Introduction

Plants, being immobile in nature, must respond to environmental perturbations, including heat stress (HS) (Zhu 2016). Plants have evolved coordinated genetic, molecular, biochemical, and physiological mechanisms to survive and adapt under abiotic stress (Mittler 2006; Wahid et al. 2007; Zhu 2016; Wani et al. 2018; Zaid et al. 2020). Given the rising global temperatures, tropical and semi-arid regions are facing frequent episodes of extreme temperatures, which are challenging crop yields (Lobell et al. 2011; Knox et al. 2012). High-temperature stress is becoming a serious problem for sustaining global crop production (Bita and Gerats 2013; Jha et al. 2014; Sadiq et al. 2020), affecting the entire plant life cycle, including physiological, biochemical, and metabolic processes (Bita and Gerats 2013; Hasanuzzaman et al. 2013; Sharma et al. 2019; Sadiq et al. 2020). Crop plants are most sensitive to HS during the reproductive stage, causing significant yield losses (Wheeler et al. 2000; Luo 2011; Gourdji et al. 2013; Deryng et al. 2014).

The effect of HS on various crops has been assessed using various simulation and prediction models (Swaminathan and Kesavan 2012; Tesfaye et al. 2016). Increasing HS associated with global climate change is predicted to reduce rainfed maize yields by 3.3–6.4% by 2030 and 5.2–12.2% by 2050 (Tesfaye et al. 2016, see Table 1). A 1 °C increase beyond normal air temperature is predicted to significantly reduce yields in two-thirds of African maize-growing regions (Lobell et al. 2011). Similarly, in South-East Asia, a 1 °C increase beyond normal air temperature reduced rice yields by 4–14% (Lobell et al. 2008). A 0.5 °C increase beyond normal winter temperatures will likely reduce rainfed wheat yields by 0.45 t ha–1 in India and 4–7% yield in China (Easterling et al. 2007). A 1 °C increase during summer is predicted to reduce soybean yields by up to 16% in Wisconsin in the United States of America (USA) (Kucharik and Serbin 2008). Table 1 shows further examples of crop yield losses due to HS.

Table 1 Crop yield losses under increasing heat stress
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Several strategies, including crop breeding, physiological and agronomic management, and genomics and transgenics approaches, have been suggested to ensure sustainable crop production under increasing HS events (Wahid et al. 2007; Bita and Gerats 2013; Jha et al. 2014). Phytohormones, including auxin/indole acetic acid (IAA), gibberellic acid (GA), abscisic acid (ABA), cytokinins (CTKs), ethylene (ET), salicylic acid (SA), brassinosteroids (BRs), strigolactone (SL), and jasmonic acid (JA) are important molecular players for regulating plant growth in response to various abiotic stress stimuli, including HS (Wani et al. 2016; Verma et al. 2016; Ahmad et al. 2019; Sharma et al. 2019). The above phytohormones significantly participate in various physiological and cellular processes, and molecular mechanisms involved in HS tolerance (Wani et al. 2016; Sharma et al. 2019). Upon perception of HS stimuli, plants release various phytohormones that contribute to plant development and physiological processes, including root development, stomatal movement, pollen development, photosynthesis, osmolyte accumulation, and curtailing reactive oxygen species (ROS) accumulation, thus helping plants to adapt under HS (Sakata et al. 2010; Franklin et al. 2011; Li et al. 2014; Thussagunpanit et al. 2015a; Wu et al. 2016, 2017; Jegadeesan et al. 2018; Rezaul et al. 2019; Raza et al. 2020).

Thus, manipulating endogenous phytohormones or applying exogenous phytohormones could be promising approaches for plant adaptation and recovery from HS to minimize yield losses. The role of various phytohormones in regulating heat tolerance is summarized in Fig. 1. Here, we discuss the implications of various phytohormones and the plausible mechanistic roles in mediating HS tolerance in various plant species.

Fig. 1
figure 1

Role of phytohormones contributing to heat stress adaptations in plants. Phytohormones contribute to plant survival under heat stress by protecting photosynthesis apparatus (Ivanov et al. 1992; Sharma et al. 2019), rescuing pollen fertility (Firon et al. 2012; Zhang et al. 2018), improving grain filling (Yang et al. 2016), accumulating osmolytes (Robertson et al. 1994), activating antioxidant activity and reducing reactive oxygen species activity (Dat et al.1998a), and activating the transcription of various heat shock protein genes (Dhaubhadel et al. 1999; Makarova et al. 2018) and regulatory transcription factors, e.g., WRKY and ethylene response factor (Pan et al. 2012; Dang et al. 2013; Huang et al. 2016)

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Indole Acetic Acid Homeostasis Maintains Reproductive Stability Under HS

