Heat stress in crop plants: its nature,impacts and integrated breeding strategies to improve heat tolerance

Increasing severity of high temperature worldwide presents an alarming threat to the humankind. As evident by massive yield losses in various food crops, the escalating adverse impacts of heat stress (HS) are putting the global food as well as nutritional security at great risk. Intrinsically, plants respond to high temperature stress by triggering a cascade of events and adapt by switching on numerous stress‐responsive genes. However, the complex and poorly understood mechanism of heat tolerance (HT), limited access to the precise phenotyping techniques, and above all, the substantial G × E effects offer major bottlenecks to the progress of breeding for improving HT. Therefore, focus should be given to assess the crop diversity, and targeting the adaptive/morpho‐physiological traits while making selections. Equally important is the rapid and precise introgression of the HT‐related gene(s)/QTLs to the heat‐susceptible cultivars to recover the genotypes with enhanced HT. Therefore, the progressive tailoring of the heat‐tolerant genotypes demands a rational integration of molecular breeding, functional genomics and transgenic technologies reinforced with the next‐generation phenomics facilities.     

Functional mechanisms of drought tolerance in maize through phenotyping and genotyping under well watered and water stressed conditions

Developing tolerant genotypes is crucial for stabilizing maize productivity under drought stress conditions as it is one of the most important abiotic stresses affecting crop yields. Twenty seven genotypes of maize (Zea mays L.) were evaluated for drought tolerance for three seasons under well watered and water stressed conditions to identify interactions amongst various tolerance traits and grain yield as well as their association with SSR markers. The study revealed considerable genetic diversity and significant variations for genotypes, environment and genotype × environment interactions for all the traits. The ranking of genotypes based on drought susceptibility index for morpho-physiological traits was similar to that based on grain yield and principal component analysis. Analysis of trait – trait and trait – yield associations indicated significant positive correlations amongst the water relations traits of relative water content (RWC), leaf water potential and osmotic potential as well as of RWC with grain yield under water stressed condition. Molecular analysis using 40 SSRs revealed 32 as polymorphic and 62 unique alleles were detected across 27 genotypes. Cluster analysis resulted in categorization of the genotypes into five distinct groups which was similar to that using principal component analysis. Based on overall performance across seasons tolerant and susceptible genotypes were identified for eventual utilization in breeding programs as well as for QTL identification. The marker-trait association analysis revealed significant associations between few SSR markers with water relations as well as yield contributing traits under water stressed conditions. These associations highlight the importance of functional mechanisms of intrinsic tolerance and cumulative traits for drought tolerance in maize.     

Genotypic variability among cotton cultivars for heat and drought tolerance using reproductive and physiological traits

Development of rapid and inexpensive screening tools for heat and drought stress tolerance is needed and will be helpful in cotton breeding programs and selecting cultivars for a niche environment. In this study, several pollen-based traits at optimum and high temperatures and physiological parameters measured during the boll-filling period were used to evaluate variability among the cultivars for heat and drought stresses. Principal component analysis and drought stress response index methods were used to categorize cotton cultivars into three heat and drought tolerant clusters. Based on the combined analysis, PX532211WRF has been identified as heat- and drought-tolerant, and would be expected to perform better under both heat- and drought-stressed environments. A poor correlation between reproductive and physiological indices indicates that screening breeders have to use different traits to screen cultivars for reproductive and vegetative tolerance. Identified traits could serve as valuable screening tools in cotton breeding programs aimed at developing genotypes to a changing climate. Moreover, cultivar-dependent relative scores will aid in the identification of cultivars best suited to niche environments to alleviate the influences of abiotic stresses at both vegetative and reproductive stages.     

