A genome-wide analysis of the small auxin-up RNA (SAUR) gene family in cotton

BackgroundSmall auxin-up RNA (SAUR) gene family is the largest family of early auxin response genes in higher plants, which have been implicated in the regulation of multiple biological processes. However, no comprehensive analysis of SAUR genes has been reported in cotton (Gossypium spp.).ResultsIn the study, we identified 145, 97, 214, and 176 SAUR homologous genes in the sequenced genomes of G. raimondii, G. arboreum, G. hirsutum, and G. barbadense, respectively. A phylogenetic analysis revealed that the SAUR genes can be classified into 10 groups. A further analysis of chromosomal locations and gene duplications showed that tandem duplication and segmental duplication events contributed to the expansion of the SAUR gene family in cotton. An exon-intron organization and motif analysis revealed the conservation of SAUR-specific domains, and the auxin responsive elements existed in most of the upstream sequences. The expression levels of 16 GhSAUR genes in response to an exogenous application of IAA were determined by a quantitative RT-PCR analysis. The genome-wide RNA-seq data and qRT-PCR analysis of selected SAUR genes in developing fibers revealed their differential expressions. The physical mapping showed that 20 SAUR genes were co-localized with fiber length quantitative trait locus (QTL) hotspots. Single nucleotide polymorphisms (SNPs) were detected for 12 of these 20 genes between G. hirsutum and G. barbadense, but no SNPs were identified between two backcross inbred lines with differing fiber lengths derived from a cross between the two cultivated tetraploids.ConclusionsThis study provides an important piece of genomic information for the SAUR genes in cotton and lays a solid foundation for elucidating the functions of SAUR genes in auxin signaling pathways to regulate cotton growth.

[1]  Mukesh Jain,et al.  Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). , 2006, Genomics.

[2]  Jiwen Yu,et al.  A genome-wide analysis of the lysophosphatidate acyltransferase (LPAAT) gene family in cotton: organization, expression, sequence variation, and association with seed oil content and fiber quality , 2017, BMC Genomics.

[3]  Yoshihiro Ugawa,et al.  Plant cis-acting regulatory DNA elements (PLACE) database: 1999 , 1999, Nucleic Acids Res..

[4]  Xianbi Li,et al.  Spatiotemporal manipulation of auxin biosynthesis in cotton ovule epidermal cells enhances fiber yield and quality , 2011, Nature Biotechnology.

[5]  Tong Zhu,et al.  SAUR39, a Small Auxin-Up RNA Gene, Acts as a Negative Regulator of Auxin Synthesis and Transport in Rice1[W] , 2009, Plant Physiology.

[6]  Vai S. Lor,et al.  Constitutive Expression of Arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in Tomato Confers Auxin-Independent Hypocotyl Elongation1[OPEN] , 2016, Plant Physiology.

[7]  Shoupu He,et al.  MicroRNA and mRNA expression profiling analysis revealed the regulation of plant height in Gossypium hirsutum , 2015, BMC Genomics.

[8]  Wenying Xu,et al.  Genome-Wide Gene Expression Profiling Reveals Conserved and Novel Molecular Functions of the Stigma in Rice1[W] , 2007, Plant Physiology.

[9]  Ping Zheng,et al.  CottonGen: a genomics, genetics and breeding database for cotton research , 2013, Nucleic Acids Res..

[10]  John Z. Yu,et al.  The draft genome of a diploid cotton Gossypium raimondii , 2012, Nature Genetics.

[11]  Identification of small auxin-up RNA (SAUR) genes in Urticales plants: mulberry (Morus notabilis), hemp (Cannabis sativa) and ramie (Boehmeria nivea) , 2016, Journal of Genetics.

[12]  S. Chen,et al.  Three SAUR proteins SAUR76, SAUR77 and SAUR78 promote plant growth in Arabidopsis , 2015, Scientific Reports.

[13]  P. Oeller,et al.  Early auxin-induced genes encode short-lived nuclear proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Xun Xu,et al.  Genome sequence of the cultivated cotton Gossypium arboreum , 2014, Nature Genetics.

[15]  C. Fankhauser,et al.  Auxin-mediated plant architectural changes in response to shade and high temperature. , 2014, Physiologia plantarum.

[16]  He Zhang,et al.  Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution , 2015, Nature Biotechnology.

[17]  M. Sussman,et al.  SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in Arabidopsis[C][W] , 2014, Plant Cell.

[18]  Jiwen Yu,et al.  Identification of candidate genes for fiber length quantitative trait loci through RNA-Seq and linkage and physical mapping in cotton , 2017, BMC Genomics.

[19]  Jun Cao,et al.  Small auxin upregulated RNA (SAUR) gene family in maize: identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghum. , 2014, Journal of integrative plant biology.