IAA is the most abundant auxin in plants, orchestrating many essential developmental and physiological processes, including cell elongation and division, pollen development, anther dehiscence, and reproductive tissue development (Gray et al. 1998; Teale et al. 2006; Cecchetti et al. 2008; Sakata et al. 2010). Like other phytohormones, IAA plays a prominent role in plant adaptation to environmental stresses, including HS (Sakata et al. 2010; Franklin et al. 2011; Sun et al. 2012; Wit et al. 2014; Zheng et al. 2016; Zhang et al. 2018), by protecting photosynthesis and reducing photooxidation-mediated damage (Tognetti et al. 2012). The promotion of hypocotyl elongation through accumulated auxin is a well-established adaptive response by plants to HS (Gray et al. 1998). Subsequently, Franklin et al. (2011) shed mechanistic insight into the roles of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4)—a transcription factor (Stavang et al. 2009)—and the SMALL AUXIN UP RNA (SUAR) genes (SAUR19–24 and SAUR61–68) that regulate auxin biosynthesis by upregulating related genes under high temperature (28 °C) and thus promoting hypocotyl elongation in Arabidopsis. The underlying genes involved in auxin biosynthesis upregulation were: YUC8, YUC9, TAA1, and CYP79B2 (Stavang et al. 2009; Franklin et al. 2011; Sun et al. 2012). Furthermore, Wang et al. (2016) demonstrated that auxin co-receptors, TIR1 and AFB2, and HEAT SHOCK PROTEIN 90 (HSP90) are involved in root and hypocotyl elongation and lateral root formation of Arabidopsis in response to HS. The authors also described the supportive role of SGT1, a co-chaperone of HSP90, in response to increasing temperature. However, the mutant SGTb1 protein encoded by the eta3 gene inhibited auxin and TIR1 accumulation, preventing auxin-mediated growth under HS. Likewise, auxin’s role in maintaining the function of male reproductive organs, especially pollen tube growth/elongation and anther dehiscence, under HS is worth mentioning (Chen and Zhao 2008; Wu et al. 2008, 2016, 2019; Sharma et al. 2018). Under high-temperature stress, inhibition of endogenous auxin biosynthesis genes YUCCA flavin monooxygenase (Sakata et al. 2010) and UDP-glucosyltransferase 74b1 (UGT74B1) (Grubb et al. 2004; Sharma et al. 2018) reduced pollen tube elongation, causing spikelet sterility and reduced pollen vigor in barley and rice and male sterility in Arabidopsis and cotton (Sakata et al. 2010; Fu et al. 2015; Song et al. 2015; Zhang et al. 2017, 2018; Wu et al. 2019). In contrast, IAA content declined at the tetrad stage and increased at the tapetal degradation and anther dehiscence stages in cotton anthers of H05, a heat-sensitive genotype, under HS (Min et al. 2014). These contrasting results suggest that anthers need an appropriate balance of IAA to confer heat tolerance. Further, in heat-stressed rice, spikelet fertility declined due to inhibited panicle expansion, which is likely the result of reduced accumulation of IAA and GA1, an active type of GA (Wu et al. 2016).

The damaging effect of HS could be counteracted/minimized by manipulating auxin biosynthesis gene(s) and exogenous supplementation of auxin to restore pollen development and pollen tube growth and reverse spikelet sterility in crop plants (Sakata et al. 2010; Zhang et al. 2017, 2018; Wu et al. 2019) (see Table 2). Several auxin-responsive genes participate in the pollen viability restoration mechanism, which has been investigated in plants under stress (Sakata et al. 2010; Pazhamala et al. 2020). Diminished expression of YUC2 and YUC6 auxin biosynthesis genes in barley and Arabidopsis anthers under HS resulted in short stamens and pollen abortion (Sakata et al. 2010). Further, external application of synthetic auxin restored anther development and pollen fertility through enhanced expression of the MCM5 gene mediating anther cell proliferation and development. External supplementation of 1 and 10 μmol L–1 NAA increased auxin content in high-temperature susceptible mutants of Nipponbare rice under HS, reducing spikelet sterility by promoting pollen tube growth in pistils (Zhang et al. 2018) (see Table 3). Interestingly, Nipponbare, a heat-tolerant rice cultivar, had higher auxin and ROS and lower peroxidase activity in pistils under HS than the heat-sensitive mutant. Reduced peroxidase activity increases ROS expression, increasing auxin in pollen tubes, which mediated HS tolerance in Nipponbare (Zhang et al. 2018). However, increased accumulation of ABA and IAA-tryptophan in KSG1177 (heat-sensitive wheat genotype) under HS resulted in pollen abortion and low seed set (Bheemanahalli et al. 2020).

Table 2 Phytohormones and the possible mechanisms contributing to heat stress tolerance in various plants
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Table 3 Various phytohormones and their concentrations attributing to high-temperature stress tolerance in different plant species
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Understanding the interaction of IAA with other phytohormones could reveal various complex regulatory networks orchestrating plant growth and development and plant adaptation mechanisms under various environmental cues. Recent investigations have revealed crosstalk between IAA, BRs, and GA3, an active type of GA, which regulates hypocotyl growth under temperature stress in Arabidopsis (Stavang et al. 2009; Maharjan and Choe 2011). However, the molecular mechanisms of IAA for rescuing pollen fertility, reducing spikelet sterility, and controlling root growth in response to HS need further investigation.

