Plant survival and productivity decrease with exposure to less favourable environments. The negative effects of environmental factors such as water-deficit and salinity stress on vegetation are relatively well studied (Farooq, Hussain, Wahid, & Siddique, 2012; Munns et al., 2020; Parihar, Singh, Singh, Singh, & Prasad, 2015), primarily due to the large losses in crop yield and forest biomass caused by these stresses. Although the impact of combined heat and drought on plants has received considerable interest in recent years due to climate change (Bras, Seixas, Carvalhais, & Jagermeyr, 2021; Lamaoui, Jemo, Datla, & Bekkaoui, 2018), there has been less focus on ascertaining the impact of heat stress alone at a range of temporal and spatial scales.

The steady increase in global mean temperatures and (more importantly) variability in extreme temperatures is translating into more frequent and extreme heat stress episodes, which in turn reduce plant productivity. Further, projected increases in both day and night temperatures and the predicted impact of these changes on agricultural and forest productivity (Impa et al., 2021; Teskey et al., 2015) have drawn attention to the need to better address the direct effects of heat on plants. In particular, there has been tremendous interest in understanding the short- and long-term effects of heat at the cellular and whole-plant levels, including work on crops of agricultural importance and species from less managed ecosystems (Figure 1). Hence, we made a concerted effort in this Special Issue to capture recent progress in our ability to quantify the impact of heat stress, and identify new tools and approaches that have been developed and implemented to capture a wide range of responses in plants. This series of reviews and research articles captures our current understanding of plant physiological and molecular responses to heat stress, as well as covering phenotyping methods, genetic diversity and potential routes through which plants can acclimate and adapt to warming climates.

1 SYNTHESIS OF PLANT RESPONSES TO HEAT

With the predicted increase in the frequency and intensity of heat events, bringing together results from different ways of studying heat stress (including heat shock, heat wave and warming experiments) is essential to emphasize the future direction of heat stress research (Jagadish, Way, & Sharkey, 2021). On exposure to heat stress, different parts of a plant can experience different tissue temperatures and can also respond differently. For example, reproductive tissues are often more susceptible to heat compared to vegetative tissue (Jagadish et al., 2021). This presents the need to understand the mechanisms that operate across different cells that make up the specific tissue or an organ, which is made possible by recent advances in single-cell gene regulatory networks (Tripathi & Wilkins, 2021). The authors, in addition to summarizing the technology for use in plant science, elaborate on approaches to help enhance heat stress resilience by using single-cell gene regulatory networks.

To know how plants respond to heat requires knowing how they sense heat. Hayes, Schachtschabel, Mishkind, Munnik, and Arisz (2021) provide an update on the molecular mechanisms that come into play during heating. They describe a variety of responses that plants use to avoid heat damage, to acclimate to the heat and to provide protection against severe heat. Plasma membrane-linked proteins, Ca²⁺ channels, H₂O₂ signals and other molecular mechanisms are brought together to make a comprehensive assessment of heat sensing. In addition, phytochrome B and phototropin and a clock component ELF3 were identified as direct temperature sensors in the model plant Arabidopsis (Hayes et al., 2021). These sensors, and other mechanisms based on lipid signalling pathways, provide a spectrum of heat sensing mechanisms to help plants acclimate or survive heat conditions.

A large genetic diversity exists in crop plants, with different level of sensitivity observed in response to heat stress, but exploiting higher levels of heat tolerance for crop improvement has been a challenge due to limitations related to phenotyping large populations (Impa et al., 2021). Using metabolomics and transcriptomics approaches, Schaarschmidt, Lawas, Kopka, Jagadish, and Zuther (2021) show the relevance of deriving molecular markers to enhance our ability to capture large genetic diversity for heat stress responses. Schaarschmidt et al. (2021) reveal underlying metabolites and transcripts that differentiate heat-tolerant rice and wheat from susceptible genotypes, indicating the possibility of developing molecular markers to complement ongoing efforts to breed crops with increased heat tolerance.

2 THE IMPORTANCE OF INCREASING NIGHT TEMPERATURES

Global mean temperature increase hides interesting patterns in temperature change that can affect plant heat responses, such as the greater increase in night-time warming compared to daytime temperature increases (K. Wang, Li, Wang, & Yang, 2017). Kronenberg et al. (2021) illustrate the importance of understanding how diel variation in temperature affects plant growth, with implications for the way in which we design and interpret our experiments. Based on multiple studies under field-based facilities, Impa et al. (2021) summarize how day and night temperatures have a differential impact on the physiological responses in crops, including rice and wheat. Interestingly, findings from the chamber conditions were shown to be scalable to field-grown wheat, but not necessarily to flooded rice (Impa et al., 2021). The authors hypothesize that findings from controlled environment chambers could be translatable to other field-grown dryland crops, similar to wheat. Importantly, differences in the impact of high night temperatures on respiration and post-flowering carbon balance were linked to changes in yield and grain quality in rice and wheat (Impa et al., 2021; Xu, Misra, Sreenivasulu, & Henry, 2021). Using a MAGICheat population of 432 genotypes, a significant reduction in stem non-structural carbohydrates was associated with yield losses under high night temperature (Xu et al., 2021).

