
==== Front
Plant Commun
Plant Commun
Plant Communications
2590-3462
Elsevier

S2590-3462(24)00326-2
10.1016/j.xplc.2024.101009
101009
Review Article
Molecular mechanisms underlying the negative effects of transient heatwaves on crop fertility
Yao Qian 12
Li Ping 12
Wang Xin xinwang@cau.edu.cn
1∗
Liao Shuhua 1
Wang Pu 1
Huang Shoubing huangshoubing@cau.edu.cn
1∗∗
1 College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China
∗ Corresponding author xinwang@cau.edu.cn
∗∗ Corresponding author huangshoubing@cau.edu.cn
2 These authors contributed equally to this article.

24 6 2024
09 9 2024
24 6 2024
5 9 10100918 3 2024
4 6 2024
22 6 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Transient heatwaves occurring more frequently as the climate warms, yet their impacts on crop yield are severely underestimated and even overlooked. Heatwaves lasting only a few days or even hours during sensitive stages, such as microgametogenesis and flowering, can significantly reduce crop yield by disrupting plant reproduction. Recent advances in multi-omics and GWAS analysis have shed light on the specific organs (e.g., pollen, lodicule, style), key metabolic pathways (sugar and reactive oxygen species metabolism, Ca2+ homeostasis), and essential genes that are involved in crop responses to transient heatwaves during sensitive stages. This review therefore places particular emphasis on heat-sensitive stages, with pollen development, floret opening, pollination, and fertilization as the central narrative thread. The multifaceted effects of transient heatwaves and their molecular basis are systematically reviewed, with a focus on key structures such as the lodicule and tapetum. A number of heat-tolerance genes associated with these processes have been identified in major crops like maize and rice. The mechanisms and key heat-tolerance genes shared among different stages may facilitate the more precise improvement of heat-tolerant crops.

Transient heatwaves lasting for days or hours have become more frequent. If they coincide with heat-sensitive stages of crop development, transient heatwaves can greatly reduce yield by impairing pollen development, inhibiting floret opening, reducing pollen viability, and arresting the fertilization process. This review overviews current progress in the understanding of the effects of heatwaves on plant reproduction at the physiological and molecular levels, that holds great potential for improving the overall heat tolerance of crops.

Key words

heat stress
floret fertility
pollen
pollen tube growth
seed set
molecular mechanism
Published: June 24, 2024
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pmcIntroduction

Heatwaves are becoming an important threat to agricultural production in a warming climate, with high temperatures expected to increase in frequency, duration, and magnitude globally (Wang et al., 2020). These trends are projected to increase further by the end of this century (Murali et al., 2023). It is estimated that an increase of 1°C in temperature will reduce grain yield by 7.1% in maize (Zea mays L.), 6.0% in wheat (Triticum aestivum L.), and 5.6% in rice (Oryza sativa L.) (Zhao et al., 2017; Wang et al., 2020). Heat stress during the reproductive phase dramatically reduces spikelet fertility and grain number in many crops (Liu et al., 2023a; Xie et al., 2023). However, most of the relevant studies have focused more attention on heat stress at large temporal and spatial scales, with less focus on short episodes such as heatwaves. As growing evidence indicates, a short-term heatwave that coincides with the most heat-sensitive stages of the crop lifecycle causes significant reductions in end-of-season grain yields (Begcy et al., 2019; Wang et al., 2023c). The effects of transient heatwaves are not always immediately obvious and are therefore overlooked for crop yield determination. Our knowledge of these effects is limited, delaying improvements in heat tolerance cultivar and development of appropriate agricultural practices for a warming climate.

The reproductive stage of cereal crops is more sensitive to heat stress than the vegetative stage, with anthesis/flowering identified as the most sensitive stage, followed by microgametogenesis (Figure 1A–1C; Jagadish, 2020; Liu et al., 2023a). Transient heatwaves over days, hours, and even shorter time scales are expected to significantly reduce grain number if they coincide with heat-sensitive stages (Begcy et al., 2019; Wang et al., 2023c). A 48-h heat-stress treatment (35°C/25°C light/dark) applied at the tetrad stage resulted in germination-defective pollen grains in maize (Figure 1D; Begcy et al., 2019). Heatwaves (35°C) during microsporogenesis for 5 days reduced spikelet fertility by ∼35% in rice (Wassmann et al., 2009). At the anthesis stage, heatwaves lasting from minutes to hours inhibit anther dehiscence and pollination after spikelet opening (Figure 1E; Wang et al., 2021). Heat stress over 35°C for 10 min causes dysfunction of pollen fertility in rice (Figure 1F; Jagadish et al., 2007). A short period of heat stress (38°C for 6 h) after pollen has landed on the stigma can lead to pollination failure in maize by limiting pollen tube growth (Figure 1G; Wang et al., 2023c). In addition, transient heatwaves during anthesis can inhibit spikelet opening, resulting in pollination failure for monoecious, cross-pollinated crops such as maize (Liu et al., 2023a). With advances in physiological, cellular, and molecular genetic approaches, the mechanisms by which transient heatwaves affect spikelet fertility have been gradually revealed in cereal crops. This information (e.g., key heat-tolerance genes) is very important for the breeding of heat-tolerant varieties, but it has not been systematically collated.Figure 1 Heatwave-sensitive stages and relevant mechanisms in maize and rice.