CTKs Contribute Plant Thermal Acclimation Beyond Growth and Development

CTKs are multifaceted phytohormones contributing to basic plant development, including cell division, breaking seed dormancy, chloroplast biogenesis, apical dominance, leaf senescence, shoot differentiation, photomorphogenic development, and nucleic acid metabolism (Sakakibara 2010; for details, see Hwang et al. 2012). The role of CTK signaling, metabolism, and its crosstalk with other phytohormones for alleviating plants from the adverse effects of various environmental cues, including HS, has been investigated (Veselova et al. 2005; Jeon et al. 2010; Rivero et al. 2010; Ghanem et al. 2011; Hwang et al. 2012; Reguera et al. 2013; Fahad et al. 2015a; Yang et al. 2016). CTKs protect plants from the deleterious effects of HS by activating antioxidant mechanisms, protecting photosynthetic apparatus, or maintaining stay green and delayed senescence (He and Jin 1999; Thomas and Howarth 2000; Liu and Huang 2002; Zavaleta-Mancera et al. 2007). The role of kinetin in scavenging free radicals and switching on the antioxidant mechanism to prevent purine breakdown is worth noting (Chakrabarti and Mukherji 2003). Liu and Huang (2002) reported that CTKs play a role in alleviating HS in creeping bentgrass by activating antioxidant mechanisms and reducing lipid peroxidation activity. During the reproductive phase, HS reduced CTKs in rice panicles due to inhibited CTK biosynthesis, interrupted CTK transport from roots to shoots, and enhanced CTK catabolism (Skalák et al. 2016; Wu et al. 2016, 2017; Wu and Yang 2019). Maintaining sufficient CTK content under HS by stabilizing CTK biosynthesis and lowering CTK oxidase and dehydrogenase activity likely increases spikelet number per panicle in rice (Ha et al. 2012; Wu et al. 2016, 2017). High-temperature stress impaired CTK transport from roots to shoots in heat-sensitive rice genotypes—LYPJ, HHZ, and N22—reducing spikelet number per panicle due to the higher activity of CTK oxidase/dehydrogenase (Wu et al. 2017). However, exogenous application of CTKs maintained spikelet number per panicle in heat-sensitive rice cultivars under HS, indicating that CTKs play a pivotal role in stabilizing spikelet numbers under HS (Wu et al. 2017). Likewise, Wu et al. (2016) advocated that the external application of CTKs retained spikelet fertility and enhanced grain size in heat-sensitive rice cultivars. External application of 60 mg L–1 6-benzylaminopurine, a synthetic CTK (see Table 3), strengthened the wheat grain sink under HS by increasing endosperm cell number and carbohydrate accumulation during grain filling in the presence of elevated levels of IAA and zeatin riboside, a naturally occurring CTK (Yang et al. 2016). Banowetz et al. (1999) also implicated CTKs for improving grain weight in wheat under HS. Similarly, improved HS tolerance by maintaining a balance between ABA and CTK has been reported in maize (Cheikh and Jones 1994). An abundance of ABA and paucity of CTK impaired maize kernel development during HS (Cheikh and Jones 1994). Thus, the application of benzyladenine to maize under HS maintained a balance between ABA and CTK, ultimately preventing kernel abortion (Cheikh and Jones 1994). Recently, the inhibitory action of CTK degradation by INCYDE-F—an inhibitor of CTK oxidase/dehydrogenase—was investigated for mediating heat tolerance in HS-acclimated Arabidopsis plants (Prerostova et al. 2020; see Table 2). Interestingly, the external application of melatonin significantly ameliorated leaf senescence in perennial ryegrass under HS by enhancing CTK biosynthesis and limiting ABA biosynthesis (Zhang et al. 2017). Further insight into the underlying molecular mechanisms mediated by CTK controlling the grain-filling process and grain weight under HS will improve grain yield. Moreover, investigation of the key gene(s) controlling CTK biosynthesis and its regulation under HS will provide novel insights into the HS tolerance mechanism in plants.

ABA Regulates Plant Response to HS

ABA is an important phytohormone with a central role in regulating various processes from plant development and seed dormancy to myriad of biotic and abiotic stress responses (Verslues and Zhu 2007; Huang et al. 2017; Kang et al. 2017; Cho et al. 2018). It is an important signaling molecule for plants exposed to various environmental stresses, including water, cold, salinity, heavy metal toxicity, and heat, and well recognized in concert with other phytohormones regulating complex gene networks (Hsu and Kao 2003; Narusaka et al. 2003; Suzuki et al. 2016; Zhang et al. 2017; Rubio et al. 2018; Albertos et al. 2019). Importantly, ABA’s mechanistic role in regulating plant water status by controlling stomatal aperture closure during water stress is well-established (Daszkowska-Golec and Szarejko 2013). However, the mechanisms of ABA’s contribution to HS tolerance in plants are not fully understood (Suzuki et al. 2016; Zhang et al. 2017). Concerted efforts in recent decades have suggested that ABA contributes to both basal and acquired thermotolerance by preventing photoinhibition and improving photosystem II (PSII) efficiency, minimizing the damaging effects of chloroplast ultrastructure, activating various antioxidant mechanisms by producing various osmolytes, upregulating heat shock transcription factors (HSFs), and switching on various HSP gene(s) and genes actively participating in maintaining ‘energy homeostasis’ in plants under HS (Ivanov et al. 1992; Robertson et al. 1994; Gong et al. 1998; Larkindale and Knights 2002; Larkindale and Huang 2004; Larkindale et al. 2005; De Block and Lijsebettens 2011; Wang et al. 2017; Rezaul et al. 2018, 2019; Li et al. 2020). ABA-treated bromegrass (Bromus inermis) enhanced HS tolerance by producing various proteins and osmolytes (Robertson et al. 1994). Likewise, maize seedlings treated with ABA and Ca2+ increased HS tolerance by enhancing antioxidant enzyme activities and reducing lipid peroxidation activity (Gong et al. 1998). Zandalinas et al. (2016) revealed that the increased activity of ascorbate peroxidase 1 and multiprotein bridging factor 1 proteins, attributing plant acclimation under combined drought and HS in response to increased ABA, safeguarded plants against HS damage. Abscisic acid enables plants to withstand HS by enhancing H2O2 activity, activating antioxidant mechanisms, and accumulating HSPs (Li et al. 2014; Rezaul et al. 2019). In contrast, increased sensitivity to HS due to impaired ABA biosynthesis has been reported (Ding et al. 2010; Kumar et al. 2012) and supported in ABA-deficient mutants displaying higher sensitivity to HS damage (Wang et al. 2014a; Wu et al. 2017). The role of ABA in mediating the thermotolerance response by regulating HSF networks and downstream HSP encoding genes is well-established (Pareek et al. 1998; Campbell et al. 2001; Larkindale and Knights 2002; Larkindale et al. 2005; Huang et al. 2016; Suzuki et al. 2016). Considering this, how HSFA6b—an HSF acting as a hub for ABA signaling and serving in thermotolerance in association with ABA—has been investigated in Arabidopsis (Huang et al. 2016). The upregulation of FaHSFAc2 encoding HSPs in tall fescue (Festuca arundinacea Schreb) treated with ABA improved HS tolerance (Wang et al. 2017) (see Table 4). Likewise, Hu et al. (2018a) advocated that overexpression of TaHsfC2a regulatory genes, mediated by ABA under HS, conferred heat tolerance in wheat by switching on various HSPs and osmoprotective genes, viz., TaHSP16.9b, TaHSP62.4, HSP101b, TaGalSyn, TaHSA32, TaRof1, and TaβAmy1. An increased abundance of ABA in the embryo, relative to the endosperm, during grain filling, contributed to heat tolerance by inducing HSP accumulation (Walker-Simmons 1987). Further investigation by Walker-Simmons and Sesing (1990) provided evidence of higher ABA accumulation in wheat grains under high-temperature stress (25 °C) during grain filling.

