Large-scale analyses of heat shock transcription factors and database construction based on whole-genome genes in horticultural and representative plants

Abstract

Heat shock transcription factor (Hsf) plays a critical role in regulating heat resistance. Here, 2950 Hsf family genes were identified from 111 horticultural and representative plants. More Hsf genes were detected in higher plants than in lower plants. Based on all Hsf genes, we constructed a phylogenetic tree, which indicated that Hsf genes of each branch evolved independently after species differentiation. Furthermore, we uncovered the evolutionary trajectories of Hsf genes by motif analysis. There were only six motifs (M1–M6) in lower plants, and then four novel motifs (M7–M10) appeared in higher plants. However, the motifs of some Hsf genes were lost in higher plants, indicating that Hsf genes have undergone sequence variation during their evolution. The number of Hsf genes lost was greater than the number of genes that were duplicated after whole-genome duplication in higher plants. The heat response network was constructed using 24 Hsf genes and 2421 downstream and 222 upstream genes of Arabidopsis. Further enrichment analysis revealed that Hsf genes and other transcription factors interacted with each other in the response to heat stress. Global expression maps were illustrated for Hsf genes under various abiotic and biotic stresses and several developmental stages in Arabidopsis. Syntenic and phylogenetic analyses were conducted using Hsf genes of Arabidopsis and the pan-genome of 18 Brassica rapa accessions. We also performed expression pattern analysis of Hsf and six Hsp family genes using expression values from different tissues and heat treatments in B. rapa. The interaction network between the Hsf and Hsp gene families was constructed in B. rapa, and several core genes were detected in the network. Finally, we constructed an Hsf database (http://hsfdb.bio2db.com) for researchers to retrieve Hsf gene family information. Therefore, our study will provide rich resources for the study of the evolution and function of Hsf genes.

References

[1] Cramer GR, Urano K, Delrot S et al. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 2011; 11: 163.

[2] Zhu JK . Abiotic stress signaling and responses in plants. Cell. 2016; 167: 313-24.

[3] He M, He CQ, Ding NZ . Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front Plant Sci. 2018; 9: 1771.

[4] Zhou T, Jia X, Liao H et al. Effects of elevated mean and extremely high temperatures on the physio-ecological characteristics of geographically distinctive populations of Cunninghamia lanceolata . Sci Rep. 2016; 6: 39187.

[5] Hu S, Ding Y, Zhu C . Sensitivity and responses of chloroplasts to heat stress in plants. Front Plant Sci. 2020; 11: 375.

[6] Mathur S, Agrawal D, Jajoo A . Photosynthesis: response to high temperature stress. J Photochem Photobiol B. 2014; 137: 116-26.

[7] Hatfield JL, Prueger JH . Temperature extremes: effect on plant growth and development. Weather Clim Extrem. 2015; 10: 4-10.

[8] Bita CE, Gerats T . Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013; 4: 273.

[9] Guo J, Wu J, Ji Q et al. Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis . J Genet Genomics. 2008; 35: 105-18.

[10] Li M, Jannasch AH, Jiang Y . Growth and hormone alterations in response to heat stress in perennial ryegrass accessions differing in heat tolerance. J Plant Growth Regul. 2020; 39: 1022-9.

[11] Zhou M, Zheng S, Liu R et al. Genome-wide identification, phylogenetic and expression analysis of the heat shock transcription factor family in bread wheat (Triticum aestivum L.) . BMC Genomics. 2019; 20: 505.

[12] Gomez-Pastor R, Burchfiel ET, Thiele DJ . Regulation of heat shock transcription factors and their roles in physiology and disease. Nat Rev Mol Cell Biol. 2018; 19: 4-19.

[13] Kant P, Kant S, Gordon M et al. STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol. 2007; 145: 814-30.

[14] Ohama N, Kusakabe K, Mizoi J et al. The transcriptional cascade in the heat stress response of Arabidopsis is strictly regulated at the level of transcription factor expression. Plant Cell. 2016; 28: 181-201.

[15] Panchuk II, Volkov RA, Schöffl F . Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis . Plant Physiol. 2002; 129: 838-53.

[16] Guo M, Liu J-H, Ma X et al. The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci. 2016; 7: 114.

[17] Song X, Liu G, Duan W et al. Genome-wide identification, classification and expression analysis of the heat shock transcription factor family in Chinese cabbage. Mol Gen Genomics. 2014; 289: 541-51.

[18] Scharf KD, Berberich T, Ebersberger I et al. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta. 2012; 1819: 104-19.

[19] Li W, Wan XL, Yu JY et al. Genome-wide identification, classification, and expression analysis of the Hsf gene family in carnation (Dianthus caryophyllus) . Int J Mol Sci. 2019; 20: 5233.

[20] Sorger PK, Pelham HRB . Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988; 54: 855-64.

[21] Yang X, Zhu W, Zhang H et al. Heat shock factors in tomatoes: genome-wide identification, phylogenetic analysis and expression profiling under development and heat stress. PeerJ. 2016; 4: e1961.

