Abstract
Background
Auxin response factors (ARFs) are a class of transcription factors that regulate the expression of auxin-responsive genes and play important functions in plant growth and development. To understand the biological functions of the auxin response factor GhARF2 gene in upland cotton, the coding sequence (CDS) of GhARF2 gene was cloned, and its protein sequence, evolutionary relationship, subcellular localization and expression pattern were analysed.
Methods
The CDS sequence of GhARF2 gene was cloned from upland cotton variety Baimian No.1, and its protein sequence was analyzed by bioinformatics method. The subcellular localization of GhARF2 protein was detected by tobacco epidermal transient transformation system, and the tissue expression and stress expression pattern of GhARF2 were analyzed by quantitative Real‑Time PCR (qRT-PCR).
Results
The full-length CDS of GhARF2 gene was 2583 bp, encoded 860 amino acids, and had a molecular weight and an isoelectric point of 95.46 KDa and 6.02, respectively. The GhARF2 protein had multiple phosphorylation sites, no transmembrane domain, and secondary structures dominated by random coils and alpha helix. The GhARF2 protein had 3 conserved typical domains of ARF gene family members, including the B3 DNA binding domain, the Auxin_resp domain, and the Aux/IAA domain. Phylogenetic analysis revealed that ARF2 proteins in different species were clustered in the Group A subgroup, in which GhARF2 was closely related to TcARF2 of Theobroma cacao L. (Malvaceae). The subcellular localization results showed that the GhARF2 protein was localized in the nucleus. Analysis of tissue expression pattern showed that the GhARF2 gene was expressed in all tested tissues, with the highest expression levels in sepal, followed by leaf, and the lowest expression levels in fiber. Further stress expression analysis showed that the GhARF2 gene was induced by drought, high-temperature, low-temperature and salt stress, and had different expression patterns under different stress conditions.
Conclusion
These results established a foundation for understanding the functions of GhARF2 and breeding varieties with high-stress tolerance in cotton.
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References
Kou X, Zhao X, Wu B, Wang C, Wu C, Yang S, Zhou J, Xue Z (2022) Auxin response factors are ubiquitous in plant growth and development, and involved in crosstalk between plant hormones: a review. Appl Sci 12(3):1360. https://doi.org/10.3390/app12031360
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140(5):943–950. https://doi.org/10.1242/dev.086363
Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci 96(10):5844–5849. https://doi.org/10.1073/pnas.96.10.5844
Boer DR, Freire-Rios A, van den Berg WA, Saaki T, Manfield IW, Kepinski S, López-Vidrieo I, Franco-Zorrilla JM, de Vries SC, Solano R, Weijers D, Coll M (2014) Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156(3):577–589. https://doi.org/10.1016/j.cell.2013.12.027
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15(2):533–543. https://doi.org/10.1105/tpc.008417
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(2):444–463. https://doi.org/10.1105/tpc.104.028316
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(1–2):13–24. https://doi.org/10.1016/j.gene.2007.01.006
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. https://doi.org/10.1186/1471-2164-12-178
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 20(5):511–524. https://doi.org/10.1093/dnares/dst027
Qiao L, Zhang W, Li X, Zhang L, Zhang X, Li X, Guo H, Ren Y, Zheng J, Chang Z (2018) Characterization and expression patterns of auxin response factors in wheat. Front Plant Sci 9:1395. https://doi.org/10.3389/fpls.2018.01395
Song S, Hao L, Zhao P, Xu Y, Zhong N, Zhang H, Liu N (2019) Genome-wide identification, expression profiling and evolutionary analysis of auxin response factor gene family in potato (Solanum tuberosum Group Phureja). Sci Rep 9(1):1755. https://doi.org/10.1038/s41598-018-37923-7
Tang Y, Du G, Xiang J, Hu C, Li X, Wang W, Zhu H, Qiao L, Zhao C, Wang J, Yu S, Sui J (2022) Genome-wide identification of auxin response factor (ARF) gene family and the miR160-ARF18-mediated response to salt stress in peanut (Arachis hypogaea L.). Genomics 114(1):171–184. https://doi.org/10.1016/j.ygeno.2021.12.015
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 Genomics 287(10):765–784. https://doi.org/10.1007/s00438-012-0718-4
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(5):1419–1430. https://doi.org/10.1093/jxb/erq010
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(20):4563–4574. https://doi.org/10.1242/dev.02012
Paolo D, Orozco-Arroyo G, Rotasperti L, Masiero S, Colombo L, de Folter S, Ambrose BA, Caporali E, Ezquer I, Mizzotti C (2021) Genetic interaction of SEEDSTICK, GORDITA and AUXIN RESPONSE FACTOR 2 during seed development. Genes (Basel) 12(8):1189. https://doi.org/10.3390/genes12081189
Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133(2):251–261. https://doi.org/10.1242/dev.02194
Wang CK, Han PL, Zhao YW, Yu JQ, You CX, Hu DG, Hao YJ (2021) Genome-wide analysis of auxin response factor (ARF) genes and functional identification of MdARF2 reveals the involvement in the regulation of anthocyanin accumulation in apple. New Zeal J Crop Hort 49(2–3):78–91. https://doi.org/10.1080/01140671.2020.1779756