(A) General morphology of the plant, tassel, and ear in maize.

(B) Morphology of the plant, spike, and floret in rice.

(C) Heat sensitivity with time during the growth period in cereals (e.g., maize), with anthesis being the most sensitive stage, followed by the tetrad stage of pollen development. V11–12, vegetative stages 11–12.

(D) Transient heatwaves at the tetrad stage disturb the normal process of microgametogenesis.

(E and F) Heatwaves during pollen shedding reduce pollen shed number and pollen viability. CT, control treatment; HT, heat treatment; EHT, excessive heat treatment.

(G) Heatwaves that occur after pollen has landed on the stigma interrupt the process of pollination.

Transient heatwaves at microgametogenesis reduce the viability of mature pollen in cereal crops

Meiosis in the microsporocyte that is essential for microsporogenesis is highly sensitive to heat stress, even within the protection of young anthers (Figure 2; Pacini et al., 1985; Ma, 2005; Müller and Rieu, 2016). Particularly at the tetrad stage, a short heatwave can disrupt chromosome segregation, resulting in abnormal tetrasomes (i.e., imbalanced trisomes and polytetrasomes with multiple nuclei in one spore) and aneuploid microspores (Wan et al., 2011; Jiang et al., 2019; Lei et al., 2020) in relation to signaling cascades, reactive oxygen species (ROS) accumulation, metabolic pathways (e.g., energy supply), structural integrity, and tapetum-specific programmed cell death (PCD) (Figure 2).Figure 2 Molecular mechanisms of pollen abortion caused by transient heatwaves during the tetrad stage.

Cross-section of the anther, including 4 pollen sacs. The anther wall has 4 layers: the epidermis (outer), inner wall, middle layer, and the innermost tapetum. Transient heatwaves disrupt the normal expression of key genes and downstream proteins in microspore cells and tapetal cells. Heat stress disrupts ROS signaling, glucose metabolism, hormone pathways, and pollen structure, leading to tapetal cell death and impaired pollen development. A1Asp, A1 aspartic acid enzyme; HXT, hexose transporter; VLCFA, very-long-chain fatty acid.

Transient heatwaves rapidly promote the synthesis of abscisic acid (ABA) by increasing the transcript levels of NCED5 and SAPK2 (stress-activated protein kinase 2) in microspore cells (Zhao et al., 2023). The stress signal is sensed by specialized cytoplasmic receptors (PYR/PYL/RCAR) and then disrupts the interaction between SnRK2s and type 2c protein phosphatases (PP2Cs). This disruption prevents the PP2C-mediated dephosphorylation of SnRK2s and consequently increases the accumulation of SAPK2 through phosphorylation (Fujii et al., 2009; Mittler and Blumwald, 2015). The interaction between SAPK2 and DEAD-box ATP-dependent RNA helicase eIF4A-1 (RH4) is crucial for ROS generation (Zhao et al., 2023). SAPK2 further activates the redox sensor oxidative stress-activated protein kinase 1 (OST1) and the NADPH oxidases RBOHD/F, resulting in a rapid increase in reactive oxygen (e.g., H2O2) production, which directly activates the annexin OsANN1 and the cyclic nucleotide-gated ion channel (CNGC) in the plasma membrane of rice (Qiao et al., 2015; Jung et al., 2023). This activation promotes Ca2+ influx and subsequently activates Ca2+ sensor proteins (CBLs), thereby amplifying ROS signals through the RBOHD/F pathway (Cui et al., 2020; Rai et al., 2020). The increased ROS are transported into the cytoplasm through channels such as plasma membrane intrinsic proteins (PIPs) (Rhee et al., 2017), disrupting ROS equilibrium and damaging cellular membranes (Zhao et al., 2018). In addition, heat-induced activation of R2R3-MYB transcription factor 12 (MYB012) suppresses the expression of flavone synthase, thus reducing the capacity for ROS scavenging (Zhou et al., 2021). Under heat stress, the abundance of mitochondria in the microspores and tapetal cells increases, which also increases ROS production (Lee and Warmke, 1979; Kumar et al., 2014). This heat-induced response, either directly or indirectly via ABA and Ca2+ signaling, can activate phospholipase D-induced phosphatidic acid, which in turn promotes ROS generation (Mishkind et al., 2009; Hayes et al., 2021; Kong et al., 2024).