Genotypic differences in utilization of assimilate sources during maturation of wheat under chronic heat and heat shock stresses

Heat stress from chronic, prolonged exposure up to 32 ^°C or heat shock from brief exposure to 33 ^°C and above alters the source of assimilates for grain growth of wheat (Triticum asetivum L.). Our objectives were to identify genotypes that resist chronic heat stress and heat shock and to determine the relative contributions of photosynthesis and stem reserves to grain filling under both conditions. Twenty-eight genotypes were grown in controlled enviroments at 20/15 and 30/25 ^°C day/night in light and darkness during maturation in the first experiment, and six genotypes were grown in light at the same temperatures and at 40/35 ^°C followed by 20/15 or 30/25 ^°C in the second experimnet. Heat susceptibility indices (HSI) were calculated from grain yields of the genotypes in both experiments. The ratio of chlorophyll variable fluorescence to maximum fluorescence (Fv/Fm), a measure of the stability of photosynthesis, and carbohydrate reserves in the stems were measured in the second experiment. Photosynthesis provided 63 and 65% of assimilates in the grain at 20/15 and 30/25 ^°C, respectively, but both stable photosynthesis in some genotypes and high content of reserves in other genotypes were associated with low susceptibility to stress. The Fv/Fm ratio was decreased by heat shock and returned to normal values intolerant genotypes when the treatment was followed by 20/15 ^°C but not 30/25 ^°C. Grain yield was highly correlated among 20/15, 30/25, and 40/35 ^°C followed by 20/15 ^°C treatments, suggesting that similar plant traits were involved. We conclude that assimilates from either stable photosynthesis or high reserve levels provided for high grain yields during heat stress. Combining the two traits could improve heat tolerance of wheat but might not be feasible if other traits are impeded. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genotype selection for physiological responses of drought tolerance using molecular markers in polycross hybrids of orchardgrass

The present study aimed to assess the effect of contrasting levels of molecular and phenotypic diversity among polycross parents of orchardgrass on the performance of synthetic progeny with respect to physiological responses and drought tolerance. Four polycross groups each composed of six parental plants were evaluated under normal irrigation and drought stress conditions. A number of 923 inter simple sequence repeats and sequence related amplified polymorphism markers and several phenotypic traits were used to select contrasting levels of diversity (high and low) in parental genotypes. Highly significant correlation was observed between molecular distance and progeny performances at both normal irrigation and drought stress conditions. High molecular diversity among polycross parents led to a significant yield advantage of first generation progeny with averages of 34.40% for normal irrigation and 48.10% for drought stress conditions. Also crosses between genetically distant parents produced progeny with considerable drought tolerance and yield stability. Positive associations between phenotypic distance of parents and progeny performance were found for most physiological traits at both moisture regimes but phenotypic distances had weak association with forage yield, stress tolerance index and yield stability of progeny. Significant associations between drought tolerance index and some physiological traits confirmed the importance of these traits in conferring drought tolerance of orchardgrass. Our results underscore the effectiveness of marker‐assisted polycross breeding to improve drought tolerance and yield stability through physiological traits in orchardgrass.     

Hydrogen peroxide reduces heat‐induced yield losses in cotton (Gossypium hirsutum L.) by protecting cellular membrane damage

We investigated the effect of various growth substances such as hydrogen peroxide, salicylic acid (SA), moringa leaf‐extract (MLE) and ascorbic acid (ASA) on leaf physiology and seed cotton yield (SCY) of heat‐stressed cotton. Cotton plants were exposed to elevated temperatures at three reproductive stages, either by staggering planting time in the field or by increasing growth cabinet temperatures (38/24°C and 45/30°C) in glasshouse. Elevated temperature at any reproductive phase significantly damaged cellular membrane and reduced SCY. Plants exposed to 38/24°C and 45/30°C in glasshouse produced 63% and 22% lower SCY, respectively, compared with plants under optimal temperature ((32/20°C). In response to high temperature, cotton plants up‐regulated activities of anti‐oxidative enzymes e.g. peroxidase and ascorbic acid. However, this defensive system could not protect cellular membrane of stressed plants from extreme temperature (38 and 45°C). In contrast, growth substances such as H2O2, ASA and MLE significantly increased anti‐oxidative enzymes activity to an extent, which reduced heat‐induced damage to cellular membrane. No significant effect of any regulator was observed on SCY under optimum temperatures; although H2O2, MLE and ASA significantly increased SCY of heat‐stressed cotton. Hydrogen peroxide increased SCY of April and May thermal regimes crops by 16% (averaged across both sowing dates) under field, while it caused 14% and 20% increase in SCY of plants exposed to sub (38/24°C) and supra optimal (45/30°C) thermal regimes under glasshouse. We concluded that growth regulators, specifically, H2O2 can protect cotton crops from heat‐induced cellular membrane damage by up‐regulating antioxidant defense system.     

