Expansion and Stress Responses of the AP2/EREBP Superfamily in Cotton

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2017 Feb 2

PMID 28143399

Citations 38

Authors

Chunxiao Liu

Tianzhen Zhang

Affiliations

Soon will be listed here.

Abstract

Background: The allotetraploid cotton originated from one hybridization event between an extant progenitor of Gosssypium herbaceum (A) or G. arboreum (A) and another progenitor, G. raimondii Ulbrich (D) 1-1.5 million years ago (Mya). The APETALA2/ethylene-responsive element binding protein (AP2/EREBP) transcription factors constitute one of the largest and most conserved gene families in plants. They are characterized by their AP2 domain, which comprises 60-70 amino acids, and are classified into four main subfamilies: the APETALA2 (AP2), Related to ABI3/VP1 (RAV), Dehydration-Responsive Element Binding protein (DREB) and Ethylene-Responsive Factor (ERF) subfamilies. The AP2/EREBP genes play crucial roles in plant growth, development and biotic and abiotic stress responses. Hence, understanding the molecular characteristics of cotton stress tolerance and gene family expansion would undoubtedly facilitate cotton resistance breeding and evolution research.

Results: A total of 269 AP2/EREBP genes were identified in the G. raimondii (D5) cotton genome. The protein domain architecture and intron/exon structure are simple and relatively conserved within each subfamily. They are distributed throughout all chromosomes but are clustered on various chromosomes due to genomic tandem duplication. We identified 73 tandem duplicated genes and 221 segmental duplicated gene pairs which contributed to the expansion of AP2/EREBP superfamily. Of them, tandem duplication was the most important force of the expansion of the B3 group. Transcriptome analysis showed that 504 AP2/EREBP genes were expressed in at least one tested G. hirsutum TM-1 tissues. In G. hirsutum, 151 non-repeated genes of the DREB and ERF subfamily genes were responsive to different stresses: 132 genes were induced by cold, 63 genes by drought and 94 genes by heat. qRT-PCR confirmed that 13 GhDREB and 15 GhERF genes were induced by cold and/or drought. No transcripts detected for 53 of the 111 tandem duplicated genes in TM-1. In addition, some homoeologous genes showed biased expression toward either A-or D-subgenome.

Conclusions: The AP2/EREBP genes were obviously expanded in Gossypium. The GhDREB and GhERF genes play crucial roles in cotton stress responses. Our genome-wide analysis of AP2/EREBP genes in cotton provides valuable information for characterizing the molecular functions of AP2/EREBP genes and reveals insights into their evolution in polyploid plants.

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References

Riddle N, Birchler J . Effects of reunited diverged regulatory hierarchies in allopolyploids and species hybrids. Trends Genet. 2003; 19(11):597-600. DOI: 10.1016/j.tig.2003.09.005. View

Sohn K, Lee S, Jung H, Hong J, Hwang B . Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Mol Biol. 2006; 61(6):897-915. DOI: 10.1007/s11103-006-0057-0. View

Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B . Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol. 2010; 10:282. PMC: 3022907. DOI: 10.1186/1471-2229-10-282. View

Alonso J, Stepanova A, Leisse T, Kim C, Chen H, Shinn P . Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003; 301(5633):653-7. DOI: 10.1126/science.1086391. View

Hu Y, Jiang L, Wang F, Yu D . Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell. 2013; 25(8):2907-24. PMC: 3784588. DOI: 10.1105/tpc.113.112631. View

Chen L, Han J, Deng X, Tan S, Li L, Li L . Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon. Sci Rep. 2016; 6:21623. PMC: 4751504. DOI: 10.1038/srep21623. View

Zhang Y, Mao L, Wang H, Brocker C, Yin X, Vasiliou V . Genome-wide identification and analysis of grape aldehyde dehydrogenase (ALDH) gene superfamily. PLoS One. 2012; 7(2):e32153. PMC: 3280228. DOI: 10.1371/journal.pone.0032153. View

Park J, Park C, Lee S, Ham B, Shin R, Paek K . Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell. 2001; 13(5):1035-46. PMC: 135557. DOI: 10.1105/tpc.13.5.1035. View

Tang H, Wang X, Bowers J, Ming R, Alam M, Paterson A . Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 2008; 18(12):1944-54. PMC: 2593578. DOI: 10.1101/gr.080978.108. View

10.

Matias-Hernandez L, Aguilar-Jaramillo A, Marin-Gonzalez E, Suarez-Lopez P, Pelaz S . RAV genes: regulation of floral induction and beyond. Ann Bot. 2014; 114(7):1459-70. PMC: 4204781. DOI: 10.1093/aob/mcu069. View

11.

Licausi F, Giorgi F, Zenoni S, Osti F, Pezzotti M, Perata P . Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics. 2010; 11:719. PMC: 3022922. DOI: 10.1186/1471-2164-11-719. View

12.

Sharoni A, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T . Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol. 2010; 52(2):344-60. DOI: 10.1093/pcp/pcq196. View

13.

Feng J, Liu D, Pan Y, Gong W, Ma L, Luo J . An annotation update via cDNA sequence analysis and comprehensive profiling of developmental, hormonal or environmental responsiveness of the Arabidopsis AP2/EREBP transcription factor gene family. Plant Mol Biol. 2005; 59(6):853-68. DOI: 10.1007/s11103-005-1511-0. View

14.

Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D . Circos: an information aesthetic for comparative genomics. Genome Res. 2009; 19(9):1639-45. PMC: 2752132. DOI: 10.1101/gr.092759.109. View

15.

Cai X, Xu P, Zhao P, Liu R, Yu L, Xiang C . Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun. 2014; 5:5833. DOI: 10.1038/ncomms6833. View

16.

Xu Y, Wang J, Wang S, Wang J, Chen X . Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol. 2004; 135(1):507-15. PMC: 429402. DOI: 10.1104/pp.104.038612. View

17.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S . MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731-9. PMC: 3203626. DOI: 10.1093/molbev/msr121. View

18.

Sakuma Y, Liu Q, Dubouzet J, Abe H, Shinozaki K, Yamaguchi-Shinozaki K . DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun. 2002; 290(3):998-1009. DOI: 10.1006/bbrc.2001.6299. View

19.

Jiao Y, Wickett N, Ayyampalayam S, Chanderbali A, Landherr L, Ralph P . Ancestral polyploidy in seed plants and angiosperms. Nature. 2011; 473(7345):97-100. DOI: 10.1038/nature09916. View

20.

Shen Y, Zhang W, He S, Zhang J, Liu Q, Chen S . An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet. 2003; 106(5):923-30. DOI: 10.1007/s00122-002-1131-x. View