[22] Lohani N, Golicz AA, Singh MB et al. Genome-wide analysis of the Hsf gene family in Brassica oleracea and a comparative analysis of the Hsf gene family in B. oleracea, B. rapa and B. napus . Funct Integr Genomics. 2019; 19: 515-31.

[23] Huang XY, Tao P, Li BY et al. Genome-wide identification, classification, and analysis of heat shock transcription factor family in Chinese cabbage (Brassica rapa pekinensis) . Genet Mol Res. 2015; 14: 2189-204.

[24] Li M, Xie F, Li Y et al. Genome-wide analysis of the heat shock transcription factor gene family in Brassica juncea: structure, evolution, and expression profiles. DNA Cell Biol. 2020; 39: 1990-2004.

[25] Zhu X, Huang C, Zhang L et al. Systematic analysis of Hsf family genes in the Brassica napus genome reveals novel responses to heat, drought and high CO2 stresses. Front Plant Sci. 2017; 8: 1174.

[26] Pei Q, Yu T, Wu T et al. Comprehensive identification and analyses of the Hsf gene family in the whole-genome of three Apiaceae species. Hortic Plant J. 2020; 7: 468-57.

[27] Guo M, Lu J-P, Zhai Y-F et al. Genome-wide analysis, expression profile of heat shock factor gene family (CaHsfs) and characterisation of CaHsfA2 in pepper (Capsicum annuum L.) . BMC Plant Biol. 2015; 15: 151.

[28] Zafar S, Hussain M, Raza M et al. Genome wide analysis of heat shock transcription factor (HSF) family in chickpea and its comparison with Arabidopsis . Plant Omics. 2016; 9: 136-41.

[29] Yu XY, Yao Y, Hong YH et al. Differential expression of the Hsf family in cassava under biotic and abiotic stresses. Genome. 2019; 62: 563-9.

[30] Liu G, Chai F, Wang Y et al. Genome-wide identification and classification of HSF family in grape, and their transcriptional analysis under heat acclimation and heat stress. Hortic Plant J. 2018; 4: 133-43.

[31] Wan X, Yang J, Guo C et al. Genome-wide identification and classification of the Hsf and sHsp gene families in Prunus mume, and transcriptional analysis under heat stress. PeerJ. 2019; 7: e7312.

[32] Dossa K, Diouf D, Cissé N . Genome-wide investigation of Hsf genes in sesame reveals their segmental duplication expansion and their active role in drought stress response. Front Plant Sci. 2016; 7: 1522.

[33] Li PS, Yu TF, He GH et al. Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement in drought and heat stresses. BMC Genomics. 2014; 15: 1009.

[34] Liu M, Huang Q, Sun W et al. Genome-wide investigation of the heat shock transcription factor (Hsf) gene family in Tartary buckwheat (Fagopyrum tataricum) . BMC Genomics. 2019; 20: 871.

[35] Zhang H, Li G, Fu C et al. Genome-wide identification, transcriptome analysis and alternative splicing events of Hsf family genes in maize. Sci Rep. 2020; 10: 8073.

[36] Ye J, Yang X, Hu G et al. Genome-wide investigation of heat shock transcription factor family in wheat (Triticum aestivum L.) and possible roles in anther development . Int J Mol Sci. 2020; 21: 608.

[37] Jin J, Tian F, Yang DC et al. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017; 45: D1040-5.

[38] Ratheesh KR, Nagarajan NS, Arunraj SP et al. HSPIR: a manually annotated heat shock protein information resource. Bioinformatics. 2012; 28: 2853-5.

[39] Song X-M, Wang J-P, Sun P-C et al. Preferential gene retention increases the robustness of cold regulation in Brassicaceae and other plants after polyploidization. Hortic Res. 2020; 7: 1-15.

[40] Song X, Ma X, Li C et al. Comprehensive analyses of the BES1 gene family in Brassica napus and examination of their evolutionary pattern in representative species. BMC Genomics. 2018; 19: 346.

[41] Song X, Wang J, Ma X et al. Origination, expansion, evolutionary trajectory, and expression bias of AP2/ERF superfamily in Brassica napus . Front Plant Sci. 2016; 7: 1186.

[42] Jacob P, Hirt H, Bendahmane A . The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J. 2017; 15: 405-14.

[43] Ohama N, Sato H, Shinozaki K et al. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 2017; 22: 53-65.

[44] Shan Q, Ma F, Wei J et al. Physiological functions of heat shock proteins. Curr Protein Pept Sci. 2020; 21: 751-60.

[45] Ul Haq S, Khan A, Ali M et al. Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int J Mol Sci. 2019; 20: 5321.

[46] Sankoff D, Zheng C . Whole genome duplication in plants: implications for evolutionary analysis. Methods Mol Biol. 2018; 1704: 291-315.

[47] Godfree RC, Marshall DJ, Young AG et al. Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress. R Soc Open Sci 2017; 4: 170934.

[48] Song X, Nie F, Chen W et al. Coriander genomics database: a genomic, transcriptomic, and metabolic database for coriander. Hortic Res. 2020; 7: 55.

[49] Yang J, Liu D, Wang X et al. The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet. 2016; 48: 1225-32.

