Elsevier

Field Crops Research

Volume 200, January 2017, Pages 114-121
Field Crops Research

Review
Field crops and the fear of heat stress—Opportunities, challenges and future directions

https://doi.org/10.1016/j.fcr.2016.09.024Get rights and content

Highlights

  • Physiological responses to heat stress coinciding with flowering in pulses and oilseeds is limited.

  • Categorizing responses into tolerance, escape or avoidance category is essential to enhance resilience to heat stress.

  • Wild accessions – a store house of opportunities for increasing heat stress resilience in cereals.

Abstract

Predicted increase in temperature variability can result in short duration of heat stress episodes coinciding with vulnerable reproductive processes leading to significant reduction in floret-fertility in crops. Recent knowledge on alternations in the pollen and stigmatic morphology, pollen biochemical and lipid composition, variable sensitivity of floral reproductive organs and differential temperature thresholds across crops advances the knowledge on heat stress induced reduction in seed-set and harvest index. Rapid increase in night-time temperature, leading to narrowing diurnal temperature amplitude is a major emerging threat to sustain crop productivity. Interestingly, wild wheat (Aegilops spp.) with higher heat-tolerance and wild rice (Oryza officinalis) escaping damage by completing flowering during early morning hours, are examples of novel opportunities to breed field crops resilient to heat stress. Information on mechanisms leading to heat stress induced sterility is biased towards rice, wheat and sorghum, while the same across other field crops is limited. Hence, increasing research efforts in this direction is critical and timely.

Introduction

Cereals, millets, oil seeds and other field crops respond differently to short and long duration heat stress exposure during different growth and developmental stages but are most vulnerable during the key reproductive stages i.e., gametogenesis and flowering (Hedhly, 2011, Prasad and Djanaguiraman, 2014, Prasad et al., 2015, Shi et al., 2015, Singh et al., 2015). Under field conditions, these key developmental processes extend over a period ranging between 14 and 21 days depending on crop species. Field crops have different optimum and critical temperature thresholds for achieving reproductive success, beyond which a series of morph-physiological processes determining seed-set are affected leading to significant yield losses. The level of damage caused is based on crop sensitivity, and duration and intensity of heat stress exposure. Continuous efforts in quantifying the impact of heat stress during the sensitive reproductive stage in crops, primarily using controlled environment facilities have identified damaging temperatures lying between 30 and 40 °C (Fig. 1). High day-time temperatures coinciding with reproductive stage can cause significant damage to reproductive processes in cereals (30–38 °C), millets (40 °C), oilseeds (35–36 °C) and pulses (32–40 °C) (Fig. 1). Information on the sensitivity at a finer developmental time scale, accounting for a large proportion of the damage during these vulnerable stages will allow developing precise genetic and molecular interventions to minimize negative impacts of heat stress. The male reproductive organ (anther/pollen or male gametophyte development) have been identified to be the major factor determining seed-set under heat stress, wherein loss of pollen viability and reduced pollen germination percentage on the stigmatic surface leading to sterile flowers has been quantified across crops (Djanaguiraman et al., 2014, González-Schain et al., 2015, Li et al., 2015, Polowick and Sawhney, 1988). Pollen tube growth and development within female tissue, following pollination have documented sensitivity to heat stress in wheat (Saini et al., 1983), cotton (Snider et al., 2009, Snider et al., 2011), chickpea (Kumar et al., 2013), rice (Jagadish et al., 2010) and other crops (Kaushal et al., 2016, references within). However, in majority of the self-pollinated crops, there is limited information on heat stress impact on the female reproductive organs (pistil – stigma, style and ovary), which warrants further detailed investigation. In addition, other mechanistic aspects such as variation in the pollen and stigmatic surface morphology, pollen and anther lipid composition, pollen reactive oxygen species (ROS) production damaging their membrane are either not known or less studied in most field crops.