[20]  Jian Wu,et al.  Genome-wide analysis of SAUR gene family in Solanaceae species. , 2012, Gene.

[21]  Shuxun Yu,et al.  Genome-wide characterization and comparative analysis of the MLO gene family in cotton. , 2016, Plant physiology and biochemistry : PPB.

[22]  Zhongxu Lin,et al.  A comparative meta-analysis of QTL between intraspecific Gossypium hirsutum and interspecific G. hirsutum × G. barbadense populations , 2015, Molecular Genetics and Genomics.

[23]  Caiping Cai,et al.  Genome-wide analysis of CrRLK1L gene family in Gossypium and identification of candidate CrRLK1L genes related to fiber development , 2016, Molecular Genetics and Genomics.

[24]  R. Voorrips MapChart: software for the graphical presentation of linkage maps and QTLs. , 2002, The Journal of heredity.

[25]  Caiping Cai,et al.  Genome-wide identification of mitogen-activated protein kinase gene family in Gossypium raimondii and the function of their corresponding orthologs in tetraploid cultivated cotton , 2014, BMC Plant Biology.

[26]  Hang He,et al.  Arabidopsis SAURs are critical for differential light regulation of the development of various organs , 2016, Proceedings of the National Academy of Sciences.

[27]  W. Gray,et al.  SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth. , 2015, Molecular plant.

[28]  S. Gan,et al.  SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis1[C][W][OA] , 2012, Plant Physiology.

[29]  G. Guinn,et al.  Changes in Abscisic Acid and Indoleacetic Acid before and after Anthesis Relative to Changes in Abscission Rates of Cotton Fruiting Forms. , 1988, Plant physiology.

[30]  J. Reed,et al.  Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. , 2012, The Plant journal : for cell and molecular biology.

[31]  Bo Hu,et al.  GSDS 2.0: an upgraded gene feature visualization server , 2014, Bioinform..

[32]  Jenn-Kang Hwang,et al.  Predicting subcellular localization of proteins for Gram‐negative bacteria by support vector machines based on n‐peptide compositions , 2004, Protein science : a publication of the Protein Society.

[33]  C. Beasley Hormonal Regulation of Growth in Unfertilized Cotton Ovules , 1973, Science.

[34]  Comprehensive analysis of SAUR gene family in citrus and its transcriptional correlation with fruitlet drop from abscission zone A , 2015, Functional & Integrative Genomics.

[35]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[36]  Ming Chen,et al.  Auxin-related gene families in abiotic stress response in Sorghum bicolor , 2010, Functional & Integrative Genomics.

[37]  Satoru Miyano,et al.  Open source clustering software , 2004 .

[38]  Yuxian Zhu,et al.  How cotton fibers elongate: a tale of linear cell-growth mode. , 2011, Current opinion in plant biology.

[39]  Jiwen Yu,et al.  Mapping quantitative trait loci for lint yield and fiber quality across environments in a Gossypium hirsutum × Gossypium barbadense backcross inbred line population , 2012, Theoretical and Applied Genetics.

[40]  Vassilios Ioannidis,et al.  ExPASy: SIB bioinformatics resource portal , 2012, Nucleic Acids Res..

[41]  M. Ohme-Takagi,et al.  DST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco. , 1993, The Plant cell.

[42]  Adi Doron-Faigenboim,et al.  Ecology, Evolution and Organismal Biology Publications Ecology, Evolution and Organismal Biology Repeated Polyploidization of Gossypium Genomes and the Evolution of Spinnable Cotton Fibres , 2022 .

[43]  Caiping Cai,et al.  Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites , 2015, Scientific Reports.

[44]  Y. Ruan,et al.  The genome sequence of Sea-Island cotton (Gossypium barbadense) provides insights into the allopolyploidization and development of superior spinnable fibres , 2015, Scientific Reports.

[45]  G. Hagen,et al.  Auxin-responsive gene expression: genes, promoters and regulatory factors , 2002, Plant Molecular Biology.

[46]  Wenxue Ye,et al.  miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development , 2014, Nature Communications.

[47]  Junhui Wang,et al.  The tissue-specific and developmentally regulated expression patterns of the SAUR41 subfamily of SMALL AUXIN UP RNA genes , 2013, Plant signaling & behavior.

[48]  Lei Fang,et al.  Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement , 2015, Nature Biotechnology.

[49]  Xiyan Yang,et al.  Transcript profiling reveals complex auxin signalling pathway and transcription regulation involved in dedifferentiation and redifferentiation during somatic embryogenesis in cotton , 2012, BMC Plant Biology.

[50]  T. Guilfoyle,et al.  Characterization of a class of small auxin-inducible soybean polyadenylated RNAs , 1987, Plant Molecular Biology.

[51]  D. Inzé,et al.  The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. , 2012, The Plant journal : for cell and molecular biology.

[52]  S. Eddy,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..