Hao Y, Hu G, Breitel D, Liu M, Mila I, Frasse P, Fu Y, Aharoni A, Bouzayen M, Zouine M (2015) Auxin response factor SlARF2 is an essential component of the regulatory mechanism controlling fruit ripening in tomato. PLoS Genet 11(12):e1005649. https://doi.org/10.1371/journal.pgen.1005649
Ren Z, Liu R, Gu W, Dong X (2017) The Solanum lycopersicum auxin response factor SlARF2 participates in regulating lateral root formation and flower organ senescence. Plant Sci 256:103–111. https://doi.org/10.1016/j.plantsci.2016.12.008
Kirolinko C, Hobecker K, Wen J, Mysore KS, Niebel A, Blanco FA, Zanetti ME (2021) Auxin response factor 2 (ARF2), ARF3, and ARF4 mediate both lateral root and nitrogen fixing nodule development in Medicago truncatula. Front Plant Sci 12:659061. https://doi.org/10.3389/fpls.2021.659061
Zhao S, Zhang ML, Ma TL, Wang Y (2016) Phosphorylation of ARF2 relieves its repression of transcription of the K+ transporter gene HAK5 in response to low potassium stress. Plant Cell 28(12):3005–3019. https://doi.org/10.1105/tpc.16.00684
Meng LS, Wang ZB, Yao SQ, Liu A (2015) The ARF2-ANT-COR15A gene cascade regulates ABA-signaling-mediated resistance of large seeds to drought in Arabidopsis. J Cell Sci 128(21):3922–3932. https://doi.org/10.1242/jcs.171207
Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, Grosdidier A, Hernandez C, Ioannidis V, Kuznetsov D, Liechti R, Moretti S, Mostaguir K, Redaschi N, Rossier G, Xenarios I, Stockinger H (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40(W1):W597–W603. https://doi.org/10.1093/nar/gks400
Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4(6):1633–1649. https://doi.org/10.1002/pmic.200300771
Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. https://doi.org/10.1006/jmbi.2000.4315
Geourjon C, Deléage G (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Bioinformatics 11(6):681–684. https://doi.org/10.1093/bioinformatics/11.6.681
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(D1):D222–D226. https://doi.org/10.1093/nar/gku1221
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35(suppl2):W585–W587. https://doi.org/10.1093/nar/gkm259
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(4):299–306. https://doi.org/10.1093/bib/bbn017
Yang Z, Ge X, Yang Z, Qin W, Sun G, Wang Z, Li Z, Liu J, Wu J, Wang Y, Lu L, Wang P, Mo H, Zhang X, Li F (2019) Extensive intraspecific gene order and gene structural variations in upland cotton cultivars. Nat Commun 10(1):2989. https://doi.org/10.1038/s41467-019-10820-x
Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7(11):847–859. https://doi.org/10.1038/nrm2020
Yu L, Liu C, Li J, Jia B, Qi X, Ming R, Qin G (2020) Identification of candidate auxin response factors involved in pomegranate seed coat development. Front Plant Sci 11:536530. https://doi.org/10.3389/fpls.2020.536530
Shen C, Yue R, Sun T, Zhang L, Xu L, Tie S, Wang H, Yang Y (2015) Genome-wide identification and expression analysis of auxin response factor gene family in Medicago truncatula. Front Plant Sci 6:73. https://doi.org/10.3389/fpls.2015.00073
Li SB, OuYang WZ, Hou XJ, Xie LL, Hu CG, Zhang JZ (2015) Genome-wide identification, isolation and expression analysis of auxin response factor (ARF) gene family in sweet orange (Citrus sinensis). Front Plant Sci 6:119. https://doi.org/10.3389/fpls.2015.00119
Zhang H, Ning C, Chunjuan D, Shang Q (2017) Genome-wide identification and expression of ARF gene family during adventitious root development in hot pepper (Capsicum annuum). Hortic Plant J 3(4):151–164. https://doi.org/10.1016/j.hpj.2017.07.001
Zhang H, Zhu J, Gong Z, Zhu JK (2022) Abiotic stress responses in plants. Nat Rev Genet 23(2):104–119. https://doi.org/10.1038/s41576-021-00413-0
Jin L, Yarra R, Zhou L, Cao H (2022) The auxin response factor (ARF) gene family in oil palm (Elaeis guineensis Jacq.): Genome-wide identification and their expression profiling under abiotic stresses. Protoplasma 259(1):47–60. https://doi.org/10.1007/s00709-021-01639-9
Yu C, Zhan Y, Feng X, Huang ZA, Sun C (2017) Identification and expression profiling of the auxin response factors in Capsicum annuum L. under abiotic stress and hormone treatments. Int J Mol Sci 18(12):2719. https://doi.org/10.3390/ijms18122719
Kang C, He S, Zhai H, Li R, Zhao N, Liu Q (2018) A sweetpotato auxin response factor gene (IbARF5) is involved in carotenoid biosynthesis and salt and drought tolerance in transgenic Arabidopsis. Front Plant Sci 9:1307. https://doi.org/10.3389/fpls.2018.01307
Gierth M, Mäser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137(3):1105–1114. https://doi.org/10.1104/pp.104.057216
Acknowledgements
This work was supported in part by the National Natural Science Foundation of China (31601347), Henan Scientific and Technological Research Program (202102110014), Training Plan for University Young Key Teachers of Henan Province (2020GGJS168) and Henan Postdoctoral Science Foundation (1902042).
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Q-LW and J-HT designed the experiments and managed the project. M-NC, JD, G-HH, Y-YL and J-BZ performed the experiments. M-NC, JD and LH performed the data analyses. M-NC, JD, Q-LW and J-HT wrote the manuscript. All authors read and approved the final manuscript.
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Chao, M., Dong, J., Hu, G. et al. Phylogeny, gene structures, and expression patterns of the auxin response factor (GhARF2) in upland cotton (Gossypium hirsutum L.). Mol Biol Rep 50, 1089–1099 (2023). https://doi.org/10.1007/s11033-022-07999-6
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DOI: https://doi.org/10.1007/s11033-022-07999-6