Effect of high temperature on pollen morphology,plant growth and seed yield in quinoa (Chenopodium quinoa Willd.)

Quinoa (Chenopodium quinoa Willd.) has gained considerable attention worldwide during the past decade due to its nutritional and health benefits. However, its susceptibility to high temperatures has been reported as a serious obstacle to its global production. The objective of this study was to evaluate quinoa growth and pollen morphology in response to high temperatures. Pollen morphology and viability, plant growth and seed set, and several physiological parameters were measured at anthesis in two genotypes of quinoa subjected to day/night temperatures of 22/16°C as a control treatment and 40/24°C as the heat stress treatment. Our results showed that heat stress reduced the pollen viability between 30% and 70%. Although no visible morphological differences were observed on the surface of the pollen between the heat‐stressed and non‐heat‐stressed treatments, the pollen wall (intine and extine) thickness increased due to heat stress. High temperature did not affect seed yield, seed size and leaf greenness. On the other hand, high temperature improved the rate of photosynthesis. We found that quinoa has a high plasticity in response to high temperature, though pollen viability and pollen wall structure were affected by high temperatures in anthesis stage. This study is also the first report of quinoa pollen being trinucleate.     

Early‐stage screening for heat tolerance in cotton

The study aimed to identify early‐stage traits of cotton for heat tolerance using multitrait approach reflecting field yield performance. Seedling growth and physiological response of 16 cultivars to high temperature were investigated at three different developmental stages and four heat stress conditions in a climate chamber. Some traits such as hypocotyl dry weight, leaf pigment contents and cellular respiration were significantly correlated with previously known yield of ten cultivars grown in the hot field conditions. Sixteen cotton cultivars were classified for their heat tolerance by principle component analysis (PCA) using yield‐correlated physiological traits. As a result, we showed that heat tolerance classification of cultivars based on PCA significantly coincided with the yield results of cultivars grown in hot field. As a conclusion, yield‐correlated physiological traits determined in the study may facilitate selection of heat‐tolerant cotton genotypes at early stage. In addition, yield‐correlated early‐stage traits can be used in phenotyping for QTL and association mapping studies to develop selection markers for heat tolerance.     

Application of Stress Indices for Heat Tolerance Screening of Common Bean

Common bean is adapted to relatively cool climatic conditions and temperatures of >30 °C during the day or >20 °C at night result in yield reduction. The long‐term goal of breeding for heat tolerance is the development of germplasm with improved field level tolerance under variable temperature conditions. Using previously developed stress indices, this study presents results from high temperature screening of 14 genotypes in both the greenhouse and field in Puerto Rico. A total of three sets of paired trials were conducted in the field and in the greenhouse under high temperature (stress) and lower temperature (low‐stress) conditions. The geometric mean (GM), stress tolerance index (STI) and stress susceptibility index (SSI) were used to evaluate the genotypic performance under stress and low‐stress conditions. The results indicate that it was possible to identify superior genotypes for heat tolerance based on their stress indices. In this evaluation of heat tolerance indices, STI and GM, although correlated, were found to be effective stress indices for the selection of genotypes with good yield potential under stress and low‐stress conditions.     