Heatwaves during the tetrad stage can affect the normal PCD of tapetal cells, thereby affecting the structural organization of the pollen cell wall (Lei et al., 2020), as well as carbohydrate metabolism (Begcy et al., 2019). For instance, short-term heatwaves can downregulate the transcript levels of 3-ketoacyl-coenzyme A and BnaA02g34360D, which is homologous to cellulose synthase CESA-6, thereby inhibiting formation of the pollen coat in Brassica napus (Heizmann et al., 2000; Persson et al., 2007; Lohani et al., 2020). Heatwaves also lead to the downregulation of genes associated with starch and energy biosynthesis, including GRMZM2G027955, which encodes an ADP-glucose pyrophosphorylase (AGPase) that catalyzes a pivotal step in starch synthesis, and they reduce the activities of cell wall invertase (cwINV), sucrose transporters (e.g., SUT1), and INV, thus increasing pollen sterility (Begcy et al., 2019; Lohani et al., 2020; Deng et al., 2021). A recent study reported that a 48-h heat event at the bicellular stage of pollen development could adversely affect sperm cell development, particularly by interfering with the spindle assembly checkpoint and the metaphase-to-anaphase transition (Li et al., 2024).

Pollen development also relies on interaction with the somatic tissues (especially the tapetal cell layer) that encase the developing pollen grains (Figure 2; Lewandowska et al., 2022). The tapetum, as the most conspicuous anther cell layer, provides essential materials for pollen wall formation, microspore development, and pollen maturation (Figure 2; Thomson and Wellmer, 2019), which is closely related to tapetal PCD (Gómez et al., 2015; Wei and Ma, 2023). Timely tapetum PCD, which is normally initiated after the first pollen mitotic division, enables the release of tapetum materials into the developing pollen grains (Li et al., 2006), providing nutrients, enzymes, carbohydrates, and other compounds required for development of the pollen wall (Parish and Li, 2010; Khan et al., 2022). However, heatwaves can disturb the timing of tapetum PCD and the progression of pollen development (Chaturvedi et al., 2021).

Heatwaves suppress expression of the tapetum-specific gene MALE STERILITY 1 (MS1) and thus reduce the interaction between MS1 protein and the transcription factor TAPETUM DEGENERATION RETARDATION (TDR), resulting in a dramatic decrease in gene expression (e.g., ETERNAL TAPETUM 1 [EAT1] and aspartic proteases AP25 and AP37, which are required for the initiation of tapetal PCD in rice) (Daneva et al., 2016; Wu et al., 2022). Likewise, heatwaves inhibit the interplay between PERSISTENT TAPETAL CELL1 (PTC1) and TDR and downregulate expression of the cysteine protease genes CP1 and C6, which encode specific lipid transfer proteins that regulate tapetum development and degeneration, thereby delaying tapetal PCD (Niu et al., 2013; Daneva et al., 2016). A recent study by Wang et al. (2023b) revealed that UDP-glucose epimerase 1 (UDG1), located downstream of TDR, directly regulates the expression of EAT1 and interacts physically with the EAT1 protein to control tapetum degradation. Expression of the thermosensitive male sterility gene TMS9-1, also known as PTC1 or OsMS1, is stringently regulated. Deviations in expression levels, both lower and higher than optimal, can lead to thermosensitive genetic male sterility (TGMS; Peng et al., 2023a). Heatwaves also induce autophagy in developing anther wall cells and microspores by repressing the expression of A1 aspartic protease and its regulator MYB DOMAIN PROTEIN 80, leading to tapetal PCD abortion (Phan et al., 2011; Dündar et al., 2019). The expression of GIBBERELLIN MYB GENE, which is located upstream of PTC1, MS1, and TDR, is also sensitive to transient heat stress (Wang et al., 2012). In addition, tapetum cells are equipped with a large number of mitochondria (Wang et al., 2017), which can promote the generation of ROS (Mittler, 2017). The elevated ROS levels generated from tapetum cells or microspore cells also disturb the normal process of tapetal PCD (Xie et al., 2022). In rice, the mechanism of TGMS under high-temperature conditions is intimately linked to mutations in specific genes. Key genes implicated in this process include OsTMS5, OsTMS10, OsTMS15, OsTMS18, and OsTMS19 (Zhou et al., 2014, 2024; Yu et al., 2017; Zhang et al., 2022; Han et al., 2023). In reported TGMS lines, these genes play distinct roles during pollen formation. For instance, under high temperatures, loss of function of the RNase ZS1 protein in tms5 plants leads to overaccumulation of UbL40 transcripts, which in turn triggers pollen developmental defects and male sterility (Zhou et al., 2014). The product of the TMS10 gene is essential for tapetum degradation and pollen wall formation, and under high temperatures, the tapetum cells in tms10 plants fail to degrade normally (Yu et al., 2017). OsTMS15 is associated with defects in the initiation of the tapetum layer (Han et al., 2023), OsTMS18 leads to defects in the exine layer (Zhang et al., 2022), and OsTMS19 encodes a mitochondrially targeted pentatricopeptide repeat protein that is highly expressed in the tapetum and induces ROS accumulation under high temperatures, affecting formation of the pollen inner wall (Zhou et al., 2024). Studies have shown that there is significant ROS accumulation in tms5, ostms15, and ostms18 plants under high temperatures during stages 10–11 (vacuolate microspore stage to vacuolate pollen stage) of anther development (Zhou et al., 2024). These genes exhibit different sensitivities to high temperatures (Peng et al., 2023b). CRITICAL STERILITY-INDUCING TEMPERATURE 2 encodes a RING-type E3 ubiquitin ligase, and its functional deficiency enhances the thermosensitivity of TGMS lines based on tms5 (Peng et al., 2024). Mutations in these genes lead to abnormal pollen development under high-temperature conditions, and the underlying mechanisms are highly relevant to our understanding of pollen developmental anomalies intransient high-temperature environments. Heat stress can upregulate SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 17, which positively regulates ASCORBATE PEROXIDASE 1 to produce ascorbate peroxidase, a major antioxidant enzyme in the ROS scavenging pathway, thus decreasing ROS accumulation in the tapetum (Chaturvedi et al., 2015; Sun et al., 2022). By contrast, heat-induced suppression of ABORTED MICROSPORES (AMS) curtails ROS generation by reducing the activity of the ROS-producing enzyme RESPIRATORY BURST OXIDASE HOMOLOG E (RBOHE), which is expected to delay tapetal PCD (Xie et al., 2014). Wheat homologs of TDR and AMS play a significant role in heat stress responses and may influence pollen morphogenesis and tapetal degeneration (Browne et al., 2021).

