Heat Stress Responses and Thermotolerance in Maize

Abstract

High temperatures causing heat stress disturb cellular homeostasis and impede growth and development in plants. Extensive agricultural losses are attributed to heat stress, often in combination with other stresses. Plants have evolved a variety of responses to heat stress to minimize damage and to protect themselves from further stress. A narrow temperature window separates growth from heat stress, and the range of temperatures conferring optimal growth often overlap with those producing heat stress. Heat stress induces a cytoplasmic heat stress response (HSR) in which heat shock transcription factors (HSFs) activate a constellation of genes encoding heat shock proteins (HSPs). Heat stress also induces the endoplasmic reticulum (ER)-localized unfolded protein response (UPR), which activates transcription factors that upregulate a different family of stress response genes. Heat stress also activates hormone responses and alternative RNA splicing, all of which may contribute to thermotolerance. Heat stress is often studied by subjecting plants to step increases in temperatures; however, more recent studies have demonstrated that heat shock responses occur under simulated field conditions in which temperatures are slowly ramped up to more moderate temperatures. Heat stress responses, assessed at a molecular level, could be used as traits for plant breeders to select for thermotolerance.

Keywords: heat stress; maize; post-transcriptional regulation; transcriptional regulation.

Figure 1

The relationship of temperature, growth, and heat stress in maize. (a) Optimal growth conditions overlap with heat stress. The optimal temperature range for maize growth is 25–33 °C, day/17–23 °C, night (https://www.extension.purdue.edu/extmedia/nch/nch-40.html), which are mid-summer temperatures in the US corn belt. The box indicates the average high temperatures (maximum daily temperatures) in June and July in Iowa, USA, a region representing an ideal climate for maize production. The trends shown here are from experiments conducted with the maize inbred line W22 grown under controlled environment conditions in the Enviratron at Iowa State University [14]. (b) An example of the temperature conditions used in the Enviratron to simulate diurnal temperature cycles under field conditions. Note the ramping up of the temperature to different maximum daily temperatures in the virtual afternoon and the ramping down in the virtual evening.

Figure 2

Two systems involved in heat stress responses in plants. Heat stress triggers protective mechanisms collectively called heat stress responses (HSRs). Both HSR in the cytoplasm and unfolded protein responses (UPR) in the endoplasmic reticulum (ER) mitigate the damage from heat stress and protect plants from further stress. The UPR and HSR occur in different cellular compartments, but both responses are elicited by misfolded proteins that accumulate in the ER and cytoplasm, respectively. The HSP and UPR genes in plants are upregulated by the activation of stress-transducing transcription factors, such as bZIP60 (basic leucine zipper 60) in the UPR and HSFs in the HSR. IRE1, a key factor in the UPR, is a dual protein kinase and ribonuclease involved in the splicing of bZIP60 mRNA. HSR, heat stress response; UPR, unfolded protein response; ER, endoplasmic reticulum; bZIP60, basic leucine zipper 60; HSP, heat shock protein; HSF, heat shock transcription factor; HSP70, heat shock protein 70; BIP, binding immunoglobulin protein; and IRE1, inositol-requiring enzyme 1.

Figure 3

Heat stress induction of the HSF genes in Arabidopsis and maize. (a) Heat stress induction of a transcriptional cascade involving HSFA genes in Arabidopsis. Modified from Nishizawa-Yokoi et al., 2011 [34] and Huang et al., 2016 [40]. (b) Comparison of HSF induction in response to step heat shock treatment (Lin et al., 2011 [29] and Zhang et al., 2020 [30]) vs. ramped heat stress conditions (simulated field conditions in which temperatures are slowly ramped up to maximum daily temperature), Li et al., 2020 [14]). Five of the 31 maize HSFs (light orange color indicated) were identified as induced under both the step heat shock treatment and ramped heat stress conditions in maize, including two A2 subgroup HSFs, two B2 HSFs, and one A6 subgroup HSF. One B1 subgroup HSF and two C1 subgroup HSFs (light orange) were specifically upregulated in response to ramped heat stress conditions, while one B1 HSF (blue) was downregulated under the same conditions. HSFA, class A heat shock transcription factor; HSFB, class B heat shock transcription factor; ABA, abscisic acid; HSP, heat shock protein; and HSF TF, heat shock transcription factor.

Figure 4

Phylogenetic relationship and domain analysis of Hsftf13. (a) Amino acid sequence alignment of the Hsftf13 subgroup genes in Arabidopsis and maize. In this clade, there is two subfamily HSF genes in Arabidopsis (HSFA2 and HSFA6,7). Two maize HSFs in subgroup HSFA2 and five HSFs in the HSFA6,7 subgroup, including Hsftf13. The evolutionary analysis was conducted in MEGA X (https://www.megasoftware.net) by using the maximum likelihood method and JTT (Jones-Taylor-Thornton) matrix-based model. The tree with the highest log likelihood is shown. (b) Amino acid sequence alignment and major domains in those HSFs. AHA motifs, activation domain, and characterized by short peptide motifs. The oligomerization domain HR-A/B is characterized by the heptad pattern of hydrophobic residues. NLS represents nuclear localization signal, and NES indicates nuclear export signal.

Figure 5

Moonlighting of cytosolic glyceraldehyde-3-phosphate dehydrogenase and the temperature-dependent alternative splicing of FLOWERING LOCUS M (FLM) in Arabidopsis. (a) Moonlighting of cytosolic glyceraldehyde-3-phosphate dehydrogenase (GAPC) (Based on Kim et al., 2020 [64]). The heat responses require GAPC and NF-YC10 interactions, and GAPC, which is normally located in the cytosol, enters the nucleus in response to heat. In the nucleus, GAPC binds to transcription factor NF-YC10 to increase the expression of heat-inducible genes, rendering Arabidopsis tolerant to heat stress. (b) Alternative splicing of FLM in response to the temperature. Modified from Capovilla et al., 2017 [74]. FLM has two splice variants, FLM-β and FLM-δ, in Arabidopsis, resulting from the temperature-dependent alternative splicing of FLM pre-mRNA via a mutually exclusive event (with Exon 2 or 3). The ratio of the two splicing isoforms, FLM-β/FLM-δ, fine-tunes the flowering time and is regulated by the ambient temperature.