Table 4 List of various phytohormone-induced genes contributing to heat stress tolerance in plants
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The role of ABA for maintaining energy homeostasis under HS has been explored (De Block and Lijsebettens 2011). Rezaul et al. (2018, 2019) and Chen et al. (2019) reported evidence of ABA’s participatory role in heat tolerance by enhancing sugar metabolism by switching on sucrose transporter genes, sucrose synthase (SUS) genes, and invertase (INV) genes to maintain ATP formation, and allocating sugars to alleviate the HS effect in rice spikelets, thus improving pollen fertility. Increased availability of carbohydrates, expression of HSP genes (HSP71.1 and HSP24.1), and ATP and NAD(H) production in Nipponbare (wild-type with flat leaf) rice subjected to exogeneous ABA application under HS revealed a significant role of ABA in enhancing heat tolerance (Li et al. 2020). However, the external application of ABA in an hts mutant of Nipponbare, featuring semi-rolled leaves, exhibited lower heat tolerance than its counterpart wild-type Nipponbare due to enhanced leaf temperature and respiration rate, which increased carbohydrate consumption and resulted in energy deficiency (Li et al. 2020). Furthermore, ABA-mediated drought priming enhanced HS tolerance in Festuca arundinacea by upregulating various regulatory genes, viz., CDPKs, DREBs, MYB, MYC, HSFs, and HSPs, but their role in conferring HS tolerance needs further investigation (Zhang et al. 2019). Unveiling the complex pathways of ABA signaling and its crosstalk with other phytohormones in response to HS and the regulatory gene network involved in inducing HS tolerance could provide insight into the role of ABA in plant HS tolerance.

Gibberellic Acid Regulates Plant Responses to HS

Gibberellic acid belongs to a group of natural diterpenoids. It is an essential phytohormone contributing to various developmental processes, including seed germination, stem elongation, and flower and fruit development (Sun and Gubler 2004; Yamaguchi 2008), and a key mediator of various abiotic stresses, including HS, in plants (Ko et al. 2007; Alonso-Ramírez et al. 2009). Vettakkorumakankav et al. (1999) illustrated the involvement of GA3 in regulating HS tolerance by treating normal and dwarf barley seedlings with GA3 and paclobutrazol (GA3 inhibitor) under HS. The GA3-treated normal and dwarf plants had more ion leakage and fewer photosynthetic pigments than the paclobutrazol-treated plants under HS; that is, the normal and dwarf plants treated with GA3 exhibited heat sensitivity (Vettakkorumakankav et al. 1999). Likewise, barley seedlings treated with a triazole, a GA3 inhibitor, had increased thermotolerance due to reduced GA3 and plant height (Sarkar et al. 2004). In rice, the incidence of HS during panicle initiation inhibited spikelet fertility by repressing panicle opening, which was ascribed to the depletion of IAA and GA1 (Wu et al. 2016). Inhibition of GA biosynthesis due to lower expression of various genes, viz., GA20ox1, GA20ox2, GA3ox1, and GA3ox2, regulating GA biosynthesis under HS was examined in Arabidopsis (Toh et al. 2012). In rice, Tang et al. (2008) documented the contributory role of GA3, IAA, and proline on pollen fertility and spikelet fertility damage imposed by high-temperature stress. Exogenous application of GA3 improved spikelet fertility in rice under HS, suggesting a significant role in protecting male reproductive organs under HS (Kwon and Paek 2016). Likewise, a GA3-mediated mechanism imparting HS tolerance in wheat by enhancing invertase activities increased grain sink activity under HS (Asthir and Bhatia 2014). Alonso-Ramírez et al. (2009) established that external addition of GA3 alleviated the inhibitory effects imposed by HS, oxidative, and salinity stresses by modulating SA biosynthesis and switching on transgene FsGASA4 (introduced from beechnut Fagus sylvatica), a GA3-responsive gene, in Arabidopsis seedlings. A recent investigation by Khan et al. (2020) demonstrated the basis of HS tolerance in date palm using externally applied GA3 in conjunction with silicon that modulated various genes, viz., GPX2, CAT, Cyt-Cu/Zn SOD, and glyceraldehyde3-phosphate dehydrogenase engaged in antioxidant mechanisms, HsfA3 encoding heat shock transcription factor, and the diminishing action of PYL4, PYL8, and PYR1 ABA signaling-related genes. Various gene(s) contributing to the HS response and tolerance due to phytohormone signaling are listed in Table 4.

Further investigation into genes related to GA biosynthesis, GA-signaling pathways and networks, and crosstalk of GA with other phytohormones using a systems biology approach could expand our understanding of GA for defending HS in crop plants (Verma et al. 2016).