In summary, transient heatwaves lasting from hours to days that occur at the microgametogenesis stage can greatly reduce mature pollen viability of many crops, in association with several key genes involved in stress signaling, ROS metabolism, cellular structure, carbohydrate metabolism, tapetal PCD, and their interactions.

Transient heatwaves during anthesis reduce spikelet fertility

The spikelet, which comprises a pair of glumes enfolding one or more florets, is a grass-specific primary inflorescence unit. As flowering approaches, lodicules located at the base of the florets expand rapidly, and filaments elongate; the glume opens, exposing anthers that then dehisce to release pollen. These processes frequently meet with transient heatwaves in the late morning or midday, resulting in reduced pollen shed numbers and pollen viability (Figure 3; Wang et al., 2021; Liu et al., 2023b).Figure 3 Molecular mechanisms by which transient heatwaves limit floret opening, restrict pollen shedding, and reduce pollen viability.

(A) Heatwaves disrupt the synthesis or levels of key regulatory substances within the lodicule, such as JAs, BRs, and ROS, which are essential for water uptake and ORS accumulation. These disruptions hinder lodicule expansion, which is critical for spikelet opening.

(B) Filament elongation is mediated by phytohormones and inorganic ions, which are impeded or even inhibited by heatwaves, but the mechanism linking the two remains elusive. CK, cytokinin.

(C) Heatwaves impede or delay the secondary thickening of the anther endothecium, suppress pollen grain expansion, and inhibit the activity of enzymes necessary for dehiscent cavity formation, ultimately leading to anther closure and hindering pollen shed. SlCysEP, cysteine proteases.

(D) Heatwaves in the late morning can disrupt pollen morphology, causing collapse of the pollen aperture and reducing pollen viability. “?” indicates speculated possible mechanisms. The pink S-curve indicates temperature changes in 1 day. Positive effects are indicated by normal arrows and negative effects by T-headed arrows.

Before flowering, lodicules accumulate increased levels of osmotic regulation substances (ORSs), including soluble sugars and potassium ions (K+), to promote water absorption and complete expansion (Figure 3A; Heslop-Harrison et al., 1987; Wang et al., 1991). Jasmonates (JAs) play pivotal roles during this process (Li et al., 2018b), with MYC2 serving as a key transcriptional activator in the downstream signaling of JAs (Chini et al., 2007). However, heat stress significantly reduces JA levels in lodicules and slows lodicule expansion (Chen et al., 2020). Heat stress is thought to reduce the expression of JA biosynthesis genes and inhibit glume opening (Du et al., 2013). Downregulation of rice allene oxide cyclase (OsAOC), a crucial gene for JA biosynthesis in rice lodicules, leads to JA deficiency, thus slowing ORS and water accumulation (Liu et al., 2017). Furthermore, recent studies have revealed that manipulation of the JA-related genes OPDA REDUCTASE 7, CHILLING TOLERANCE 1, and JASMONATE ZIM-DOMAIN PROTEIN 9 can influence the cellulose and hemicellulose composition and the stiffness of lodicule cell walls by regulating sugar metabolism, thus controlling flowering time in rice (Wang et al., 2024). JAs also enhance α-amylase activity in rice lodicules, facilitating the conversion of starch to soluble sugars (Yang et al., 2020). In plants that lack amyloplasts (e.g., maize and rye), ions such as K+ are proposed to be more important factors affecting ORSs of lodicules (Zhou et al., 2022), and K+ accumulation in lodicules is regulated by JAs (Liu et al., 2017). Calcium (Ca2+) can modulate JA biosynthesis through Ca2+ sensors and regulate lodicule expansion (Qin et al., 2005; Wang et al., 2019a). The distribution and form of Ca2+ within rice lodicules were markedly altered by exogenous JA treatment, indicating a synergistic effect of Ca2+ and JAs on OSR contents (Qin et al., 2005). There is also evidence that JAs can promote floret respiration and facilitate CO2 release to promote lodicule expansion, with the latter possibly occurring via acidification of the lodicule cytosol and enhancement of cell wall relaxation as auxiliary pathways (Wang et al., 1989; Zeng et al., 1999). Moreover, spraying with exogenous JA enhances the activity of the antioxidant system and inhibits the production of ROS in lodicules, which are crucial for alleviating heat-stress-induced glume closure (Yang et al., 2020). However, heat stress at flowering not only reduces lodicule soluble sugar and starch while decreasing catalase and α-amylase activities but also lowers JA and methyl jasmonate levels, leading to the disruption of key links in glume opening (Yan et al., 2016; Chen et al., 2020; Yang et al., 2020). In addition, brassinosteroids (BRs) play important roles in promoting maize glume opening under heat stress, probably by enhancing the cytoskeleton of lodicules (Liu et al., 2018, 2023b; Ruan et al., 2018). Heat stress can downregulate expression of ZmBZR (BRASSINAZOLE-RESISTANT), a key regulator of BR synthesis (Manoli et al., 2018). A number of genes that regulate daily flowering patterns have recently been identified. For example, DIURNAL FLOWER OPENING TIME 1, also known as EARLY MORNING FLOWERING 1, interacts with pectin methylesterases (PMEs) and endo-1,4-β-glucanase to regulate the level of pectin methylation and the pectin and cellulose content in the cell walls of rice lodicules, and their knockout leads to early flowering (Wang et al., 2022; Xu et al., 2022a). These relevant findings offer a potential direction for mitigating the effects of transient heatwaves during flowering by avoiding the hottest spells of the day.