Season-long high-temperature stress decreases biomass production, seed number, individual seed weight and yield of all grain crops, which is reflected in the harvest index (HI = grain yield/total aboveground biomass). Knowledge on temperature thresholds that can differentiate field crops with higher HI will provide additional options for deploying resilient replacement crops in scenarios faced with heat stress challenges. Another component of the climate change phenomena is the rapid increase in night temperature resulting in narrowing diurnal temperature amplitude. Recent studies indicate significant negative impact of high night temperature on yield and grain quality among field crops (Bahuguna et al., 2016, Garcia et al., 2015, Garcia et al., 2016, Lyman et al., 2013, Narayanan et al., 2015, Shi et al., 2013, Sunoj et al., 2016, Welch et al., 2010). Warmer nights negatively affect the balance between photosynthesis and night respiration rates, reducing the overall carbohydrate pool and biomass leading to reduced yield and lower HI (Bahuguna et al., 2016, Garcia et al., 2016, Shi et al., 2013).

Breeding efforts focused on increasing yield have gradually minimized or in some cases outbreed the plasticity for stress response, rendering crop production vulnerable to climatic changes. Different mechanisms have been identified to minimize heat stress damage during flowering in rice, including heat escape (early morning flowering; Ishimaru et al., 2010, Julia and Dingkuhn, 2012, Hirabayashi et al., 2014), heat avoidance through transpiration cooling (Julia and Dingkuhn, 2013) and heat tolerance through resilient reproductive processes (Jagadish et al., 2010). Such systematic quantification of mechanisms or traits in other crops is unclear. Additionally, options to sustain genetic gains and simultaneously increase resilience to heat stress is possible through exploring diversity in wild species for heat tolerance (example – wheat; [Pradhan et al., 2012, Pradhan and Prasad, 2015]). Hence, this focused review highlights the progress achieved in quantifying the degree of sensitivity on a developmental time scale during the reproductive phase, comparative assessment of floral organs vulnerability and varying temperature thresholds inducing changes in harvest index (HI) in different crops important for global food security. Opportunities available through exploring wild species and research direction for crop improvement to sustain global food production under future hotter climates are highlighted and discussed.

Section snippets

Reproductive stage vulnerability on a developmental time scale

On a broader developmental scale, reproductive stages in field crops are known to be more susceptible to heat stress compared to vegetative stages. However, the finer window of sensitivity during reproductive stages particularly flowering is less known across different crops. Among cereals such as wheat and rice, the duration taken by a spike, head or panicle, respectively to complete flowering is about 5–6 days and across different tillers (in rice) may take up to 14 days (Bahuguna et al., 2015

Mechanistic advances in floral organs response to heat stress

In spite of the progress achieved in identifying the narrow time scale of sensitivity in some of the major field crops, the question on the role of male and female reproductive organs and their contribution towards stress induced sterility is not entirely clear. Recent findings indicate male reproductive organ to be highly sensitive while the pollen-pistil interaction leading to fertilization could be hindered due to the damage caused by heat stress on stigma, style or ovary (Fig. 3). Seed-set

Long duration high temperature stress thresholds reducing harvest index in crops

Impact of heat stress over longer duration encompassing vegetative, reproductive and the grain filling phase results in distinct differences in HI. Among different field crops wheat is the most sensitive cereal with its HI beginning to drop immediately after a mean daily temperature of 16 °C while other tropical and subtropical crops do not experience the same phenomena until 26 °C (Fig. 5). Temperature close to 30 °C and beyond leads to complete loss of yield in wheat while other cereals have a 10

Wild species, a wealth of opportunity

Utilizing some of the extremely useful traits/genes from wild accessions into ongoing breeding programs could be challenging, but a systematic strategy can help overcome this bottleneck and benefit from the wealth of diversity housed in wild species and accessions. An excellent example has been the exploration of the time of day of flowering in rice, wherein the early morning flowering trait has been systematically phenotyped and isolated from wild rice Oryza officinalis and incorporated into

Future directions

Evidently a narrow genetic pool is exploited by current heat tolerance breeding programs. Novel donors with higher heat tolerance or escape as illustrated above provides ample evidence for systematic exploration of wild species and accessions. Crop responses to heat stress are generally clubbed under heat tolerance category without having investigated for heat avoidance or escape phenomena, which are equally effective under field conditions. Phenotyping approaches classifying heat stress

Acknowledgements

We thank Kansas Wheat Alliance, Kansas Grain Sorghum Commission, USAID Feed the Future Innovation Labs (Climate Resilient Wheat; and Sustainable Intensification), and Coordinated Agricultural Project Grant no. 2011-68002-30029 (Triticeae – CAP) from the USDA National Institute of Food and Agriculture for supporting research of authors. Contribution no. 16-187-J from Kansas Agricultural Experiment Station.

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