabolic changes, yield, and yield‐related traits compared with control (15°C) conditions. Four of the six tested genotypes recorded a significant increase in night respiration after 4 days of HNT exposure, with all the cultivars regulating carbon loss and demonstrating different degree of acclimation to extended HNT exposure. Metabolite profiling indicated carbohydrate metabolism in spikes and activation of the TriCarboxylic Acid (TCA) cycle in leaves as important pathways operating under HNT exposure. A significant increase in sugars, sugar‐alcohols, and phosphate in spikes of the tolerant genotype (Tascosa) indicated osmolytes and membrane protective mechanisms acting against HNT damage. Enhanced night respiration under HNT resulted in higher accumulation of TCA cycle intermediates like isocitrate and fumarate in leaves of the susceptible genotype (TX86A5606). Lower grain number due to lesser productive spikes and reduced grain weight due to shorter grain‐filling duration determined HNT‐induced yield loss in winter wheat. Traits and mechanisms identified will help catalyze the development of physiological and metabolic markers for breeding HNT‐tolerant wheat.
Carbon loss under high night‐time temperature (HNT) leads to significant yield decline in wheat. Winter wheat genotypes exhibited considerable variation for HNT‐induced enhanced night respiration in flag leaves and acclimation upon extended HNT exposure. Alterations in carbohydrate metabolism in spikes with increased sugars acting as osmoprotectants and activation of TCA cycle in leaves due to enhanced night respiration, provides novel insights into metabolites involved in HNT response in wheat.
Future increases in global surface temperature threaten those worldwide who depend on rice production for their livelihoods and food security. Past analyses of high-temperature stress on rice ...production have focused on paddy yield and have failed to account for the detrimental impact of high temperatures on milling quality outcomes, which ultimately determine edible (marketable) rice yield and market value. Using genotype specific rice yield and milling quality data on six common rice varieties from Arkansas, USA, combined with on-site, half-hourly and daily temperature observations, we show a nonlinear effect of high-temperature stress exposure on yield and milling quality. A 1 °C increase in average growing season temperature reduces paddy yield by 6.2%, total milled rice yield by 7.1% to 8.0%, head rice yield by 9.0% to 13.8%, and total milling revenue by 8.1% to 11.0%, across genotypes. Our results indicate that failure to account for changes in milling quality leads to understatement of the impacts of high temperatures on rice production outcomes. These dramatic losses result from reduced paddy yield and increased percentages of chalky and broken kernels, which together decrease the quantity and market value of milled rice. Recently published estimates show paddy yield reductions of up to 10% across the major rice-producing regions of South and Southeast Asia due to rising temperatures. The results of our study suggest that the often-cited 10% figure underestimates the economic implications of climate change for rice producers, thus potentially threatening future food security for global rice producers and consumers.
Rapid increases in minimum night temperature than in maximum day temperature is predicted to continue, posing significant challenges to crop productivity. Rice and wheat are two major staples that ...are sensitive to high night‐temperature (HNT) stress. This review aims to (i) systematically compare the grain yield responses of rice and wheat exposed to HNT stress across scales, and (ii) understand the physiological and biochemical responses that affect grain yield and quality. To achieve this, we combined a synthesis of current literature on HNT effects on rice and wheat with information from a series of independent experiments we conducted across scales, using a common set of genetic materials to avoid confounding our findings with differences in genetic background. In addition, we explored HNT‐induced alterations in physiological mechanisms including carbon balance, source–sink metabolite changes and reactive oxygen species. Impacts of HNT on grain developmental dynamics focused on grain‐filling duration, post‐flowering senescence, changes in grain starch and protein composition, starch metabolism enzymes and chalk formation in rice grains are summarized. Finally, we highlight the need for high‐throughput field‐based phenotyping facilities for improved assessment of large‐diversity panels and mapping populations to aid breeding for increased resilience to HNT in crops.
Impact of high night temperature on grain yield and quality in field crops, captured across spatial scales, allows the identification of tolerant germplasm, traits and mechanisms from controlled environments that have relevance under field conditions.
Heat stress during flowering has differential impact on male and female reproductive organ viability leading to yield losses in field crops. Unlike flooded rice, dryland cereals such as sorghum, ...pearl millet and wheat have optimised their flower opening during cooler early morning or late evening hours to lower heat stress damage during flowering. Although previous studies have concluded that pollen viability determines seed set under heat stress, recent findings have revealed pearl millet and sorghum pistils to be equally sensitive to heat stress. Integrating flower opening time during cooler hours with increased pollen and pistil viability will overcome heat stress-induced damage during flowering under current and future hotter climatic conditions.
High‐temperature during flowering in rice causes spikelet sterility and is a major threat to rice productivity in tropical and subtropical regions, where hybrid rice development is increasingly ...contributing to sustain food security. However, the sensitivity of hybrids to increasing temperature and physiological responses in terms of dynamic fertilization processes is unknown. To address these questions, several promising hybrids and inbreds were exposed to control temperature and high day‐time temperature (HDT) in Experiment 1, and hybrids having contrasting heat tolerance were selected for Experiment 2 for further physiological investigation under HDT and high‐night‐time‐temperature treatments. The day‐time temperature played a dominant role in determining spikelet fertility compared with the night‐time temperature. HDT significantly induced spikelet sterility in tested hybrids, and hybrids had higher heat susceptibility than the high‐yielding inbred varieties. Poor pollen germination was strongly associated with sterility under high‐temperature. Our novel observations capturing the series of dynamic fertilization processes demonstrated that pollen tubes not reaching the viable embryo sac was the major cause for spikelet sterility under heat exposure. Our findings highlight the urgent need to improve heat tolerance in hybrids and incorporating early‐morning flowering as a promising trait for mitigating HDT stress impact at flowering.