Stamen filament elongation is also a necessary process for anther exposure from the glume, which typically occurs simultaneously with lodicule expansion (Figure 3B; Heslop-Harrison and Heslop-Harrison, 1996). However, filament elongation is greatly slowed under heat stress (Katano et al., 2020). K+ acts as a major osmotic factor in filament elongation (Heslop-Harrison et al., 1987). JA, BR, gibberellin (GA), and auxin also play important roles in promoting filament elongation as individual or combined factors (Reeves et al., 2012; Wang et al., 2023a). However, the specific mechanisms that underlie the effects of heat stress on filament elongation remain to be fully clarified, as there have been very few studies in this area.

After anther exposure, anther dehiscence proceeds as the temperature rises and relative humidity decreases over the course of the morning, and pollen grains are released from the anther pores (Figure 3C). During pollen maturation, the anther endothecium and the secondary thickening that is located within this cell layer undergo expansion and deposition, respectively. Subsequently, the septum located between two pollen sacs is enzymatically lysed and breaks down. The stomium then splits as a consequence of tension forces that result from pollen swelling and anther dehydration, leading to anther opening (Matsui et al., 1999a; Wilson et al., 2011). However, these processes are also sensitive to transient heatwaves (Raja et al., 2019). Weak secondary thickening of the anther endothecium was observed in heat-stressed rice, which increased the difficulty of anther opening (Hu et al., 2021). The expression of genes (i.e., TEOSINTE BRANCHED1, CYCLOIDEA, and PCF FAMILY 24) involved in endodermal thickening is disrupted in maize under heat stress, resulting in delayed endodermal thickening and leading to closed anthers and male sterility (Wang et al., 2015; Khan et al., 2022). The pressure from rapid pollen expansion shortly before anther opening, coupled with the secondary thickening near the stomium, is likely a more important contributor to anther opening (Matsui et al., 1999b), and heat stress can inhibit this process, resulting in poor dehiscence (Matsui et al., 2000). In addition, Keijzer et al. (1996) reported that in maize, dehiscent cavity formation is an enzymatic process, and the activities of the relevant enzymes (e.g., polygalacturonases, cysteine proteases) can be greatly reduced under heat stress (Senatore et al., 2009; Marciniak and Przedniczek, 2021). In particular, during pollen release, heatwaves lasting days, hours, or even minutes can significantly reduce pollen viability (Jia et al., 2020; Lohani et al., 2020). Heat exposure diminishes pollen viability by decaying mitochondria and suppressing the activity of enzymes in sucrose metabolism, thereby compromising energy provision (Sun, 2023). Moreover, pollen possesses a distinct lipidome, as noted by Ischebeck (2016). Lipid composition of wheat and sorghum pollen grains is altered in response to heatwaves as an adaptive mechanism, but this may also contribute to pollen dysfunction (Prasad and Djanaguiraman, 2011; Narayanan et al., 2018). Heat stress reduces the expression of CESΑ6, a gene encoding the cellulose synthase complex in pollen, weakening adaptation of the pollen cell wall to heat (Lohani et al., 2020). Extreme heatwaves can also result in rapid pollen dehydration and thus disrupt pollen morphology and structure, leading to reduced pollen viability. In addition, waxes are important components of the tryphine on the pollen surface, serving to alleviate environmental stress (Lewandowska et al., 2020). In rice, a naturally occurring allele with a loss of THERMOTOLERANCE 2 (TT2) function was found to maintain normal expression of the wax synthesis gene Wax Synthesis Regulatory 2 (OsWR2) by inhibiting the heat-induced increase in cytoplasmic Ca2+, thus enhancing heat tolerance (Kan et al., 2022). Nevertheless, few studies have focused on the effects of transient heatwaves on pollen viability over such short periods.

