Varying Architecture of Heat Shock Elements Contributes to Distinct Magnitudes of Target Gene Expression and Diverged Biological Pathways in Heat Stress Response of Bread Wheat.

Peng Zhao,Xue Shi,Xiaoming Wang,Bingjin Wu,Dongzhi Zhang,Sidra Javed,Shengbao Xu

doi:10.3389/fgene.2020.00030

Peng Zhao, Xue Shi + Show 5 more

Open Access

https://doi.org/10.3389/fgene.2020.00030

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Abstract

The heat shock transcription factor (HSF) binds to cis-regulatory motifs known as heat shock elements (HSEs) to mediate the transcriptional response of HSF target genes. However, the HSF–HSEs interaction is not clearly understood. Using the newly released genome reference sequence of bread wheat, we identified 39,478 HSEs (95.6% of which were non-canonical HSEs) and collapsed them into 30,604 wheat genes, accounting for 27.6% wheat genes. Using the intensively heat-responsive transcriptomes of wheat, we demonstrated that canonical HSEs have a higher propensity to induce a response in the closest downstream genes than non-canonical HSEs. However, the response magnitude induced by non-canonical HSEs was comparable to that induced by canonical HSEs. Significantly, some non-canonical HSEs that contain mismatched nucleotides at specific positions within HSEs had a larger response magnitude than that of canonical HSEs. Consistently, most of the HSEs identified in the promoter regions of heat shock proteins were non-canonical HSEs, suggesting an important role for these non-canonical HSEs. Lastly, distinct diverged biological processes were observed between genes containing different HSE types, suggesting that sequence variation in HSEs plays a key role in the evolution of heat responses and adaptation. Our results provide a new perspective to understand the regulatory network underlying heat responses.

Highlights

Wheat (Triticum aestivum L.), a globally important crop, contributes about a fifth of the total calories consumed by humans (IWGSC, 2018)
Combined with the previous result showing that Genes contained only one gapped HSEs (TGGs) had a lower propensity to induce an heat stress (HS) response of closest downstream genes (CDGs), we proposed that gapped heat shock elements (HSEs) tend to release from heat shock factors (HSF) regulation
We comprehensively identified the distribution of HSEs and illustrated, for the first time, that varying HSE architecture affects the HSF DNA binding affinity and the corresponding response magnitude of CDGs in plants, mediating different HS response processes

Summary

Introduction

Wheat (Triticum aestivum L.), a globally important crop, contributes about a fifth of the total calories consumed by humans (IWGSC, 2018). The identification of thermotolerant genes and the Evolution of Heat Shock Elements characterization of molecular mechanisms underlying HS responses and adaptations became urgent to improve wheat thermotolerance. Under HS, heat shock factors (HSF), which converge the heat signaling transduced from several pathways and are regarded as the terminal link in heat signaling, bind to each other to form polymers and activate the expression of HSPs by recognizing and binding to conserved DNA sequences, known as heat shock elements (HSEs), in the promoter region of HSPs (von KoskullDoring et al, 2007; Saidi et al, 2011; Bokszczanin et al, 2013; Vu et al, 2019). The factors that affect this stimulus and the corresponding activation efficiency are largely unknown

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