Abstract
Auxin response factors (ARFs) are recently discovered transcription factors that bind with auxin response elements (AuxRE, TGTCTC) to regulate the expression of early auxin-responsive genes. To our knowledge, the ARF gene family has never been characterized in cotton, the most important fiber crop in the world. In this study, a total of 35 ARF genes, named as GrARFs, were identified in a diploid cotton species Gossypium raimondii. The 35 ARF genes were located in 12 of the 13 cotton chromosomes; the intron/exon distribution of the GrARF genes was similar among sister pairs, whereas the divergence of some GrARF genes suggests the possibility of functional diversification. Our results show that the middle domains of nine GrARF proteins rich in glutamine (Q) are activators, while 26 other GrARF proteins rich in proline (P), serine (S), and threonine (T) are repressors. Our results also show that the expression of GrARF genes is diverse in different tissues. The expression of GrARF1 was significantly higher in leaves, whereas GrARF2a had higher expression level in shoots, which implicates different roles in the tested tissues. The GrARF11 has a higher expression level in buds than that in leaves, while GrARF19.2 shows contrasting expression patterns, having higher expression in leaves than that in buds. This suggests that they play different roles in leaves and buds. During long-term evolution of G. raimondii, some ARF genes were lost and some arose. The identification and characterization of the ARF genes in G. raimondii elucidate its important role in cotton that ARF genes regulate the development of flower buds, sepals, shoots, and leaves.
Similar content being viewed by others
References
Abel S, Ballas N, Wong LM, Theologis A (1996) DNA elements responsive to auxin. Bioessays 18:647–654. doi:10.1002/bies.950180808
Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17. doi:10.1104/Pp.111.1.9
Attia KA, Abdelkhalik AF, Ammar MH, Wei C, Yang J, Lightfoot DA, El-Sayed WM, El-Shemy HA (2009) Antisense phenotypes reveal a functional expression of OsARF1, an auxin response factor, in transgenic rice. Curr Issues Mol Biol 11(Suppl 1):i29–34
Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146:250–264. doi:10.1104/pp. 107.109538
Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308. doi:10.1016/j.tplants.2004.04.003
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195. doi:10.1371/journal.pcbi.1002195
Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574. doi:10.1242/dev.02012
Finet C, Berne-Dedieu A, Scutt CP, Marletaz F (2013) Evolution of the ARF gene family in land plants: old domains, new tricks. Mol Biol Evol 30:45–56. doi:10.1093/molbev/mss220
Fukaki H, Taniguchi N, Tasaka M (2006) PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J Cell Mol Biol 48:380–389. doi:10.1111/j.1365-313X.2006.02882.x
Goetz M, Vivian-Smith A, Johnson SD, Koltunow AM (2006) AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18:1873–1886. doi:10.1105/tpc.105.037192
Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262
Guilfoyle T, Hagen G, Ulmasov T, Murfett J (1998) How does auxin turn on genes? Plant Physiol 118:341–347
Guilfoyle TJ, Hagen G (2001) Auxin response factors. J Plant Growth Regul 20:281–291. doi:10.1007/s003440010026
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. doi:10.1016/j.pbi.2007.08.014
Ha CV, Le DT, Nishiyama R, Watanabe Y, Sulieman S, Tran UT, Mochida K, Dong NV, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) The auxin response factor transcription factor family in soybean: genome-wide identification and expression analyses during development and water stress. DNA Res Int J Rapid Publ Rep Genes Genomes 20:511–524. doi:10.1093/dnares/dst027
Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235. doi:10.1093/molbev/mst012
Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148:993–1003. doi:10.1104/pp. 108.122457
Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411. doi:10.1093/emboj/17.5.1405
Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770
Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162. doi:10.1111/j.1742-4658.2009.07033.x
Kepinski S, Leyser O (2005) Plant development: auxin in loops. Curr Biol CB 15:R208–210. doi:10.1016/j.cub.2005.03.012
Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genom MGG 285:245–260. doi:10.1007/s00438-011-0602-7
Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306. doi:10.1093/bib/bbn017
Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193–204. doi:10.1016/j.devcel.2004.07.002
Li J, Dai X, Zhao Y (2006) A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol 140:899–908. doi:10.1104/pp. 105.070987
Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 61:1419–1430. doi:10.1093/jxb/erq010
Lin L, Pierce GJ, Bowers JE, Estill JC, Compton RO, Rainville LK, Kim C, Lemke C, Rong J, Tang H, Wang X, Braidotti M, Chen AH, Chicola K, Collura K, Epps E, Golser W, Grover C, Ingles J, Karunakaran S, Kudrna D, Olive J, Tabassum N, Um E, Wissotski M, Yu Y, Zuccolo A, ur Rahman M, Peterson DG, Wing RA, Wendel JF, Paterson AH (2010) A draft physical map of a D-genome cotton species (Gossypium raimondii). BMC Genomics 11:395. doi:10.1186/1471-2164-11-395
Lin Y, Cheng Y, Jin J, Jin X, Jiang H, Yan H, Cheng B (2014) Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes. PLoS One 9:e102825. doi:10.1371/journal.pone.0102825