High‐temperature during flowering in rice causes spikelet sterility and is a major threat to rice productivity in tropical and subtropical regions. Our investigations, involving both high day‐time and high night‐time temperatures, revealed that high day‐time temperature played a dominant role in determining spikelet fertility compared with high night‐time temperature. Rice hybrids were more susceptible than the high‐yielding inbred varieties to high day‐time temperature. Our novel observations capturing the dynamic fertilization processes demonstrated that pollen tubes not reaching the viable embryo sac was the major cause for spikelet sterility under heat exposure.
Heat and drought stress are projected to become major challenges to sustain rice (Oryza sativa L.) yields with global climate change. Both stresses lead to yield losses when they coincide with ...flowering. A significant knowledge gap exists in the mechanistic understanding of the responses of rice floral organs that determine reproductive success under stress. Our work connects the metabolomic and transcriptomic changes in anthers, pistils before pollination and pollinated pistils in a heat‐tolerant (N22) and a heat‐sensitive (Moroberekan) cultivar. Systematic analysis of the floral organs revealed contrasts in metabolic profiles across anthers and pistils. Constitutive metabolic markers were identified that can define reproductive success in rice under stress. Six out of nine candidate metabolites identified by intersection analysis of stressed anthers were differentially accumulated in N22 compared with Moroberekan under non‐stress conditions. Sugar metabolism was identified to be the crucial metabolic and transcriptional component that differentiated floral organ tolerance or susceptibility to stress. While susceptible Moroberekan specifically showed high expression of the Carbon Starved Anthers (CSA) gene under combined heat and drought, tolerant N22 responded with high expression of genes encoding a sugar transporter (MST8) and a cell wall invertase (INV4) as markers of high sink strength.
A novel attempt was made to associate temporal and spatial dynamics with the transcriptome and the metabolome of the anther, pistil before pollination and pollinated pistil exposed to heat or combined drought and heat stress, with key physiological processes determining stress induced spikelet sterility. Our work identifies key constitutive metabolite markers specific to reproductive organs that could be extremely valuable particularly with constrains associated with infrastructural challenges for precision stress phenotyping. We demonstrate that the tolerant cultivar N22 having the potential to avoid carbon starvation through e.g. the operation of sugar transporters and a cell wall invertase to reduce the impact of heat or drought stress on anthers, unlike the susceptible cultivar Moroberekan.
Unlike sporadic daytime heat spikes, a consistent increase in night‐time temperatures can potentially derail the genetic gains being achieved. Ten winter wheat genotypes were exposed to six different ...night‐time temperatures (15–27°C) during flowering and grain‐filling stages in controlled environment chambers. We identified the night‐time temperature of 23oC as the critical threshold beyond which a consistent decline in yields and quality was observed. Confocal laser scanning micrographs of central endosperm, bran, and germ tissue displayed differential accumulation of protein, lipid, and starch with increasing night‐time temperatures. KS07077M‐1 recorded a decrease in starch and an increase in protein and lipid in central endosperm with increasing night‐time temperatures, whereas the same was significantly lower in the tolerant SY Monument. Expression analysis of genes encoding 21 enzymes (including isoforms) involved in grain–starch metabolism in developing grains revealed a high night‐time temperature (HNT)‐induced reduction in transcript levels of adenosine diphosphate glucose pyrophosphorylase small subunit involved in starch synthesis and a ≥2‐fold increase in starch degrading enzymes isoamylase III, alpha‐, and beta‐amylase. The identified critical threshold, grain compositional changes, and the key enzymes in grain starch metabolism that lead to poor starch accumulation in grains establish the foundational knowledge for enhancing HNT tolerance in wheat.
High night temperature‐induced reduction in winter wheat grain‐yields and starch accumulation is attributed to decreased transcript levels of AGPase and increased transcript levels of isoamylase III, alpha‐, and beta‐amylases
High night temperatures (HNTs) can reduce significantly the global rice (Oryza sativa) yield and quality. A systematic analysis of HNT response at the physiological and molecular levels was performed ...under field conditions.
Contrasting rice accessions, N22 (highly tolerant) and Gharib (susceptible), were evaluated at 22°C (control) and 28°C (HNT). Nitrogen (N) and nonstructural carbohydrate (NSC) translocation from different plant tissues into grains at key developmental stages, and their contribution to yield, grain-filling dynamics and quality aspects, were evaluated. Proteomic profiling of flag leaf and spikelets at 100% flowering and 12 d after flowering was conducted, and their reprogramming patterns were explored.
Grain yield reduction in susceptible Gharib was traced back to the significant reduction in N and NSC translocation after flowering, resulting in reduced maximum and mean grain-filling rate, grain weight and grain quality. A combined increase in heat shock proteins (HSPs), Ca signaling proteins and efficient protein modification and repair mechanisms (particularly at the early grain-filling stage) enhanced N22 tolerance for HNT.
The increased rate of grain filling and efficient proteomic protection, fueled by better assimilate translocation, overcome HNT tolerance in rice. Temporal and spatial proteome programming alters dynamically between key developmental stages and guides future transgenic and molecular analysis targeted towards crop improvement.
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