Rapid induction of small heat shock proteins improves physiological adaptation to high temperature stress in peanut

With the changing climatic scenario and increasing global mean temperature, heat stress became a major limiting factor for today's agriculture. To identify the underlying mechanism associated with heat tolerance in peanut, two experiments (field and growth chamber) were conducted with four genotypes (ICGS 44, GG 7, AK 159 and DRG 1) having differential high temperature stress sensitivity. Field grown plants under three different temperature (D₁, D₂ and D₃) regimes simulated three temperature treatment effects with a variability of 3–4/4–5°C in mean day/night temperature, respectively. In growth chamber, imposition of heat shock (10°C above ambient inside growth chamber) revealed not only rapid induction (within 0.5 hr) of HSPs, especially small HSPs (HSP 17, HSP 40) in tolerant genotypes, but also its sustenance for longer duration (2 hr), which might help them to have better physiological adaptation strategies under high temperature stress. This was evident from significant advancement in phenophases observed with increase in temperature by 15–18 days at physiological maturity, while pollen viability and membrane stability reduced below 50% and 41%, respectively in DRG 1 with increase in mean day/night temperature. Maintenance of higher photosynthesis and transpiration rate and stomatal conductance helped the tolerant genotype ICGS 44 to keep relatively cooler canopy and higher photosynthates, ensuring better physiological condition in this genotype under heat stress. Significant increase (~2.5‐fold) in inositol and hexoses (glucose and fructose) content and reduction (>50%) in sucrose content in leaf tissues indicated degradation of storage carbohydrates for improved osmotic adjustment especially in tolerant genotypes under elevated temperature.     

Determination of Moisture Deficit and Heat Stress Tolerance in Corn Using Physiological Measurements and a Low‐Cost Microcontroller‐Based Monitoring System

In the southern United States, corn production encounters moisture deficit coupled with high‐temperature stress, particularly during the reproductive stage of the plant. In evaluating plants for environmental stress tolerance, it is important to monitor changes in their physical environment under natural conditions, especially when there are multiple stress factors, and integrate this information with their physiological responses. A low‐cost microcontroller‐based monitoring system was developed to automate measurement of canopy, soil and air temperatures, and soil moisture status in field plots. The purpose of this study was to examine how this system, in combination with physiological measurements, could assist in detecting differences among corn genotypes in response to moisture deficit and heat stress. Three commercial hybrids and two inbred germplasm lines were grown in the field under irrigated and non‐irrigated conditions. Leaf water potential, photosynthetic pigments, cell membrane thermostability (CMT) and maximum quantum efficiency of photosystem II (Fv/Fm) were determined on these genotypes under field and greenhouse conditions. Variations observed in air and soil temperatures, and soil moisture in plots of the individual corn genotypes helped explain their differences in canopy temperature (CT), and these variations were reflected in the physiological responses. One of the commercial hybrids, having the lowest CT and the highest CMT, was the most tolerant among the genotypes under moisture deficit and heat stress conditions. These results demonstrated that the low‐cost microcontroller‐based monitoring system, in combination with physiological measurements, was effective in evaluating corn genotypes for drought and heat stress tolerance.     

Traits in Spring Wheat Cultivars Associated with Yield Loss Caused by a Heat Stress Episode after Anthesis

Heat stress resulting from climate change and more frequent weather extremes is expected to negatively affect wheat yield. We evaluated the response of different spring wheat cultivars to a post‐anthesis high temperature episode and studied the relationship between different traits associated with heat tolerance. Fifteen spring wheat (Triticum aestivum L.) cultivars were grown in pots under semifield conditions, and heat stress (35/26 °C) and control treatments (20/12 °C) were applied in growth chambers for 5 days starting 14 days after flowering. The heat stress treatment reduced final yield in all cultivars. Significant variation was observed among cultivars in the reduction in average grain weight and grain dry matter yield under heat stress (up to 36 % and 45 %, respectively). The duration of the grain‐filling period was reduced by 3–12 days by the heat treatment. The reduction in the grain‐filling period was negatively correlated with grain nitrogen yield (r = ?0.60). A positive correlation (r = 0.73) was found between the treatment effect on green leaf area (GLA) and the reduction in yield resulting from heat stress. The amount of stem water‐soluble carbohydrates (WSC) was not related to treatment effects on grain yield or grain weight. However, the treatment effect on stem WSC remobilization was negatively correlated with reduction in grain‐filling duration due to heat stress (r = ?0.74) and positively with treatment effect on grain N yield (r = 0.52). The results suggest that the effect of the heat treatment on GLA was the trait most associated with yield reduction in all cultivars. These findings suggest the importance of ‘stay green’‐associated traits in plant breeding as well as the need for better modelling of GLA in crop models, especially with respect to brief heat episodes during grain filling. There is in particular a need to model how heat and other stresses, including interacting effects of heat and drought, affect duration of GLA after flowering and how this affects source–sink relations during grain filling.     