SA Improves Plant Performance By Boosting Plant Defense Mechanisms Against HS

SA is a multifunctional hormone contributing to plant growth, seed germination, development, photosynthesis, transpiration, leaf senescence, redox homeostasis, and defense responses to various biotic and abiotic stresses, including HS (Javid et al. 2011; Vicente and Plasencia 2011; Fahad and Bano 2012; Bastam et al. 2013; Khanna et al. 2016; Zhang et al. 2017; Ahmad et al. 2018a; Kohli et al. 2019; van Butselaar and Van den Ackerveken 2020; Ding and Ding 2020). There is accumulating evidence of SA contributing to thermotolerance in various plants by activating antioxidant mechanisms, accumulating osmoprotectants and HSPs, and inducing excessive H2O2 production that mediates signal transduction (Dat et al. 1998a, b; Lopez-Delgado et al. 1998; Wang and Li 2006; Hayat et al. 2009; Wang et al. 2010, 2014b; Khan et al. 2013; Kohli et al. 2018a, b; Kaya et al. 2020a). The ameliorative role of SA in mediating HS tolerance by improving key processes, viz., photosynthesis and nitrogen assimilation activity, and increasing proline content by enhancing γ-glutamyl kinase and reducing proline oxidase enzyme activity has been established in wheat (Khan et al. 2013). External application of SA enhanced photosynthetic activity by improving net photosynthesis rate, Rubisco and PSII efficiency, chlorophyll content, proline content, soluble protein, HSPs, and sugar content, and reducing membrane damage, attributing to heat tolerance in wheat (Kousar et al. 2018), brassica (Kaur et al. 2009; Hayat et al. 2009), cotton (Galani et al. 2016), grapevine (Wang and Li 2007; Wang et al. 2010), tall fescue (Festuca arundinacea Schreb) (Pirnajmedin et al. 2020), and alfalfa (Wassie et al. 2020). Likewise, SA can alleviate plant injury from HS by activating the antioxidant defense system in various plant species (Dat et al. 1998a; Saleh et al. 2007; Kaur et al. 2009; Li 2015; Khanna et al. 2016; Zhang et al. 2017; Janda et al. 2020). Exogenous application of SA (50 ppm) along with H2O2 (30 ppm), ascorbic acid (70 ppm), and moringa leaf extract enhanced net photosynthetic rate and yield-contributing traits in cotton and protected plants from heat-induced injury by modulating the antioxidant enzyme mechanism (Sarwar et al. 2018; see Table 3). Similarly, the synergistic effect of SA and H2S on HS tolerance induced proline, betaine, and trehalose accumulation and enhanced antioxidant activity in maize under HS (Li 2015; Li et al. 2015). Moreover, SA treatment in rice at 40 °C alleviated spikelet damage by inducing higher activity of ROS-scavenging enzymes and accumulating soluble sugars, proline and IAA, ABA, and BR (Zhang et al. 2017). Feng et al. (2018) argued that H2O2 induced higher accumulation of SA, which improved pollen viability, minimized ROS activity, and inhibited tapetum programmed cell death in rice under HS. Brachypodium treated with 0.5 mM NaSA had elevated levels of glutathione-S-transferase under HS, which supports the role of SA in activating the antioxidant mechanism for ameliorating HS injury (Janda et al. 2020). Furthermore, various gene(s) have been induced by SA that contribute to HS tolerance (Wen et al. 2008; Feng et al. 2018; Janda et al. 2020). An SA treatment under high-temperature stress reduced excessive ROS in rice anthers and tapetum degradation by repressing caspase-3, thus preventing programmed cell death in anthers (Feng et al. 2018). Moreover, the authors postulated the role of EAT1, MIL2, and DMT1 genes (see Table 4), related to tapetum development, in SA-mediated protection of pollen abortion from HS; the molecular mechanism remains elusive. Increased expression of the phenylalanine ammonia-lyase enzyme contributing to phenylpropanoid metabolism due to external application of SA in grape berry increased the accumulation of phenolics, thus imparting HS tolerance in grape berry (Wen et al. 2008). Dang et al. (2013) speculated that the CaWARKY40 gene has an important role in regulating HS tolerance mediated by SA, JA, and ET in transgenic tobacco. Under HS, overexpression of CaWRKY40 enhanced expression of SA‐dependent NtPR1a/c, NtPR2 genes, JA‐responsive NtPR1b gene, JA biosynthesis‐associated NtLOX1 gene, and ET synthesis genes, viz., NtACS6 and NtEFE26.Therefore, ET-, SA-, and JA-mediated regulation of the CaWRKY40 gene could enhance downstream genes related to HS tolerance. Likewise, positive overexpression of the regulatory gene AtWRKY39 in cooperation with SA, JA, and calcium signaling pathways imparting heat tolerance has been established in Arabidopsis thaliana (Li et al. 2010). A model proposed by Divi et al. (2010) depicted the interplay of BR with SA, ABA, and ET mediating various stress tolerance mechanisms. They also explained the positive regulation of BR with NPR1, a regulator of SA-mediated defense genes, which plays a pivotal role in conferring HS tolerance. Thus, modulation of SA responsive gene(s) or SA signaling is an attractive approach for protecting plants from HS damage. However, the molecular mechanisms involved in SA minimizing ROS activity, protecting pollen grains from HS-induced damage, and inducing various regulatory genes under HS remain elusive.

Brassinosteroids as Emerging Phytohormones: Their Possible Roles in Regulating HS Tolerance