3 CARBON DYNAMICS AS A KEY REGULATOR OF PLANT HEAT STRESS RESPONSES

The dynamics of carbon regulation under warmer conditions are key to ensuring plant productivity. Carbon balance can be viewed as a push-pull dynamic that is driven by mitochondrial respiration and photosynthetic efficiency. Scafaro et al. (2021) synthesize current knowledge on how mitochondrial respiration responds to heat, including changes to respiratory metabolism under moderate heat and the inactivation of respiratory enzymes under excessive temperatures. This push-pull mechanism is further examined by Coast et al. (2021), who evaluated the acclimation of both photosynthesis and respiration to higher growth temperatures in wheat and found temperature-dependent shifts in source-sink dynamics. Continuing the theme of carbon balance, Ferguson, Tidy, Murchie, and Wilson (2021) highlight the need to sustain carbon supply to ensure the viability of reproductive organs for maintaining productivity under heat stress. Focusing on source-sink dynamics, they emphasize the relevance of non-foliar photosynthesis to supply carbon for highly energy intensive reproductive processes (Ferguson et al., 2021). Plant responses under heat are also strongly influenced by relative humidity, which can either enhance (dry air) or lower (moist air) evaporative demand, thus leading to the differential impact of heat stress on plants exposed to similar temperatures (Sadok, Lopez, & Smith, 2021). By examining stomatal-, cuticular- and water viscosity-based mechanisms, Sadok et al. (2021) highlight the need to consider trade-offs between temperature and evaporative demand while developing new crop varieties for future hotter and drier climates.

The ability to maintain photosynthesis is critical for supplying carbohydrates to fuel metabolism and reproduction during heat stress, and this Special Issue compiles a suite of research papers investigating the response of CO₂ assimilation under warmer conditions. Osei-Bonsu, McClain, Walker, Sharkey, and Kramer (2021) highlight the importance of photorespiration and alternative electron sinks in preventing photodamage to Photosystem II (PSII) in high temperature and high light conditions. Indeed, the heat tolerance of PSII is often considered a limiting factor in the ability to maintain photosynthesis under high temperatures, an idea that is explored by Perez, Socha, Tserej, and Feeley (2021) and Slot et al. (2021). Perez et al. (2021) found that high heat tolerance of PSII was associated with species that were thermal generalists, thus providing a proxy for evaluating the thermal niche of plants, while Slot, Cala, et al. (2021) showed that PSII heat tolerance varies in a predictable way with site temperature and elevation. The ability to acclimate CO₂ uptake rates to higher temperatures is often related to shifts in the thermal sensitivity and capacity of photosynthetic processes, and can occur quite quickly (Slot, Rifai, & Winter, 2021).

One mechanism for creating more heat tolerant photosynthesis is via increasing the expression of the carboxylating enzyme Rubisco and its chaperone protein Rubisco activase, which was shown to stimulate CO₂ uptake rates and plant biomass in rice under high temperatures (Qu et al., 2021). Another important mechanism for increasing the tolerance of plants to heat stress is heat priming, whereby the plant is exposed to a high, but non-damaging temperature before a later heat stress is imposed (Jagadish et al., 2021). This heat priming can reduce the negative effects of heat stress on photosynthesis by stimulating stomatal conductance and the production of volatile and non-volatile antioxidant compounds (Liu et al., 2021).

A full understanding of high temperature effects will require knowledge of how these will interact with other factors. For example, Y. Li, Hou, and Tao (2021) report that production practices such as tillage influence morphological responses during warmer seasons by negatively impacting photosynthetic parameters. L. Li et al. (2021) found some influence of drought on high temperature responses and also compensation between above ground and below ground biomass on the ability of the ecosystem under study to act as a CO₂ sink, based on a four-year field experiment. In addition to abiotic stress and agronomic interactions, warming scenarios, due to changes in temperature can alter the plant pest and disease incidence and spread (Velásquez, Castroverde, & He, 2018). Gupta et al. (2021) have unravelled underlying mechanisms involving salicylic acid and ethylene, leading to root zone warming-induced immune responses against phytopathogens in tomato.

