Abstract
A novel SQUAMOSA PROMOTER BINDING PROTEIN (SBP)-box gene, designated as VpSBP5, was isolated from Chinese wild Vitis pseudoreticulata clone “Baihe-35-1” infected by Erysiphe necator under natural field conditions. The full-length cDNA sequence of VpSBP5 comprised 3,811 bp and encoded a polypeptide of 1,030 amino acids which contained a highly conserved SBP domain bearing two zinc-binding sites of the C2HCH type and a nuclear localization signal. The deduced amino acid sequence of VpSBP5 was identical to that of VvSBP5 and grouped into the same clade (group 1) with AtSPL1, AtSPL12, AtSPL14, VvSBP7, and VvSBP17. We further confirmed that VpSBP5 gene is indeed targeted to the nucleus and possesses transcriptional activation activity. The expression of VpSBP5 as determined by reverse transcription PCR, was induced by E. necator in the E. necator-resistant V. pseudoreticulata clone Baihe-35-1 and the susceptible clone “Hunan-1,” and exhibited a quicker response in Baihe-35-1. Moreover, the expression of VpSBP5 was induced by salicylic acid (SA) and methyl jasmonate (MeJA) in Baihe-35-1. Together, our results indicate that VpSBP5 is likely to participate in the regulation of the resistance to E. necator by inducing SA and MeJA molecular signals in grape, and the degree of disease resistance of the grapevine genotypes may correlate with the time of the peak appearing.
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References
Berger S (2002) Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta 214:497–504
Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237:91–104
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574
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
Endah R, Beyene G, Kiggundu A, van den Berg N, Schlüter U, Kunert K, Chikwamba R (2008) Elicitor and Fusarium-induced expression of NPR1-like genes in banana. Plant Physiol Biochem 46:1007
Gandikota M, Birkenbihl RP, Höhmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693
Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4:301–308
Hou H, Li J, Gao M, Singer SD, Wang H, Mao L, Fei Z, Wang X (2013) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape. PLoS One 8:e59358
Hultquist JF, Dorweiler JE (2008) Feminized tassels of maize mop1 and ts1 mutants exhibit altered levels of miR156 and specific SBP-box genes. Planta 229:99–113
Imanishi S, Nakakita M, Yamashita K, Furuta A, Utsuno K, Muramoto N, Kojima H, Nakamura K (2000) Aspirin and salicylic acid do not inhibit methyl jasmonate-inducible expression of a gene for ornithine decarboxylase in tobacco BY-2 cells. Biosci Biotechnol Biochem 64:125–133
Jung C, Yeu SY, Koo YJ, Kim M, Choi YD, Cheong JJ (2007) Transcript profile of transgenic Arabidopsis constitutively producing methyl jasmonate. J Plant Biol 50:12–17
Jung JH, Seo PJ, Kang SK, Park CM (2011) miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions. Plant Mol Biol 76:35–45
Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant Microbe Interact 16:295–305
Kim HS, Delaney TP (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J 32:151–163
Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250:7–16
Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA 102:18730–18735
Lannenpaa M, Janonen I, Holtta-Vuori M, Gardemeister M, Porali I, Sopanen T (2004) A new SBP-box gene BpSPL1 in silver birch (Betula pendula). Physiol Plant 120:491–500
Le Henanff G, Heitz T, Mestre P, Mutterer J, Walter B, Chong J (2009) Characterization of Vitis vinifera NPR1 homologs involved in the regulation of pathogenesis-related gene expression. BMC Plant Biol 9:54–68
Mare C, Mazzucotelli E, Crosatti C, Francia E, Stanca A, Cattivelli L (2004) Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Mol Biol 55:399–416
Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262
Pieterse CMJ, van Loon LC (1999) Salicylic acid-independent plant defence pathways. Trends Plant Sci 4:52–58
Rea G, Metoui O, Infantino A, Federico R, Angelini R (2002) Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiol 128:865–875
Riechmann J, Heard J, Martin G, Reuber L, Keddie J, Adam L, Pineda O, Ratcliffe O, Samaha R, Creelman R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
Riese M, Höhmann S, Saedler H, Münster T, Huijser P (2007) Comparative analysis of the SBP-box gene families in P. patens and seed plants. Gene 401:28–37
Salinas M, Xing S, Höhmann S, Berndtgen R, Huijser P (2011) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 1–14
Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660
Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195
Stone JM, Liang X, Nekl ER, Stiers JJ (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754
Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019
Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136:955–964
Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20:1231–1243
Wang Y, Hu Z, Yang Y, Chen X, Chen G (2009) Function annotation of an SBP-box gene in Arabidopsis based on analysis of co-expression networks and promoters. Int J Mol Sci 10:116–132
Wang Y, Hu Z, Yang Y, Chen X, Chen G (2010) Genome-wide identification, phylogeny, and expression analysis of the SBP-box gene family in grapevine. Russ J Plant Physiol 57:273–282
Wen Z, Gao M, Jiao C, Wang Q, Xu H, Walter M, Xu W, Bassett C, Wang X (2012) Characterization and expression analysis of a retinoblastoma-related gene from Chinese wild Vitis pseudoreticulata. Plant Mol Biol Rep 30:983–991
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547
Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293
Xing S, Salinas M, Hohmann S, Berndtgen R, Huijser P (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22:3935–3950
Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191–203
Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085
Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E, Ishizuka Y, Terada T, Shirouzu M, Osanai T, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J Mol Biol 337:49–63
Yamasaki K, Kigawa T, Inoue M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y, Terada T, Shirouzu M, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2006) An Arabidopsis SBP-domain fragment with a disrupted C-terminal zinc-binding site retains its tertiary structure. FEBS Lett 580:2109–2116
Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein–like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361
Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5:313–324
Zhang JJ, Wang YJ, Wang XP, Yang KQ, Yang JX (2003) An improved method for rapidly extracting total RNA from Vitis (in Chinese). J Fruit Sci 3:178–189
Zhu X, Liu S, Meng C, Qin L, Kong L, Gm X (2013) WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Mol Biol Rep. doi:10.1007/s11105-013-0565-4
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This study was supported by the National Natural Science Foundation of China (nos. 31071782 and 30671446), 948 Project from Ministry of Agriculture of China (2012-S12), and Chinese Universities Scientific Fund (QN2011056).
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ESM Fig. S1
Full length cloning of VpSBP5 from Chinese wild V. pseudoreticulata ‘Baihe-35-1’. 24 a. The production for 3’ RACE. b. The production for 5’ RACE. (JPEG 8 kb)
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Hou, H., Yan, Q., Wang, X. et al. A SBP-Box Gene VpSBP5 from Chinese Wild Vitis Species Responds to Erysiphe necator and Defense Signaling Molecules. Plant Mol Biol Rep 31, 1261–1270 (2013). https://doi.org/10.1007/s11105-013-0591-2
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DOI: https://doi.org/10.1007/s11105-013-0591-2