Integrated analysis of co-expression, conserved genes and gene families reveal core regulatory network of heat stress response in Cleistogenes songorica, a xerophyte perennial desert plant

Qi Yan,Xifang Zong,Fan Wu,Yanrong Wang,Tiantian Ma,Yufeng Zhao,Penglei Wang,Qian Ma,Jie Li,Jiyu Zhang

doi:10.1186/s12864-020-07122-8

Abstract

BackgroundAs global warming continues, heat stress (HS) is becoming an increasingly significant factor limiting plant growth and reproduction, especially for cool-season grass species. The objective of this study was to determine the transcriptional regulatory network of Cleistogenes songorica under HS via transcriptome profiling, identify of gene families and comparative analysis across major Poaceae species.ResultsPhysiological analysis revealed significantly decreased leaf relative water content (RWC) but increased proline (Pro) content in C. songorica under 24 h of HS. Transcriptome profiling indicated that 16,028 and 14,645 genes were differentially expressed in the shoots and roots of C. songorica under HS, respectively. Two subgenomes of C. songorica provide equal contribution under HS on the basis of the distribution and expression of differentially expressed genes (DEGs). Furthermore, 216 DEGs were identified as key evolutionarily conserved genes involved in the response to HS in C. songorica via comparative analysis with genes of four Poaceae species; these genes were involved in the ‘response to heat’ and ‘heat acclimation’. Notably, most of the conserved DEGs belonged to the heat-shock protein (HSP) superfamily. Similar results were also obtained from co-expression analysis. Interestingly, hub-genes of co-expression analysis were found to overlap with conserved genes, especially heat-shock protein (HSP). In C. songorica, 84 HSP and 32 heat-shock transcription factor (HSF) genes were identified in the allotetraploid C. songorica genome, and might have undergone purifying selection during evolutionary history based on syntenic and phylogenetic analysis. By analysing the expression patterns of the CsHSPs and CsHSFs, we found that the transcript abundance of 72.7% of the CsHSP genes and of 62.5% of the CsHSF genes changed under heat stress in both the shoots and roots. Finally, a core regulatory network of HS was constructed on the basis of the CsHSP, CsHSF and other responsive genes in C. songorica.ConclusionsRegulatory network and key genes were comprehensively analysed and identified in C. songorica under HS. This study improves our knowledge of thermotolerance mechanisms in native grasses, and also provides candidate genes for potential applications in the genetic improvement of grasses.

Highlights

As global warming continues, heat stress (HS) is becoming an increasingly significant factor limiting plant growth and reproduction, especially for cool-season grass species
Phenotype and physiology responses of C. songorica under HS To study the physiological changes caused by HS, nineweek-old seedlings of C. songorica were placed in three growth chamber with a 40 °C temperature during the day and night for 0 h, 6 h, 12 h, 24 h, 36 h, 48 h or 72 h
We suggested heat-shock protein (HSP) play a core role in regulatory networks of C. songorica under HS, and confirmed our analysis results were reliable to reflect the regulatory networks of C. songorica under HS

Summary

Introduction

Heat stress (HS) is becoming an increasingly significant factor limiting plant growth and reproduction, especially for cool-season grass species. The objective of this study was to determine the transcriptional regulatory network of Cleistogenes songorica under HS via transcriptome profiling, identify of gene families and comparative analysis across major Poaceae species. Increasing amounts of evidence suggested that stress tolerance genes of native grass could facilitate tolerance improvement of plant for drought, heat, salt stress. Overexpression of the heat-shock transcription factors 1 (HSFs) of resurrection plant Boea hygrometrica leads to increased thermotolerance and retarded growth in transgenic Arabidopsis and tobacco [10]. We confirmed that overexpression of functional genes form C. songorica improved tolerance to drought and salt in both alfalfa and Arabidopsis, such as CsLEA and CsALDH [6,7,8]. The transcriptional regulatory network and potential candidate genes involved in HS response of native plant is not well documented, especially those of grass species

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