4 HEAT STRESS EFFECTS ON NON-VASCULAR PLANTS

Understanding heat stress effects on non-vascular plants can provide basic information on the universality of tolerance and resilience mechanisms among land plants. This is also crucial because warming is greatest in high northern latitudes where mosses (especially sphagnum) often dominate the landscape. The tundra is a major CO₂ sink and so the rapidly increasing temperature, and how this will affect the mosses that dominate the tundra, is an important area of study. Recently, heat stress-induced reactive oxygen species signalling was shown to propagate through tissues such as mesophyll cells, and not only through vascular bundles in plants (Zandalinas & Mittler, 2021). This discovery provides support to the perception of heat stress stimuli and similar systemic plant responses including acquired acclimation between vascular and non-vascular plants. As plants moved onto land they were subjected to greater heat stress and temperature variability. Guihur, Fauvet, Finka, Quadroni, and Goloubinoff (2021) found that a number of heat-related mechanisms, such as acquired thermotolerance and accumulation of heat shock proteins are present in the moss Physcomitrium patens. Even the liverwort Marchantia polymorpha has a significant number of genes recognized as related to heat tolerance in angiosperms (Marchetti et al., 2021).

5 NEGATIVE IMPACTS OF HEAT EXPOSURE ON PLANT REPRODUCTION AND FRUIT DEVELOPMENT

Successful reproduction and seed-set depend on pollen-pistil interactions and the respective viability of pollen and pistil after exposure to heat stress. Both the male reproductive organ (anther/pollen) and female reproductive organ (pistil) are sensitive to heat exposure (Masoomi-Aladizgeh et al., 2021; Y. Wang, Impa, Sunkar, & Jagadish, 2021). Heat stress imposed during the pollen tetrad and binucleate stages resulted in profound damage to pollen despite elevated levels of sugars, thereby suggesting mechanisms beyond carbohydrate supply as the reason for pollen sterility (Masoomi-Aladizgeh et al., 2021). Further, heat stress during pollen tube growth in Arabidopsis revealed significant down-regulation of membrane transporters (Poidevin, Forment, Unal, & Ferrando, 2021). In addition to membrane transporters, the presence of ribosomes on non-coding RNAs is a novel regulatory aspect of plant fertilization, which indicates the role of alternative players in pollen development and tube growth, apart from sugars (Masoomi-Aladizgeh et al., 2021; Poidevin et al., 2021).

Although sugar supply was not the central mechanism leading to pollen sterility in cotton (Masoomi-Aladizgeh et al., 2021), other plants such as beans (Phaseolus vulgaris, Santiago et al., 2021) and other species (Ferguson et al., 2021) rely on sugar supply and availability to retain pollen viability. The manner in which changes in the anther oxidative pentose phosphate pathway play a role in anther sugar accumulation and support H₂O₂ scavenging machinery is another dimension to the pollen viability narrative under heat stress (Santiago et al., 2021). These studies indicate that the level to which crops depend on sugars to retain pollen viability could vary and that a general conclusion regarding this mechanism of pollen quality cannot be drawn. To complement the progress achieved in ensuring pollen viability under heat stress, it is equally essential to ensure a viable pistil by reducing the negative impact of heat during pistil development, pollen-pistil interactions (pollen germination and pollen tube growth) and fertilization and early embryogenesis (Y. Wang et al., 2021), for sustaining crops yields under a future hotter climate.

Temperature is also a strong regulator of seed and fruit development. Seed development temperature can alter the balance between abscisic acid and gibberellic acid, thus affecting dormancy induction and maintenance in seeds, as shown by Tuan, Nguyen, Jordan, and Ayele (2021). As well, Almeida, Perez-Fons, and Fraser (2021) looked at the cellular metabolism of tomato fruits under heat stress. Their results on nutritional attributes (including carotenogenesis, sucrose and triacylglycerols accumulation and lipid re-modelling) provide new insights into mechanisms to help develop tomato fruits that are better adapted to heat stress (Almeida et al., 2021).

6 FUTURE OUTLOOK

New tools and advances in the methodology developed for imposing and capturing heat stress responses on single plants need to be made applicable to populations, to benefit crop improvement programs. The majority of heat stress or heat wave responses have been captured under controlled environment conditions or to some extent under field-based facilities, but we are yet to find means for feasibly testing and validating a large proportion of information across heat-prone environments. Sensor-based technology, apart from thermal imaging needs to be explored to capture responses such as night respiration or changes in source-sink sugar partitioning to be able to rapidly advance our ability to develop heat stress resilient plants. In addition to currently popular DNA-based molecular markers, developing targeted heat stress responsive metabolite or protein chips can help in capturing additional genetic diversity that is currently locked up in gene banks. Progress achieved with the molecular responses have largely been restricted to the improvement of crop species, and findings ways to extend these to other plants including forest species that constitute the natural ecosystem will help in protecting global biodiversity under a future hotter climate. Taken together, it is evident that global warming affects plants negatively, including crops (Ferguson et al., 2021) and forests (Tiwari et al., 2020).

CONFLICT OF INTEREST

Authors declare no conflict of interest.