BRs are a novel class of polyhydroxylated plant steroid hormones synthesized in the endoplasmic reticulum (Kim et al. 2006; Northey et al. 2016; Nolan et al. 2017, 2020; Ahanger et al. 2018, 2020). They comprise brassinolide (BL), castasterone (CS), and various derivatives involved in regulating plant growth and development, seed germination, pollen tube growth, flower and fruit production, protein synthesis, nucleic acid synthesis, and various environmental stress responses, including HS (Grove et al. 1979; Clouse and Sasse 1998; Nakaya et al. 2002; Ogweno et al. 2007; Hayat et al. 2010; Zhang et al. 2013; Fahad et al. 2015b; Lozano-Durán and Zipfel 2015; Sharma et al. 2016; Ahmad et al. 2018b, c, 2019; Jan et al. 2020; Kaya et al. 2020b; Nolan et al. 2020). The working mechanism of BR signaling, from binding to cell surface receptors to switching on TFs in response to various stresses, has been investigated (Krishna 2003; Nolan et al. 2020). BR-mediated HS tolerance has been reported in B. inermis (Wilen et al. 1995), brassica (Brassica napus) (Dhaubhadel et al. 1999, 2002), tomato (Solanum lycopersicum) (Dhaubhadel et al. 1999; Singh and Shono 2005; Ogweno et al. 2010; Mazorra et al. 2011), Vigna radiata (Hayat et al. 2010), and barley (Hordeum vulgare) (Janeczko et al. 2011). The counteractive effect of BRs against HS in rice enhanced chlorophyll content, photosynthetic activity, stomatal conductivity, and filled seed numbers (Thussagunpanit et al. 2015a, b). The mechanism of BR that contributes to plant HS tolerance is mediated by various essential physiological and biochemical processes, viz., photosynthetic efficiency by maximizing the carboxylation rate of Rubisco and improving the efficiency of PSII photochemistry, enhancing chlorophyll content, stomatal conductivity, membrane stability, and proline content, reducing lipid peroxidation, activating antioxidant mechanisms, and maintaining redox homeostasis (Cao and Zhao 2008; Ogweno et al. 2007, 2010; Hayat et al. 2010; Kaur et al. 2018; Kaya et al. 2019). The ameliorative effects of trihydroxylated spirotane, an analog of BR, by decreasing the negative effect of HS on photosynthetic activity and promoting growth has been reported for banana under HS (Gonzalez-Olmedo et al. 2005). Thussagunpanit et al. (2015a) reported that EBR and 7,8-dihydro-8α-20-hydroxyecdysone (DHECH), a mimic compound of BR, impart HS tolerance. Rice plants treated separately with 1 nM EBR and 1 nM DHECH at the flowering stage at 40/30 °C (day/night temperature) protected photosynthetic apparatus by enhancing stomatal conductance and increasing the PSII quantum yield, improving plant yield (Thussagunpanit et al. 2015a). Likewise, exogenous application of EBR in Cucumis melo L. aided the recovery of chlorophyll content and improved photosynthesis and photochemical activity of PSI under high-temperature stress (Zhang et al. 2013, 2014). The role of BRs in minimizing ROS activity and maintaining plant cellular redox homeostasis by activating antioxidant and glyoxylase mechanisms under HS has been reported (Hussain et al. 2019). Likewise, Cao and Zhao (2008) revealed that BR contributed to HS tolerance in contrasting heat-tolerant and heat-sensitive rice cultivars by enhancing antioxidant enzymes and diminishing the lipid peroxidation process. Furthermore, Ogweno et al. (2007, 2010) reported HS tolerance at 40/30 °C in EBR-treated tomato plants due to improved photosynthetic activity that activated antioxidant mechanisms and concomitantly prevented photoinhibition and lipid oxidation activity. EBR in association with Si improved HS tolerance in a heat-sensitive wheat cultivar (PBW343) by switching on antioxidant mechanisms and producing excessive proline (Hussain et al. 2019) (see Table 1). Brassinosteroids induced the expression of various HSPs, viz., hsp100, hsp90, and hsp70, in tomato and B. napus, protecting the cellular protein synthesis machinery from HS (Dhaubhadel et al. 1999, 2002; Singh and Shono 2005). Crosstalk of BRs with JA, ABA, ET, and SA signaling pathways mediating HS tolerance has been demonstrated (Divi et al. 2010); however, the precise molecular mechanism remains poorly understood. A thorough understanding of BR-responsive BRASSINAZOLE RESISTANCE1 (BZR1)/BRI1-EMS SUPPRESSOR 1 (BES1) transcription factors controlling BR-targeted genes regulating the HS response in plants could help to develop HS-tolerant plants (Anwar et al. 2018).

Research is needed to clarify the participatory role of BRs and their crosstalk with other phytohormones for modulating the defense response of plants to HS.

ET and Its Crosstalk with Other Phytohormones Regulating HS Tolerance in Plants

ET is an important gaseous phytohormone involved in controlling various plant developmental processes and regulating various biotic and abiotic stresses, including HS (Larkindale and Knight 2002; Larkindale and Huang 2004; Larkindale et al. 2005; Muller and Munne-Bosch 2015; Abdelrahman et al. 2017). However, the regulatory mechanisms contributing to heat tolerance remain under investigation. Larkindale and Knight (2002) and Larkindale et al. (2005) reported ET-mediating basal thermotolerance after studying mutant, wild and transgenic Arabidopsis. Larkindale and Knight (2002) illustrated the involvement of Ca2+, SA, ABA, and ET in protecting plants from HS-induced oxidative damage by comparing seedling survival of an ET-insensitive mutant (etr-1), ABA-insensitive mutant (abi-1), nahG transgenic line with a depleted level of SA, and the corresponding wild-type Columbia, Landsberg erecta, and Columbia background Arabidopsis lines treated with HS. The significant role of these phytohormones conferring HS tolerance was confirmed in the mutants defective in these phytohormones, which had lower survival rates than the wild types. Larkindale et al. (2005) also confirmed the participatory role of ET, SA, and ABA in HS tolerance because the abi1 and abi2 mutants defective in ABA signaling had impaired acquired thermotolerance. However, ein-2 and etr-1 mutants defective in ET signaling had greater impairment in basal thermotolerance than acquired thermotolerance in Arabidopsis (Larkindale and Knight 2002). Recently, ET’s role in safeguarding plant cells from oxidative stress damage by switching on various antioxidant systems and HSF genes has been investigated in rice under HS through the external application of 1-aminocyclopropane-1-carboxylic acid (ACC), an ET precursor (Wu and Yang 2019). The upregulatory activity of Oryza sativa EIN2 (OsEIN2) and OsEIL1 genes, contributing to ET signaling pathways, and HsfA2b, HSFA2a, c, d, e, and f HSF genes protecting rice seedlings under HS was investigated (Wu and Yang 2019). ACC plays a role in the HS tolerance of creeping bentgrass (Agrostis stolonifera var. palustris) by increasing superoxidase dismutase (SOD), peroxidase (POX), and ascorbate peroxidase (APX) activities by protecting plants against HS-induced oxidative damage (Larkindale and Huang 2004). Jegadeesan et al. (2018) uncovered both upregulatory and downregulatory genes participating in increased ET biosynthesis and signaling that contribute to HS tolerance in tomato pollen grains (Table 4), which agrees with the findings of Firon et al. (2012), who reported that tomato plants pre-treated with ET releaser retained high-quality fertile pollen grain under HS. The role of ethylene-responsive factor (ERF) TFs, acting as a regulatory gene for controlling various abiotic stresses, is well recognized (Mizoi et al. 2012). Upregulation of various ERF genes, including Arabidopsis thaliana ERF1 (AtERF1) in Arabidopsis (Cheng et al. 2013), Cicer arietinum ERF116 (CarERF116) in chickpea (Deokar et al. 2015), and Solanum lycopersicon ERF5 (SlERF5) in tomato (Pan et al. 2012), reportedly confer HS tolerance. An increased abundance of ET during HS reduced wheat yields due to low spikelet fertility and reduced final grain weights (Cheng and Lur 1996; Yang et al. 2004; Hays et al. 2007; Huberman et al. 2013). A genome-wide association study elucidated five and 22 marker-trait associations for spike ET content and its association with spike dry weight, respectively, under HS in the field in a panel of 130 wheat genotypes (Valluru et al. 2017). The authors also found a negative correlation between spike ET content and spike dry weight and suggested exploring genes that control the reduced ET effect on plant yield under HS for improving plant yield. Likewise, inhibition of ET biosynthesis by downregulating ET signaling components, viz., ACS6 and ETR2, could improve grain yield under drought stress in rice and maize (Young et al. 2004; Wuriyanghan et al. 2009; Habben et al. 2014). Moreover, crosstalk of ET with other phytohormones, viz., ABA, SA, and JA, for controlling various abiotic stresses, including HS, by inducing ERF genes has been reported (Muller and Munne-Bosch 2015). Crosstalk of various phytohormones and phytohormone-responsive genes mediating HS tolerance is depicted in Fig. 2. Complete molecular understanding of ET-mediating basal thermotolerance and thermopriming, signaling pathway, induction of antioxidant mechanism and expression of ERFs viz., ERF95 and ERF97, and HSFs especially, HSFA2 could help improve HS tolerance in plant (Wu and Yang 2019; Huang et al. 2020; Singh et al. 2021).

