Abstract
Auxin response factor (ARF) acts as a vital component of auxin signaling and participates in growth, development, and stress responses in plants. In the present study, we comprehensively analyzed kiwifruit’s (Actinidia chinensis) ARF genes (AcARFs) and their involvement in abiotic stress response. We identified a total of 41 AcARFs encoding ARFs in the A. chinensis genome. AcARF genes were characterized by the classic ARF_resp and a B3 domain and primarily localized on the cytoplasm and nucleus. AcARFs were categorized into eight subgroups as per the phylogenetic analysis. Synteny analysis showed that 35 gene pairs in AcARF family underwent segmental and whole genome duplication events. Promoter cis-element prediction revealed that AcARFs might be involved in abiotic factors related to stress response, which was later assessed and validated by qRT-PCR based expression analysis. Additionally, AcARFs showed tissue-specific expression. These findings extend our understanding of the functional roles of AcARFs in stress responses. Taken together, the systematic annotation of the AcARF family genes provides a platform for the functional and evolutionary study, which might help in elucidating the precise roles of the AcARFs in stress responses.
Similar content being viewed by others
References
Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328. https://doi.org/10.1007/s00425-005-0088-9
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–208. https://doi.org/10.1093/nar/gkp335
Berendzen KW, Weiste C, Wanke D, Kilian J, Harter K, Droge-Laser W (2012) Bioinformatic cis-element analyses performed in Arabidopsis and rice disclose bZIP- and MYB-related binding sites as potential AuxRE-coupling elements in auxin-mediated transcription. Bmc Plant Biol. https://doi.org/10.1186/1471-2229-12-125
Bouzroud S, Gouiaa S, Hu N, Bernadac A, Mila I, Bendaou N, Smouni A, Bouzayen M, Zouine, (2018) Auxin Response Factors (ARFs) are potential mediators of auxin action in tomato response to biotic and abiotic stress (Solanum lycopersicum). PLoS ONE. 13(2):e0193517. https://doi.org/10.1371/journal.pone.0193517
Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500
de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170. https://doi.org/10.1111/j.1365-313X.2008.03671.x
de Jong M, Wolters-Arts M, Garcia-Martinez JL, Mariani C, Vriezen WH (2011) The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62:617–626. https://doi.org/10.1093/jxb/erq293
Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2006) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA 103:236–241. https://doi.org/10.1073/pnas.0507127103
Finn RD, Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–285. https://doi.org/10.1093/nar/gkv1344
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. https://doi.org/10.1016/j.pbi.2007.08.014
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:e1005649. https://doi.org/10.1371/journal.pgen.1005649
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. https://doi.org/10.1093/emboj/17.5.1405
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:W585–W587. https://doi.org/10.1093/nar/gkm259
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015a) GSDS 20: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Hu W, Zuo J, Hou X, Yan Y, Wei Y, Liu J, Li M, Xu B, Jin Z (2015b) The auxin response factor gene family in banana: genome-wide identification and expression analyses during development, ripening, and abiotic stress. Front Plant Sci 6:742. https://doi.org/10.3389/fpls.2015.00742
Huang S, Jian D, Deng D, Tang W, Liu Y (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun 4(4):2640. https://doi.org/10.1038/ncomms3640
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. https://doi.org/10.1111/j.1742-4658.2009.07033.x
Ji C, Jiang L (2015) Molecular characterization of ARF family proteins in Arabidopsis. Mol Biol Cell 26:862–875
Jing Z, Liu Z (2018) Genome-wide identification of WRKY transcription factors in kiwifruit (Actinidia spp.) and analysis of WRKY expression in responses to biotic and abiotic stresses. Genes Genomics 40:429–446. https://doi.org/10.1007/s13258-017-0645-1
Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59. https://doi.org/10.1186/1471-2229-7-59
Kalve S, Sizani BL, Markakis MN, Helsmoortel C, Vandeweyer G, Laukens K, Sommen M, Naulaerts S, Vissenberg K, Prinsen E, Beemster GTS (2020) Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF-mediated auxin responses. New Phytol 226:1766–1780. https://doi.org/10.1111/nph.16490
Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665. https://doi.org/10.1093/aob/mct229
Keller O, Odronitz F, Stanke M, Kollmar M, Waack S (2008) Scipio: using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species. BMC Bioinform 9:278. https://doi.org/10.1186/1471-2105-9-278
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 Genomics 285:245–260. https://doi.org/10.1007/s00438-011-0602-7
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
Li SB, OuYang WZ, Hou XJ, Xie LL, Hu CG, Zhang JZ (2015a) 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
Li Q, Yu H, Cao PB, Fawal N, Mathe C, Azar S, Cassan-Wang H, Myburg AA, Grima-Pettenati J, Marque C (2015b) Explosive tandem and segmental duplications of multigenic families in eucalyptus grandis. Genome Biol Evol (4):1068–1081. https://doi.org/10.1093/gbe/evv048
