Abstract
Wheat (Triticum aestivum), one of the world’s most important crops, is facing unprecedented challenges due to global warming. To evaluate the gene resources for heat adaptation in hexaploid wheat, small heat shock proteins (sHSPs), the key plant heat protection genes, were comprehensively analysed in wheat and related species. We found that the sHSPs of hexaploid wheat were massively expanded in A and B subgenomes with intrachromosomal duplications during polyploidization. These expanded sHSPs were under similar purifying selection and kept the expressional patterns with the original copies. Generally, a strong purifying selection acted on the α-crystallin domain (ACD) and theoretically constrain conserved function. Meanwhile, weaker purifying selection and strong positive selection acted on the N-terminal region, which conferred sHSP flexibility, allowing adjustments to a wider range of substrates in response to genomic and environmental changes. Notably, in CI, CV, ER, MI and MII subfamilies, gene duplications, expression variations and functional divergence occurred before wheat polyploidization. Our results indicate the massive expansion of active sHSPs in hexaploid wheat may also provide more raw materials for evolving functional novelties and generating genetic diversity to face future global climate changes, and highlight the expansion of stress response genes with wheat polyploidization.
Highlights
Diverse heat shock proteins (HSPs), one key component of cellular protein quality control network, are very important for plant heat stress adaptation[1,2,3]
SHSP expansion in the CI subfamily occurred in chromosomes 4AS, 3AS, 1AL (Fig. 3b), 4BL and 3B (Fig. 3c), and the Small heat shock proteins (sHSPs) of the MI subfamily mainly located in chromosome 7BS (Fig. 3d). These results suggest that sHSP expansion in hexaploid wheat originated from intrachromosomal duplications, which is consistent with the segmental duplications of sHSPs observed in A. thaliana, rice and soybean[22, 23, 45], and exhibit a notably higher intrachromosomal duplication ratio during wheat polyploidization[31, 41]
The sHSPs of the CI, CV, CIX, ER, MI and MII subfamilies could be divided into two groups in the polygenetic tree, and these two groups were likely paralogs originating from gene duplications (Supplementary Fig. S4). These duplicated sHSPs showed obvious species preferences; for example, the groups CIb and ERb were only present in monocots, whereas the groups CIXb, MIb and MIIb were unique to Triticeae. These results indicated that the original duplications, which led to the different groups of sHSPs, were ancient events that mostly related to speciation, rather than to the wheat polyploidizaion
Summary
Diverse heat shock proteins (HSPs), one key component of cellular protein quality control network, are very important for plant heat stress adaptation[1,2,3]. The autopolyploid which resulted from whole genome duplication or unreduced gametes fusion within a single species, and the allopolyploidy which resulted from interspecific hybridisation, generate extra gene copies[33, 34] These duplicated genes underwent subfunctionalization, neofunctionalization, specialization, pseudogenization or concerted evolution, leading to greater genetic diversity[34,35,36], which is the key factor in adaptation to new habitats and distribution to larger geographical areas than those covered by their progenitors[28, 34]. As the key heat protection genes, twenty-seven candidate sHSPs have been identified in hexaploid wheat, with all found to localise to the mitochondria (26) or nucleus (1)[37]. We demonstrate the evolutionary pattern and mechanism of sHSPs in Triticeae and provide evidence for massive intrachromosomal gene duplications, selection pressure variations and the expression pattern diversity during wheat polyploidization. Our results provide fundamental evidence that will be valuable for further wheat sHSP applications as well as for its evolutionary pattern variations with polyploidization
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