Ovule dichotomy per locule of the trilocular pistil in cassava,Manihot esculenta: a useful abnormality for increased seed production?

Histologically, the cassava pistil is trilocular with a single ovule in each locule producing a maximum of three seeds in nature. Heat stress (35°/45°C, night/day temperatures), as a physical treatment was attempted to induce useful reproductive and vegetative traits in 10 F₁ hybrids derived from ‘OMR 36‐41’and ‘OMR 36‐42’crosses, and two Asian cassava cultivars,‘Rayong 60’and ‘Rayong 1′, under greenhouse and field conditions. Cytoembryological examination of the repro‐ ductive organs revealed morpho‐structural features of normal pistil in all clones except ‘Rayong 1’which exhibited reproductive variations under greenhouse culture. Genetically, an important variation was ovule dichotomy per locule of the trilocular pistil so that each pistil contained six instead of the usual three ovules and lacked any outer integument. These ovules possessed functional embryo sacs with varying nuclear number. A pair of the dichotomous ovules possessed two embryo sacs of apparent different megaspore mother cells. Vegetatively, F₁ hybrids were dwarf (0.50m) in their phenotype and flowered 1 month earlier than the 1.5‐2.0m tall cultivars under greenhouse conditions.     

A strategy of ideotype development for heat-tolerant wheat

Heat stress significantly limits yield in many wheat-growing areas globally including north-western NSW. While various traits linked to high-temperature tolerance have been identified, the combination of traits that optimize the heat tolerance of wheat has not been established in most environments. A total of 554 genotypes were evaluated in the field at different times of sowing in north-western NSW for three consecutive years to develop a heat-tolerant wheat ideotype for this environment. The later sown experiments were exposed to higher temperatures at the critical reproductive and grain-filling stages of development. The impact of high temperature was greatest at anthesis, and eventual grain yield was reduced by between 4% and 7% with every 1°C rise in average maximum temperature above the optimum of 25°C. High temperature reduced yield, plant height, grain weight and days to anthesis and maturity, and increased the percentage of screenings and grain protein content. Genotypes that produced higher yield under heat stress had shorter days to flowering and maturity, higher NDVI during grain filling, greater chlorophyll content at the milk stage of grain fill, taller plants, greater grain weight and number, and lower screenings compared with the benchmark cultivar Suntop. The genotype closest to the predicted heat-tolerant wheat ideotype identified from trait ranges had 79.6% similarity.     

Mapping of Quantitative Trait Loci Associated with Reproductive‐Stage Salt Tolerance in Rice

Salinity tolerance in rice varies with the state of growth, with the seedling and reproductive stages being the most sensitive. However, association between tolerances at the two stages is poor, suggesting that they are regulated by different processes and genes. Tolerance at the reproductive stage is the most crucial as it determines grain yield. An F₂ mapping population was developed from two rice genotypes contrasting in tolerance: Cheriviruppu and Pusa Basmati 1 (PB1). Cheriviruppu is highly tolerant at the reproductive stage, while PB1 is highly sensitive at both seedling and reproductive stages. One hundred and thirty‐one microsatellite markers polymorphic between the parents were used to construct a linkage map of 1458.5 cM (Kosambi), with a mean intermarker distance of 11.1 cM. Sixteen QTLs with LOD values ranging from 3.2 to 22.3 were identified on chromosomes 1, 7, 8 and 10, explaining 4–47 % of the phenotypic variation. The maximum number of QTL clusters for different component traits was colocalized on the long arm of chromosome 1 and chromosome 7. We identified several significant epistatic interactions, including three inter‐QTL interactions, using MapManager. The results suggest that pollen fertility, Na⁺ concentration and Na/K ratio in the flag leaf are the most important mechanisms controlling salt tolerance at the reproductive stage in rice. The study reports the construction of a genetic map for reproductive‐stage salt tolerance in rice and demonstrates its utility for molecular mapping of QTLs controlling salinity tolerance‐related traits, which will be useful in marker‐assisted selection in the future.     