Fig. 2
figure 2

Phytohormones regulate various genes controlling heat stress tolerance in plants. In response to heat stress, plants adapt by activating various transcription factors (TFs) that regulate various phytohormones. Abscisic acid (ABA) and jasmonic acid (JA) positively regulate DREB2A (Zhang et al. 2019; Tian et al. 2020) and ethylene (ET) positively regulates ethylene response factor (ERF) for attributing heat tolerance in plants (Cheng et al. 2013; Muller and Munne-Bosch 2015). In contrast, ABA negatively regulates ERF1 (Cheng et al. 2013) and jasmonic acid positively regulates bZIP3, WRKY40 for controlling heat tolerance (Dang et al. 2013; Balfagón et al. 2019). Several gene(s) are involved in mediating heat tolerance through their upregulation by exogeneous application of various phytohormones contributing heat tolerance: HSP101 and HSP70 are induced by JA and ET (Muller and Munne-Bosch 2015), FsGASA4 is induced by gibberellic acid (Alonso-Ramírez et al. 2009), SUT, SUS, INV, and RBOH1 are induced by ABA (Rezaul et al. 2018, 2019; Chen et al. 2019; Li et al. 2020), YUCCA, YUC1, and YUC9 are induced by auxin (Stavang et al. 2009; Franklin et al. 2011; Sun et al. 2012), CKX1 is induced by cytokinin (Macková et al. 2013), ERF1, EIN2, EIN3, HsfA1a, and HsfA2a induced by ET (Wu and Yang 2019), and EAT1, MIL2, DMT1, and MBF1c are induced by salicylic acid (Feng et al. 2018). However, PIN1, PIN2, and PIN5 are negatively regulated by strigolactone (Hu et al. 2018b)

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Strigolactones: Novel Players Mediating Plant HS Tolerance

Strigolactones (SLs) are a group of terpenoid lactones regulating plant architecture, mainly shoot branching and mesocotyl, hypocotyl, internode, and root elongation, to improve plant abiotic stress tolerance, including HS (Umehara et al. 2008; Toh et al. 2012; Brewer et al. 2013; de Saint Germain et al. 2013; Jia et al. 2014; Van Ha et al. 2014; Hu et al. 2018a, b). How SLs regulate HS tolerance in plants is unclear. Hu et al. (2018a, b) revealed that SLs applied externally to tall fescue (Festuca arundinacea Schreb) controlled HS tolerance by promoting root elongation through the upregulation of cell division and cell-cycle-related genes, such as PCNA, CycD2, and CDKB, and downregulation of the auxin receptor TIR1 gene and transport genes, such as PIN1, PIN2, and PIN5 (see Table 4). Subsequently, Hu et al. (2019) highlighted the role of SLs in conferring HS tolerance in tall fescue through leaf elongation by enhancing the activity of cell-cycle-related genes and diminishing the activity of auxin transport-related genes. Future research on the contribution of SLs to HS tolerance could advance our understanding of the mechanistic role of SLs in HS tolerance in plants.

Jasmonates: a Multifunctional Phytohormone Functioning Beyond Plant Biotic Stress Defense

Jasmonates (JAs) play a pivotal role in the plant defense response to various pathogens (Vijayan et al. 1998; Mei et al. 2006) and serve as multifunctional phytohormones contributing to plant development, growth, and reproduction processes (Wasternack 2007; Browse 2009). Their participatory role in controlling various abiotic stresses, including salinity, cold, light, heavy metals, and HS, in plants has been investigated (Dar et al. 2015; Kazan 2015; Sharma and Laxmi 2016; Per et al. 2018; Balfagón et al. 2019; Savchenko et al. 2019; Ali and Baek 2020). While JA plays an assertive role in response to various biotic and abiotic stresses in plants, it adversely affects plant growth and photosynthesis (Kazan and Manners 2012; Yang et al. 2012; Wasternack 2014).