The heat-tolerance genes TT1 and TT3 confer thermotolerance during both vegetative and reproductive growth in rice (Li et al., 2015b; Zhang et al., 2022). TT1, notably OgTT1 in African rice (Oryza glaberrima), effectively eliminates the cytotoxic denatured proteins caused by heat stress and protects cells from heat stress (Li et al., 2015b). TT3 comprises TT3.1 and TT3.2, and during heat stress, TT3.1 aids in maintaining chloroplast stability by mediating degradation of the chloroplast precursor protein TT3.2, whose accumulation is detrimental to chloroplasts (Zhang et al., 2022). Overexpression of TT3.1 or knockdown of TT3.2 significantly increases yield under heat stress (Zhang et al., 2022). Studies on TT1, TT2, and TT3 have also highlighted enhanced heat tolerance and sustained yield during the reproductive stage under heat stress (Li et al., 2015b; Kan et al., 2022; Zhang et al., 2022).

Transient heatwaves during pollination lead to fertilization failure

Pollination, as a key determinant of seed fertilization, is an intricate process in the crop life cycle that encompasses several critical stages, from pollen–stigma adhesion to sperm release toward the embryo sac for double fertilization (Figure 4A; Dresselhaus and Franklin-Tong, 2013). This process is conspicuously thermosensitive, especially pollen grain adhesion, hydration, and germination on the stigma and style-mediated pollen tube growth (Prasad and Djanaguiraman, 2014; Shi et al., 2018; Wang et al., 2023c).Figure 4 Molecular mechanisms underlying the failure of cereal crop fertilization caused by transient heatwaves.

(A) Pistil structure and the pollen tube journey, along with heat sensitivity at 5 stages, using rice (self-pollinated) and maize (cross-pollinated) as examples. Shades of red within the thermometer represent different sensitivities, and gray indicates uncertainty.

(B) Pollen germination sequence: a schematic illustrating the process of mature pollen germination on the stigma.

(C) Pathways that mediate the effects of heat stress on pollen germination. cAMP, cyclic adenosine monophosphate; cGMP, cyclic guanosine monophosphate; (E)PG, (exo)polygalacturonase; Glu, glucose; RBOHs, respiratory burst oxidase homologs; UDP-glu, uridine diphosphate glucose.

(D) Summary of the effects of heat on pollen germination, emphasizing structure, signal transduction, and energy supply.

(E) Pathways involved in the effects of heat stress on pollen tube elongation within TTs.

(F) Molecular basis of the inhibition of pollen tube elongation by heat. For a detailed analysis, refer to the main text.

After landing on the stigma, pollen grains rapidly absorb water from the stigma and initiate internal metabolism, a process called pollen hydration (Figure 4B). The pollen wall, especially the innermost layer (the plasma membrane; Figure 4C), which is mainly composed of proteins and lipids, plays a pivotal role in pollen hydration (Edlund et al., 2004). However, heat stress can damage the structural integrity of these membranes and hamper pollen hydration (Das et al., 2014).

Pollen germination and early pollen tube growth are expected to be more stress sensitive (Tunc-Ozdemir et al., 2013). During pollen germination, Ca2+ acts as a pivotal orchestrator by establishing gradients below the pollen germination site, a process essential for germination activation and polarized growth (Sze et al., 2006; Ge et al., 2007). Key proteins such as CNGCs and annexins regulate Ca2+ permeability and signaling in cell membranes (Gao et al., 2012). A study by Cui et al. (2020) highlighted the role of OsCNGC14 and OsCNGC16 in the heat resilience of rice (Figure 4D). Heat stress can also increase levels of cyclic nucleotides (cNMP) such as cAMP and cGMP to activate CNGCs, thus inducing Ca2+ influx in pollen grains (Gao et al., 2012; Tunc-Ozdemir et al., 2013). Likewise, a surge in the accumulation of annexins was detected in rice and wheat pollen in response to heatwaves, indicating their possible roles as sensors in heat signaling (Kamal et al., 2010; Jami et al., 2012). The influx of Ca2+ can activate transcriptional regulatory factors of the heat shock response (HSR), such as heat shock factors (HSFs), that can protect plants from heat stress, by binding to Ca2+/calmodulin (CaM) (Liu et al., 2008). Calcium-dependent protein kinases (CDPKs) are well known for the perception and transmission of Ca2+ signals under environmental stress (Kong et al., 2013). Under heat stress, there is notable upregulation of OsCDPK25 in rice, indicating its potential role in enhancing heat tolerance (Wan et al., 2007). In addition, increased Ca2+ levels in pollen can activate the ROS-producing enzyme RBOHD, either directly or indirectly (via CDPKs) (Kobayashi et al., 2007). The conversion of O2⋅− produced by RBOHD to H2O2 leads to membrane depolarization and subsequent cellular entry, which triggers the ROS/redox signaling network and activates HSFs (Mittler et al., 2012).