[50] Wang X, Wang H, Wang J et al. The genome of the mesopolyploid crop species Brassica rapa . Nat Genet. 2011; 43: 1035-9.

[51] Song X, Yang Q, Bai Y et al. Comprehensive analysis of SSRs and database construction using all complete gene-coding sequences in major horticultural and representative plants. Hortic Res. 2021; 8: 122.

[52] On D, Ej M . Transgenosis of Arabidopsis thaliana for understanding plant gene structure and functions. Biologia. 2001; 56: 1-5.

[53] Cai X, Chang L, Zhang T et al. Impacts of allopolyploidization and structural variation on intraspecific diversification in Brassica rapa . Genome Biol. 2021; 22: 166.

[54] Song X, Hu J, Wu T et al. Comparative analysis of long noncoding RNAs in angiosperms and characterization of long noncoding RNAs in response to heat stress in Chinese cabbage. Hortic Res. 2021; 8: 48.

[55] Cheng F, Mandakova T, Wu J et al. Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa . Plant Cell. 2013; 25: 1541-54.

[56] van Dijk EL, Jaszczyszyn Y, Naquin D et al. The third revolution in sequencing technology. Trends Genet. 2018; 34: 666-81.

[57] Kumar KR, Cowley MJ, Davis RL . Next-generation sequencing and emerging technologies. Semin Thromb Hemost. 2019; 45: 661-73.

[58] Naish M, Alonge M, Wlodzimierz P et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science. 2021; 374: eabi7489.

[59] Miga KH, Koren S, Rhie A et al. Telomere-to-telomere assembly of a complete human X chromosome. Nature. 2020; 585: 79-84.

[60] Cheng F, Liu S, Wu J et al. BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol. 2011; 11: 136.

[61] Letunic I, Bork P . Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019; 47: W256-9.

[62] Mistry J, Chuguransky S, Williams L et al. Pfam: the protein families database in 2021. Nucleic Acids Res. 2021; 49: D412-9.

[63] Letunic I, Doerks T, Bork P . SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 2012; 40: D302-5.

[64] Marchler-Bauer A, Anderson JB, Chitsaz F et al. CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res. 2009; 37: D205-10.

[65] Zimmermann L, Stephens A, Nam SZ et al. A completely re-implemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol. 2018; 430: 2237-43.

[66] Nakamura T, Yamada KD, Tomii K et al. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics. 2018; 34: 2490-2.

[67] Price MN, Dehal PS, Arkin AP . FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009; 26: 1641-50.

[68] Bailey TL, Boden M, Buske FA et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009; 37: W202-8.

[69] Stolzer M, Lai H, Xu M et al. Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees. Bioinformatics. 2012; 28: i409-15.

[70] Wang Y, Tang H, Debarry JD et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40: e49.

[71] De Clercq I, Van de Velde J, Luo X et al. Integrative inference of transcriptional networks in Arabidopsis yields novel ROS signalling regulators. Nat Plants. 2021; 7: 500-13.

[72] Jacomy M, Venturini T, Heymann S et al. ForceAtlas2, a continuous graph layout algorithm for handy network visualization designed for the Gephi software. PLoS One. 2014; 9: e98679.

[73] El-Gebali S, Mistry J, Bateman A et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019; 47: D427-32.

[74] Virtanen P, Gommers R, Oliphant TE et al. SciPy 1.0: fundamental algorithms for scientific computing in python. Nat Methods. 2020; 17: 261-72.

[75] Chen C, Chen H, Zhang Y et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13: 1194-202.

[76] Winter D, Vinegar B, Nahal H et al. An "electronic fluorescent pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One. 2007; 2: e718.

[77] Tong C, Wang X, Yu J et al. Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa . BMC Genomics. 2013; 14: 689.

[78] Trapnell C, Williams BA, Pertea G et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010; 28: 511-5.

[79] Mistry J, Finn RD, Eddy SR et al. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 2013; 41: e121.

[80] Song X, Liu G, Huang Z et al. Temperature expression patterns of genes and their coexpression with LncRNAs revealed by RNA-Seq in non-heading Chinese cabbage. BMC Genomics. 2016; 17: 297.

[81] Song XM, Liu TK, Duan WK et al. Genome-wide analysis of the GRAS gene family in Chinese cabbage (Brassica rapa ssp. pekinensis) . Genomics. 2014; 103: 135-46.

[82] Lescot M, Dehais P, Thijs G et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002; 30: 325-7.

[83] Xue GP, Drenth J, McIntyre CL . TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets . J Exp Bot. 2015; 66: 1025-39.

[84] Xue GP, Sadat S, Drenth J et al. The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes. J Exp Bot. 2014; 65: 539-57.

[85] Nover L, Bharti K, Doring P et al. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones. 2001; 6: 177-89.

[86] Cheng F, Wu J, Fang L et al. Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa . PLoS One. 2012; 7: e36442.

[87] Bostock M, Ogievetsky V, Heer J . D³: data-driven documents . IEEE Trans Vis Comput Graph. 2011; 17: 2301-9.