Ma J, Wang Q, Sun R, Xie F, Jones DC, Zhang B (2014) Genome-wide identification and expression analysis of TCP transcription factors in Gossypium raimondii. Sci Rep 4:6645. doi:10.1038/srep06645
Mun JH, Yu HJ, Shin JY, Oh M, Hwang HJ, Chung H (2012) Auxin response factor gene family in Brassica rapa: genomic organization, divergence, expression, and evolution. Mol Genet Genom MGG 287:765–784. doi:10.1007/s00438-012-0718-4
Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118. doi:10.1242/dev.01955
Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127:3877–3888
Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463. doi:10.1105/tpc.104.028316
Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen X, Triplett BA, Stelly DM, Chen ZJ (2009) Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol 10:R122. doi:10.1186/gb-2009-10-11-r122
Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910. doi:10.1105/tpc.105.034876
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–301. doi:10.1093/nar/gkr1065
Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193. doi:10.1016/S0076-6879(06)11009-5
Schmittgen TD, Lee EJ, Jiang J (2008) High-throughput real-time PCR. Methods Mol Biol 429:89–98. doi:10.1007/978-1-60327-040-3_7
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. doi:10.1038/nature08670
Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481–4491
Shao Y, Wei G, Wang L, Dong Q, Zhao Y, Chen B, Xiang Y (2011) Genome-wide analysis of BURP domain-containing genes in Populus trichocarpa. J Integr Plant Biol 53:743–755. doi:10.1111/j.1744-7909.2011.01068.x
Shen C, Wang S, Bai Y, Wu Y, Zhang S, Chen M, Guilfoyle TJ, Wu P, Qi Y (2010) Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.). J Exp Bot 61:3971–3981. doi:10.1093/jxb/erq208
Song Y, Wang L, Xiong L (2009) Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta 229:577–591. doi:10.1007/s00425-008-0853-7
Stowe-Evans EL, Harper RM, Motchoulski AV, Liscum E (1998) NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. Plant Physiol 118:1265–1275
Sun R, Wang Q, Ma J, He Q, Zhang B (2014) Differentiated expression of microRNAs may regulate genotype-dependent traits in cotton. Gene 547:233–238. doi:10.1016/j.gene.2014.06.052
Tian CE, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J Cell Mol Biol 40:333–343. doi:10.1111/j.1365-313X.2004.02220.x
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543
Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822
Ulmasov T, Hagen G, Guilfoyle TJ (1997a) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868
Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J Cell Mol Biol 19:309–319
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997b) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971. doi:10.1105/tpc.9.11.1963
Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24. doi:10.1016/j.gene.2007.01.006
Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005a) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216. doi:10.1105/tpc.105.033076
Wang K, Wang Z, Li F, Ye W, Wang J, Song G, Yue Z, Cong L, Shang H, Zhu S, Zou C, Li Q, Yuan Y, Lu C, Wei H, Gou C, Zheng Z, Yin Y, Zhang X, Liu K, Wang B, Song C, Shi N, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu S (2012a) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44:1098–1103. doi:10.1038/ng.2371
Wang S, Bai Y, Shen C, Wu Y, Zhang S, Jiang D, Guilfoyle TJ, Chen M, Qi Y (2010) Auxin-related gene families in abiotic stress response in Sorghum bicolor. Funct Integr Genomics 10:533–546. doi:10.1007/s10142-010-0174-3
Wang S, Tiwari SB, Hagen G, Guilfoyle TJ (2005b) AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17:1979–1993. doi:10.1105/tpc.105.031096
Wang Y, Deng D, Shi Y, Miao N, Bian Y, Yin Z (2012b) Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Mol Biol Rep 39:2401–2415. doi:10.1007/s11033-011-0991-z
Watahiki MK, Yamamoto KT (1997) The massugu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol 115:419–426
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735. doi:10.1093/aob/mci083
Wu J, Wang F, Cheng L, Kong F, Peng Z, Liu S, Yu X, Lu G (2011) Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Rep 30:2059–2073. doi:10.1007/s00299-011-1113-z
Xie FL, Jones DC, Wang QL, Sun RR, Zhang BH (2015) Small RNA sequencing identifies miRNA roles in ovule and fibre development. Plant Biotechnol J. doi:10.1111/pbi.12296
Xing H, Pudake RN, Guo G, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 12:178. doi:10.1186/1471-2164-12-178
Zhang B, Pan X (2009) Expression of microRNAs in cotton. Mol Biotechnol 42:269–274. doi:10.1007/s12033-009-9163-y
Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics MGG 271:402–415. doi:10.1007/s00438-004-0990-z
Acknowledgment
This project is partially support by grants from US NIFA (to BZ) and Cotton Incorporated (to BZ) and a grant from the National Natural Science Foundation of China (31170263 to QW).
Conflict of interest
The authors have declared that no competing interests exist.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary 1
DNA sequence of GrARF genes. (DOCX 74 kb)
Supplementary 2
Protein sequence of GrARF genes. (DOCX 24 kb)
Supplementary 3
Primers of GrARF genes. (XLS 22 kb)
Rights and permissions
About this article
Cite this article
Sun, R., Wang, K., Guo, T. et al. Genome-wide identification of auxin response factor (ARF) genes and its tissue-specific prominent expression in Gossypium raimondii . Funct Integr Genomics 15, 481–493 (2015). https://doi.org/10.1007/s10142-015-0437-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-015-0437-0