ROS, as vital signaling molecules, play a crucial role in pollen hydration and germination by regulating cuticular permeability (Gao et al., 2016). Upon germination under normal conditions, there is a surge of ROS production within the cytoplasm and cell wall of pollen grains (Smirnova et al., 2009). ROS can also activate the HSR, triggering HSF–heat shock protein signaling in response to heat stress (Mittler et al., 2012). In addition, ROS trigger the unfolded protein response (UPR) within the endoplasmic reticulum (ER), which can also protect plants from heat stress (Mittler et al., 2012). Another stress sensor in the ER, INOSITOL REQUIRING ENZYME1 (IRE1) can enhance bZIP60 levels under heat stress, and the latter functions as a link between the UPR and the HSR through its distribution in different cellular compartments (Li et al., 2020). It has been suggested that there may be an interaction between ROS and IRE1 in response to heat stress. However, excessive ROS accumulation is a primary response to heat stress that can lead to membrane damage in pollen (Das et al., 2014). These two aspects of ROS suggest that an appropriate ROS level should be maintained in pollen grains when improving crop tolerance to transient heatwaves during pollen release.

Pollen germination operates in an autotrophic mode during the initial phase, depending on accumulated substances (e.g., sugars, pectinases, actins, proteins) (Stephenson et al., 2003; Dai et al., 2007; Wei et al., 2010). However, heatwaves decrease carbohydrate accumulation in pollen grains (Begcy et al., 2019) by reducing the activity of sucrose synthase (SUS), and shrunken 1 (SH-1) and SUS1 were downregulated during anthesis in response to a 15-day heat stress treatment (Li et al., 2022). Heatwaves may also reduce the conversion and transport of exogenous sucrose into pollen grains by reducing the activity of cwINV, and levels of carbohydrates such as hexose are thus further reduced (Borghi et al., 2019). These heatwave-induced changes in carbohydrate metabolism impede the energy supply needed for pollen germination.

Heat stress may also hinder pollen cell wall remodeling and the formation of pollen tube emergence zones by disturbing expansin (EXP) and polygalacturonase (PG) release, signaling pathways, and protein synthesis (Allen and Lonsdale, 1993; Cosgrove et al., 1997; Wu et al., 2018; Cascallares et al., 2020). Heatwaves can significantly reduce the expression of ribosomal protein S19, which has a pivotal role in cellular protein synthesis (Jagadish et al., 2010). Furthermore, the aperture of the pollen grain is crucial for its germination (Li et al., 2018a; Zhang et al., 2020), but heat stress in sorghum and maize leads to loss and/or collapse of the aperture in mature pollen, probably associated with dysfunction of cell wall remodeling (Djanaguiraman et al., 2014; Wang et al., 2019b).

The pollen tube, with a wall composed predominantly of pectin (callose in the inner layer and pectic fibers in the outer), is the fastest-growing plant cell (Figure 4E). The tube tip is almost entirely composed of pectin, primarily methyl-esterified homogalacturonan (HG), which is crucial for tube wall plasticity (Chebli and Geitmann, 2007). PMEs play an important role in enhancing the cell wall integrity of the pollen tube by mediating the methylation of pectin (especially HG) (Wolf et al., 2009; Guan et al., 2013). Heat stress can increase the gene expression levels of five Hys genes involved in pectin metabolism, including PMEs in rice, which may alter pectin levels in rice florets (Wu et al., 2015). These five Hys genes and their associations with reported heat-responsive genes are expected to be important for revealing the molecular mechanisms that underlie heat-stress tolerance of crop reproductive organs (Wu et al., 2015). In addition, callose plugs are essential for maintaining the tube cell in the apical region, and heat stress can result in abnormal plugs, thus inhibiting tube growth in wheat (Saini et al., 1983; Leroux et al., 2015).

Polarized expansion of the pollen tube depends on the actin cytoskeleton and Ca2+ gradients in the apical region, which direct vesicular transport from the Golgi to the cell wall of the tube tip (Hepler et al., 2001). During this process, RHO-RELATED GTPASES FROM PLANTS (ROPs) regulate the dynamics of apical filamentous actin (F-actin) and Ca2+ gradients (Gu et al., 2003; Ou and Yi, 2022; Xu et al., 2022b). Heatwaves that occur at this stage can damage F-actin and inhibit Ca2+ oscillations, especially in the subapical region of the tube, disrupting cytoskeletal structure and function, vesicle transport, and cell wall deposition and thus hindering polar tip growth (Parrotta et al., 2016; Weigand et al., 2021). In addition, ROS can signal pollen tube elongation by interacting with other factors such as Ca2+ ions (Potocký et al., 2012; Santiago and Sharkey, 2019; Aloisi et al., 2022). However, excessive ROS accumulation induced by heatwaves inhibits pollen tube growth, an effect that can be partly reduced by flavonols (Muhlemann et al., 2018).

