Abstract
Auxin has been widely implicated in various aspects of plant growth and development, including flower development. In order to further elucidate the role of auxin during flower development, especially on the pistil development process, auxin response factors (ARFs), an important component in auxin signalling pathway, were studied in the early flower buds of Japanese apricot (Prunus mume Sieb. et Zucc). In this study, a comprehensive overview of the ARF gene family in Japanese apricot is presented, including the chromosomal locations, phylogenetic relationships, gene structures, the domain and nuclear localization analysis. Seventeen Japanese apricot genes that encode ARF proteins (PmARFs) have been identified based on the genome sequence of Japanese apricot. Comparison of the expression of some PmARF genes between perfect and imperfect flower buds in Japanese apricot suggests that PmARFs, especially the PmARF13 and PmARF17 gene may be required for pistil development and function in Japanese apricot. These results will be useful for future functional analyses of the ARF family genes in plants.
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References
Abel S, Theologis A (1996) Early genes and auxin action Plant Physiology 111:9
Abel S, Ballas N, Wong LM, Theologis A (1996) DNA elements responsive to auxin Bioessays 18:647–654
Attia KA et al (2009) Antisense phenotypes reveal a functional expression of OsARF1, an auxin response factor, in transgenic rice. Curr Iss Mol Biol 11(1):129
Banks JA et al (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963
Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799
Chu M (1999) China fruit records-Mei China Forestry, Beijing
Davies PJ (1995) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic, Dordrecht, The Netherlands
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445
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
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic acids research:gkr367
Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230
Gao Z, Shi T, Luo X, Zhang Z, Zhuang W, Wang L (2012) High-throughput sequencing of small RNAs and analysis of differentially expressed microRNAs associated with pistil development in Japanese apricot BMC genomics 13:371
Goetz M, Vivian-Smith A, Johnson SD, Koltunow AM (2006) AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell Online 18:1873–1886
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460
Guilfoyle T, Hagen G, Ulmasov T, Murfett J (1998) How does auxin turn on genes? Plant Physiol 118:341–347
Guo A-Y, Zhu Q-H, Gu X, Ge S, Yang J, Luo J (2008) Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. Gene 418:1–8
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385
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
Hardtke CS et al (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131:1089–1100
Hou J-H, Gao Z-H, Zhang Z, Chen S-M, Ando T, Zhang J-Y, Wang X-W (2011) Isolation and characterization of an AGAMOUS homologue PmAG from the Japanese apricot (Prunus mume Sieb. et Zucc.). Plant Mol Biol Rep 29:473–480
Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006a) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59
Jain M, Kaur N, Tyagi AK, Khurana JP (2006b) The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genomics 6:36–46
Jain M, Tyagi AK, Khurana JP (2006c) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88:360–371
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
Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451
Kim J, Harter K, Theologis A (1997) Protein–protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci 94:11786–11791
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
Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Larsson E, Franks RG, Sundberg E (2013) Auxin and the Arabidopsis thaliana gynoecium. J Exp Bot 64:2619–2627
Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell Online 20:1738–1746
Li X et al (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184
Liu S, Hu L (2013a) Genome-wide analysis of the auxin response factor gene family in cucumber. Genet Mol Res 12:4317–4331
Liu S, Hu L (2013b) Genome-wide analysis of the auxin response factor gene family in cucumber. Genet Mol Res 12:4317–4331
Liu X et al (2014) AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy. Plant J 80:629–641
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Martínez-Fernández I et al (2014) The effect of NGATHA altered activity on auxin signaling pathways within the Arabidopsis gynoecium Frontiers in plant science 5:1–11
Mashiguchi K et al (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci 108:18512–18517
Meisel L et al (2005) A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol Res 38:83–88
Nagpal P et al (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118
Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation The Plant Cell. Online 3:677–684
Okushima Y et al (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 Online 17:444–463
Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype The Plant Cell. Online 13:829–841
Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity The Plant Cell. Online 17:2899–2910
Petrášek J et al (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux Science 312:914–918
Punta M et al (2012) The Pfam protein families database. Nucl Acids Res 40:D290–D301
Raes J, Vandepoele K, Simillion C, Saeys Y, Van de Peer Y (2003) Investigating ancient duplication events in the Arabidopsis genome. In: Genome evolution. Springer, pp 117–129
Rensing SA et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69
Riaño-Pachón DM, Ruzicic S, Dreyer I, Mueller-Roeber B (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8:42
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 133:251–261
Sessions RA, Zambryski PC (1995) Arabidopsis gynoecium structure in the wild and in ettin mutants. Development 121:1519–1532
Shi T, Zhang Q-L, Gao Z-H, Zhang Z, Zhuang W-B (2011) Analyses on pistil differentiation process and related biochemical indexes of two cultivars of Prunus mume. J Plant Res Environ 20:35–41
Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci 99:13627–13632
Stepanova AN et al (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis The Plant Cell. Online 23:3961–3973
Sun Hai-long, Song Juan, Gao Zhi-hong, Ni Zhao-jun, Zhen Z (2014) Isolation and expression analysis of PmKNAT2 gene from Japanese apricot 47(17):3444–3452
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell Online 15:533–543
Tobeña-Santamaria R, Bliek M, Ljung K, Sandberg G, Mol JN, Souer E, Koes R (2002) FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture. Genes Dev 16:753–763
Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71
Ulmasov T, Hagen G, Guilfoyle TJ (1997a) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868
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 Online 9:1963–1971
Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci 96:5844–5849
Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319
Wan S, Li W, Zhu Y, Liu Z, Huang W, Zhan J (2014) Genome-wide identification, characterization and expression analysis of the auxin response factor gene family in Vitis vinifera. Plant cell Rep, pp 1–11
Wang S, Tiwari SB, Hagen G, Guilfoyle TJ (2005a) AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell Online 17:1979–1993
Wang X, Shi X, Hao B, Ge S, Luo J (2005b) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165:937–946
Wang D et al (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24
Wang Y, Deng D, Shi Y, Miao N, Bian Y, Yin Z (2012) Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Mol Biol Rep 39:2401–2415
Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102:9703–9708
Wilmoth JC et al (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130
Wiśniewska J et al (2006) Polar PIN localization directs auxin flow in plants. Science 312:883
Won C et al (2011) Conversion of tryptophan to indole-3-acetic acid by tryptophan aminotransferases OF Arabidopsis and YUCCAs in Arabidopsis. Proc Natl Acad Sci 108:18518–18523
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis Science 291:306–309
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We gratefully acknowledge the Fundamental Research Funds for the Central University (KYZ201208), the Qinglan Project of Jiangsu Province and the National Science Foundation of China (31101526) for providing financial support.
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Communicated by J.-H Liu.
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Song, J., Gao, Z., Huo, X. et al. Genome-wide identification of the auxin response factor (ARF) gene family and expression analysis of its role associated with pistil development in Japanese apricot (Prunus mume Sieb. et Zucc). Acta Physiol Plant 37, 145 (2015). https://doi.org/10.1007/s11738-015-1882-z
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DOI: https://doi.org/10.1007/s11738-015-1882-z