The role of JA in heat tolerance in Arabidopsis was demonstrated by Clarke et al. (2009) by assessing electrolyte leakage in cell membrane treated with methyl jasmonate (MeJA) under HS—an external application of 5 µm MeJA protected cell viability under HS, while application > 5 µm reversed this result by enhancing membrane damage, indicating that its ability to ameliorate the negative effect of HS is concentration specific (Clarke et al. 2009). Shahzad et al. (2015) compared the effect of MeJA by treating pea plants with various concentrations of MeJA, viz., 50, 100, and 200 µM under HS (40 °C), cold stress (4 °C), and control (20 °C) conditions—200 µM of MeJA inhibited plant growth and reduced photosynthesis, stomatal conductance, and chlorophyll content under HS. To dissect the role of various regulatory TFs controlled by JA in response to HS, Dang et al. (2013) showed that external application of JA enhanced CaWRKY40 gene activity, conferring HS tolerance in pepper plants. Similarly, JA alleviated the negative effects of combined high light and HS by inducing several regulatory genes, viz., bZIP3, BHLH114, BHLH137, and WRKY8, which might allow plants to withstand heat and high light stress (Balfagón et al. 2019). Recently, Tian et al. (2020) reported the role of JAs in mediating heat tolerance through the DREB2A regulatory gene. Interplay/crosstalk of JA with other phytohormones mediating plant growth and development, complex signaling, and various biotic and abiotic stresses has been established (Raza et al. 2020). Synergistic and antagonistic effects of JA with other phytohormones play an essential role in providing abiotic and biotic stress tolerance in plants (Wang et al. 2020). The molecular role of JA in concert with SA imparting basal thermotolerance has been established in Arabidopsis by assessing electrolyte leakage in HS-treated double mutants, cpr5‐1 npr1‐1 cpr5‐1 jar1‐1, and the corresponding single mutant (Clarke et al. 2009). Similarly, Tsai et al. (2019) advocated that JA is associated with SA-enhanced heat tolerance and tomato yellow leaf curl virus resistance in tomato. Nevertheless, JA acts as an antagonist to ET for governing the HS response (Sharma and Laxmi 2016). The molecular mechanism and signaling of JAs and their crosstalk with other phytohormones controlling abiotic stresses, including HS responses, remain unknown (Yang et al. 2019). Furthermore, insights into the regulatory mechanisms of JAZ and JAV1 repressor proteins involved in regulating the transcription of various JA-responsive genes under various stresses, including HS, could improve our understanding of how JA is involved in plant HS adaptation (Raza et al. 2020).

Embracing Genetic Engineering for Manipulating Phytohormone-Responsive Gene(s) Regulating Heat Tolerance

Genetic engineering/transgenics is a powerful approach for deciphering the functional roles of various regulatory and phytohormone-responsive gene(s) contributing to HS tolerance (Cheng et al. 2013; Muller and Munne-Bosch 2015). Manipulation of phytohormone-responsive gene(s) could be a novel avenue for designing heat-tolerant crops. Previously, Alonso-Ramírez et al. (2009) monitored overexpression of the beechnut (Fagus sylvatica) GA-responsive gene FsGASA4 that induces endogenous SA, imparting higher thermotolerance in transgenic Arabidopsis. Likewise, in transgenic Arabidopsis, overexpression of ERF1, an ERF TF involved in ET signaling and response-mediated HS tolerance, upregulated the AtHsfA3 heat shock factor and various heat shock protein genes, viz., HSP23.6, HSP70, and HSP17.6A (Cheng et al. 2013). Youm et al. (2008) advocated the overexpression role of CaPF1, a pepper transcription factor ERF gene contributing to higher heat tolerance in transgenic potato. Similarly, overexpression of HSFA6b, serving as a positive regulator for ABA signaling, exhibited increased heat tolerance in transgenic Arabidopsis (Huang et al. 2016). Overexpression of the AtDWF4 gene involved in BR biosynthesis conferred HS tolerance in transgenic B. napus (Sahni et al. 2016). Overexpression of the Triticum aestivum BR-insensitive1 (TaBRI1) gene imparts thermotolerance in transgenic Arabidopsis by increasing membrane stability under HS (Singh et al. 2016). However, transgenic Arabidopsis containing the NahG (encoding salicylate hydrolase) gene is depleted of SA under HS, increasing electrolyte leakage due to heat shock and oxidative stress-mediated damage, indicating the essential role of SA in plant basal thermotolerance (Clarke et al. 2004). Increased expression of the tomato NAC transcription factor (SIJA2) in transgenic tobacco decreased heat tolerance due to a reduction in SA accumulation (Liu et al. 2017), suggesting a vital role of SA in conferring heat tolerance. Technological innovations, viz., next-generation sequencing, could unveil phytohormone-responsive candidate regulatory genes/noncoding RNAs regulating HS tolerance across genomes (Wang et al. 2019). Furthermore, augmentation CRISPR/Cas9-based genome editing is a promising approach for precisely modifying phytohormone-responsive TFs/genomic regions controlling the HS response for the future design of heat-tolerant crop plants (LeBlanc et al. 2018; Debbarma et al. 2019).

Perspective and Conclusion

Increasing HS events is a major issue for overall plant growth, causing great concern for global food security (Wahid et al. 2007). Among the various strategies for developing heat-tolerant crops, the role of phytohormones in mitigating the effect of HS deserves attention.

Exogenous application of various phytohormones could improve plant performance by protecting key physiological processes, viz., photosynthesis by minimizing photoinhibition, lowering lipid peroxidation, and stimulating antioxidant mechanisms under HS (Sharma et al. 2019). However, the complex molecular mechanisms of various phytohormones contributing to morpho-physiological adaptations in plants, such as minimizing ROS activity, rescuing pollen fertility, and protecting spikelet fertility, grain-filling process, and grain weights under HS need greater attention. Phytohormones regulate various biological regulatory pathways and processes related to HS. Phytohormones can switch on the signaling of various regulatory gene(s) under HS. Simultaneously, crosstalk/interactions of various phytohormones play a pivotal role in regulating the HS response in plants; however, understanding their complete molecular mechanisms controlling HS tolerance remains elusive. Among the phytohormone-based strategies for developing HS-tolerant crop plants, phytohormone priming could improve plant’s adaptation to HS. However, the bioformulations need rigorous testing under laboratory conditions before applying in the field. Likewise, manipulating phytohormone-responsive TFs/genomic regions controlling the HS response through genetic engineering/genome editing technologies is an emerging approach for designing HS-tolerant crops. As the role of phytohormone signaling and crosstalk in regulating plant growth in response to HS is complex, it merits further investigation (Verma et al. 2016). Moreover, the underlying regulatory genes and gene networks stimulated by the phytohormones in response to HS need further research.