The heatwave-induced suppression of pollen tube growth is also associated with the pistil, which provides vital materials and energy for growth (Wang et al., 2023c). A significant restriction of early pollen tubes in the transmitting tracts (TTs) was observed within 2 and 6 h of a heatwave after pollination in rice and maize, respectively (Zhang et al., 2018; Wang et al., 2023c) and was associated with ROS accumulation, disruption of phytohormone homeostasis, and reduced energy supply (Figure 4E). Heatwaves rapidly elevated the expression of Osrboh2 in pollinated pistils of rice and significantly increased ROS content (Figure 4F; Zhang et al., 2018). Elevated ROS levels can increase peroxidase (POD) contents by enhancing the expression of POX, which disrupts energy homeostasis and limits pollen tube growth by degrading auxin (Selinski and Scheibe, 2014; Zhang et al., 2018). In post-pollination silk of maize exposed to a heatwave, downregulation of HAIRPIN-INDUCED 3, a homolog of rice BOTRYOID POLLEN 1 encoding a uridine diphosphate (UDP)-glucose epimerase that regulates UDP-sugar homeostasis, and upregulation of METALLOTHIONEIN 8 and METALLOTHIONEIN 9, together lead to ROS accumulation and PCD (Chen et al., 2023; Gong et al., 2024). Sugar starvation induced by postpollination heatwaves was observed during pollen tube growth in rice and maize (Li et al., 2015a; Wang et al., 2023c). Heatwaves significantly increased sucrose accumulation in the style but reduced hexose levels, greatly limiting sucrose utilization and energy supply (Wang et al., 2023c). In addition, heatwaves reduce the stylar expression of arabinogalactan protein (AGP) genes, which are vital for pollen tube guidance and cellular integrity (Cheung and Wu, 1999; Mareri et al., 2016; Lohani et al., 2020). Understanding how heatwaves affect the interactions between pollen tubes and pistils in different crops remains a significant challenge.

Concluding remarks and future perspectives

In a warming climate, heat stress effects on agriculture have received more attention in recent years, but with limited focus on transient heatwaves due to underestimation of their effects on crop yield loss. The most heat-sensitive growth stages at different timescales from hours to days have been accurately determined for many crops on the basis of numerous temperature-controlled experiments (Lv et al., 2024). Avoiding overlap between heatwaves and these sensitive stages, as well as specifically increasing heat tolerance at these stages, is thus an important strategy. However, it is becoming extremely difficult to completely avoid such overlap by adjusting sowing dates or altering crop phenology, especially in multi-cropping regions, owing to increased heat stress. Even in a single day during the hot season, the duration and severity of heat stress have increased in the past few decades, and the need to enhance crop heat tolerance has become more urgent. Studies of heat stress effects on crop fertility should be more precise. Current studies are mainly directed at two broad aspects of heat stress: its ecology and its molecular basis. The former focuses on global warming and crop penalties, whereas the latter mainly deals with gene identification and function, leaving a knowledge gap in crop physiology. To date, the critical organs and their detailed roles in coping with transient heatwaves have not been completely clarified in many crops. Many studies have focused on pollen development and flowering pattern, leading to the identification of some heat-tolerance genes. These candidate genes, identified at heat-sensitive stages, have great potential for use in the improvement of crop heat tolerance. However, heat-tolerance genes related to more detailed aspects of flowering, such as floret opening angle or peak flowering time in a single day, remain to be characterized. Deficiencies in the phenomics of specific reproductive organs such as the floret and its components contribute to difficulties in precisely identifying key heat-tolerance genes. Most candidate genes have been identified from transcriptomic data and have not yet been subjected to mutant-based functional validation. Nevertheless, consistent alteration of the same metabolic pathways (e.g., sugar and ROS metabolism) in response to heatwaves at different heat-sensitive stages suggests that it is feasible to breed integrated heat-tolerant crop varieties. Compared with heat tolerance, heat escape may be a more feasible approach to reducing heat effects on crop fertility. For example, the early-morning flowering trait can enhance rice floret fertility under heat-stress conditions in the field (Ishimaru et al., 2022). Some critical genes that regulate this trait have been identified in rice, showing great potential for use in breeding of heat-tolerant cultivars. However, this trait has not been closely examined in other crops. In practice, artificial pollination facilitated by drones flying over crops early in the morning can also increase crop yield under heat stress, and this approach can be considered before crop cultivars with the early-morning flowering trait are released.

Funding

This work was supported by grants from the 10.13039/501100012166 National Key R&D Program of China (2023YFD2303304 ), the National Science Foundation of China (32272214 ), the 2115 Talent Development Program of China Agricultural University, the Chinese Universities Scientific Fund (2024TC062 ), and the Pinduoduo-China Agricultural University Research Fund (PC2023B02006 ).

Author contributions

Q.Y., P.L., and S.H. planned and designed the study. Q.Y. and P.L. created the graphs and wrote the manuscript. X.W. and S.H. assisted in materials visualization. P.W., X.W., S.L., and S.H. assisted in the revision of the manuscript.

Acknowledgments

We thank the team of physiology and cultivation for maize of the College of Agronomy and Biotechnology, China Agricultural University, for excellent advice, and we thank Mayang Liu and Xuanlong Lv for their critical reading of this review.

Published by the Plant Communications Shanghai Editorial Office in association with Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and CEMPS, CAS.
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