Mapping the QTLs underlying drought stress at developmental stage of sorghum (Sorghum bicolor (L.) Moench) by association analysis

This study was conducted to identify quantitative trait loci (QTLs) for drought tolerance in sorghum (Sorghum bicolor (L.) Moench) by association mapping using a simple sequence repeat (SSR)-marker-based diversity research set. Genotypic data for 98 SSR marker loci on ten chromosomes were used for the association analysis. The experiment was conducted under control (well-watered) and drought stress conditions, and the phenotypic values of 23 morphological traits were recorded. Drought tolerance was assessed by using a leaf drying score as a parameter of the tolerance/susceptibility: scores were assigned on a scale from 1 (most tolerant) to 9 (most susceptible). Under the control conditions, 17 QTLs associated with 12 traits were identified on chromosomes 1, 2, 4, 8, 9, and 10, with ?Log₁₀ (P) ranging from 2.5 to 7.6 and explaining 9.5–57.5 % of the total phenotypic variance for the traits. Under the drought stress conditions, nine QTLs associated with 8 traits were identified on chromosomes 1, 2, 3, and 10 that explained 9–61.2 % of the total phenotypic variance for the traits, with ?Log₁₀ (P) ranging from 2.5 to 3.5. QTLs for some traits were detected only under the drought stress condition, suggesting that these traits are important in drought tolerance. These QTLs could be used to further dissect the genetic and physiological basis of drought tolerance in sorghum.     

QTL mapping for six ear leaf architecture traits under water‐stressed and well‐watered conditions in maize (Zea mays L.)

Morphological traits for ear leaf are determinant traits influencing plant architecture and drought tolerance in maize. However, the genetic controls of ear leaf architecture traits remain poorly understood under drought stress. Here, we identified 100 quantitative trait loci (QTLs) for leaf angle, leaf orientation value, leaf length, leaf width, leaf size and leaf shape value of ear leaf across four populations under drought‐stressed and unstressed conditions, which explained 0.71%–20.62% of phenotypic variation in single watering condition. Forty‐five of the 100 QTLs were identified under water‐stressed conditions, and 29 stable QTLs (sQTLs) were identified under water‐stressed conditions, which could be useful for the genetic improvement of maize drought tolerance via QTL pyramiding. We further integrated 27 independent QTL studies in a meta‐analysis to identify 21 meta‐QTLs (mQTLs). Then, 24 candidate genes controlling leaf architecture traits coincided with 20 corresponding mQTLs. Thus, new/valuable information on quantitative traits has shed some light on the molecular mechanisms responsible for leaf architecture traits affected by watering conditions. Furthermore, alleles for leaf architecture traits provide useful targets for marker‐assisted selection to generate high‐yielding maize varieties.     

Productivity,persistence and traits related to drought tolerance in smooth bromegrass

This study was conducted to evaluate drought tolerance and persistence in a germplasm of smooth bromegrass and association of forage productivity with different traits. Thirty‐six genotypes of smooth bromegrass were clonally propagated and evaluated under two soil moisture environments for three years (2013–2015). High genotypic variation was observed among genotypes for all the measured traits. Drought stress decreased mean values for traits related to productivity. Also, the long‐term stress for three years reduced the persistence of plants. Results indicated that indirect selection based on components of forage yield, which had high heritability and high correlation with yield, would be more effective to improve drought tolerance in this germplasm. The results of principal component analysis showed that there was a negative relationship between phenological traits with the persistence‐related traits and yield production. This suggests that selection for earliness may indirectly promote persistent genotypes. The results showed that some Hungarian genotypes are valuable gene sources for persistence. The most persistent genotypes from both groups (Iranian and foreign) were identified using the biplot method. These genotypes may be useful for the development of populations for future studies.