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950. https://doi.org/10.1242/dev.086363
Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339. https://doi.org/10.1104/pp.013623
McAtee P, Karim S, Schaffer R, David K (2013) A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci 4:79. https://doi.org/10.3389/fpls.2013.00079
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 287:765–784. https://doi.org/10.1007/s00438-012-0718-4
Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118. https://doi.org/10.1242/dev.01955
Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D (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. https://doi.org/10.1105/tpc.104.028316
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130. https://doi.org/10.1105/tpc.106.047761
Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Hong Q (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300. https://doi.org/10.1105/tpc.105.036723
Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910. https://doi.org/10.1105/tpc.105.034876
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: Identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864. https://doi.org/10.1186/gb-2000-1-1-reports234
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
Silva AE, Villanueva WJ, Knidel H, Bonato VC, Reis SF, Von Zuben FJ (2005) A multi-neighbor-joining approach for phylogenetic tree reconstruction and visualization. Genet Mol Res 4:525–534
Singh VK, Rajkumar MS, Garg R, Jain M (2017) Genome-wide identification and co-expression network analysis provide insights into the roles of auxin response factor gene family in chickpea. Sci Rep 7:10895. https://doi.org/10.1038/s41598-017-11327-5
Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L (2008) The arabidopsis information resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014. https://doi.org/10.1093/nar/gkm965
Tippmann HF (2004) Analysis for free: comparing programs for sequence analysis. Brief Bioinform 5:82–87
Tiryaki I (2009) Biosynthesis metabolism and signaling pathway of Auxin in plants Philipp. Agric Sci 92:243–253
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543
Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
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. https://doi.org/10.1016/j.gene.2007.01.006
Wang YC et al (2018) Auxin regulates anthocyanin biosynthesis through the Aux/IAA-ARF signaling pathway in apple. Hortic Res-Engl. https://doi.org/10.1038/s41438-018-0068-4
Wang SX, Shi FY, Dong XX, Li YX, Zhang ZH, Li H (2019) Genome-wide identification and expression analysis of auxin response factor (ARF) gene family in strawberry (Fragaria vesca). J Integr Agr 18:1587–1603. https://doi.org/10.1016/S2095-3119(19)62556-6
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Tae-ho L, Jin H, Barry M, Guo H (2012) Mcscanx: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7):e49–e49. https://doi.org/10.1093/nar/gkr1293
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552
Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130. https://doi.org/10.1111/j.1365-313X.2005.02432.x
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735. https://doi.org/10.1093/aob/mci083
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
Yu H, Soler M, Mila I, San Clemente H, Savelli B, Dunand C, Paiva JA, Myburg AA, Bouzayen M, Grima-Pettenati J (2014) Genome-wide characterization and expression profiling of the AUXIN RESPONSE FACTOR (ARF) gene family in Eucalyptus grandis. PLoS ONE 9:e108906. https://doi.org/10.1371/journal.pone.0108906
Yuan YJ, Xu X, Gong ZH, Tang YW, Deng W (2019) Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato. Hortic Res-Engl. https://doi.org/10.1038/s41438-019-0167-x
Zhou P, Fatima M, Ma XY, Liu J, Ming R (2019) Auxin regulation involved in gynoecium morphogenesis of papaya flowers. Hortic Res Engl. https://doi.org/10.1038/s41438-019-0205-8
Acknowledgements
We gratefully thank for funding from Shaanxi Engineering Research Center for Kiwifruit, Shaanxi Aerospace Breeding Engineering Research Center and Key Disciplines of Botany of Xi'an City.
Funding
This research was funded by National Natural Science Foundation of China (31701935), Agricultural technology R & D project of Xi’an City (20NYYF0037), Key Industry Chain Project of Shaanxi Province (2018TSCXL-NY-01–03; 2020ZDLNY03-01; S2021-YF-YBNY-0248) and Natural Science Foundation of Chongqing (cstc2020jcyj-msxmX1064).
Author information
Authors and Affiliations
Contributions
Conceptualization, QL and LS; methodology, MX, YL, JD, YW and LS; software, LS; formal analysis, LS; resources, LS; data curation, LS. and QL; writing—original draft preparation, LS; writing—review and editing, QL; funding acquisition, LS and QL; All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Su, L., Xu, M., Zhang, J. et al. Genome-wide identification of auxin response factor (ARF) family in kiwifruit (Actinidia chinensis) and analysis of their inducible involvements in abiotic stresses. Physiol Mol Biol Plants 27, 1261–1276 (2021). https://doi.org/10.1007/s12298-021-01011-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-01011-4