Skip to main content
SpringerLink
Log in

A characterization of grapevine of GRAS domain transcription factor gene family

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

GRAS domain genes are a group of important plant-specific transcription factors that have been reported to be involved in plant development. In order to know the roles of GRAS genes in grapevine, a widely cultivated fruit crop, the study on grapevine GRAS (VvGRAS) was carried out, and from which, 43 were identified from 12× assemble grapevine genomic sequences. Further, the genomic structures, synteny, phylogeny, expression profiles in different tissues of these genes, and their roles in response to stress were investigated. Among the genes, two potential target genes (VvSCL15 and VvSCL22) for VvmiR171 were experimentally verified by PPM-RACE and RLM-RACE, in that not only the cleavage sites of miR171 on the target mRNA were mapped but also the cleaved fragments and their expressing patterns were detected. Transgenic Arabidopsis plants over expression VvSCL15 showed lower tolerance to drought and salt treatments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Abarca D, Pizarro A, Hernández I, Sánchez C, Solana SP, del Amo A, Carneros E, Díaz-Sala C (2014) The GRAS gene family in pine: transcript expression patterns associated with the maturation-related decline of competence to form adventitious roots. BMC Plant Biol 14:354

    Article  PubMed  PubMed Central  Google Scholar 

  • Allison MC, Bouché N (2008) microRNA-directed regulation: to cleave or not cleave. Trends Plant Sci 13:359–367

    Article  Google Scholar 

  • Benfey PN, Scheres B (2000) Root development. Curr Biol 10:R813–R815

    Article  CAS  PubMed  Google Scholar 

  • Bolle C (2004) The role of GRAS protein in plant signal transduction and development. Planta 218:683–692

    Article  CAS  PubMed  Google Scholar 

  • Bolle C, Koncz C, Chun NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome. A signal transduction. Genes Dev 14:1269–1278

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamaoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Burklew CE, Xie F, Ashlock J, Zhang B (2014) Expression of microRNAs and their targets regulates floral development in tobacco (Nicotiana tabacum). Funct Integr Genomics 14:299–306

    Article  CAS  PubMed  Google Scholar 

  • Carra A, Mica E, Gambino G, Pindo M, Moser C, Pe ME, Schubert A (2009) Cloning and characterization of small non-coding RNAs from grape. Plant J 59:750–763

    Article  CAS  PubMed  Google Scholar 

  • Chang SJ, Jepf P, Johne A (1993) Simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116

    Article  CAS  Google Scholar 

  • Chen X (2008) MicroRNA metabolism in plants. Curr Top Microbiol Immunol 320:117–136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA (2011) PLEXdb: gene expression resource for plants and plant pathogens. Nucleic Acids Res 40:D1194–D1201

    Article  PubMed  PubMed Central  Google Scholar 

  • Fode B, Siemsen T, Thurow C, Weigel R, Gatz C (2008) The Arabidopsis GRAS protein SCL14 interacts with classIITGA transcription factors and is essential for the activation of stress inducible promoters. Plant Cell 20:3122–3135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu H, Tie Y, Xu C, Zhang Z, Zhu J, Shi Y, Jiang H, Sun Z, Zheng X (2005) Identification of human fetal liver miRNAs by a novel method. FEBS Lett 579:3849–3854

    Article  CAS  PubMed  Google Scholar 

  • Grant-Downton R, Hafidh S, Twell D, Dickinson HG (2009) Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol Plant 2:500–512

    Article  CAS  PubMed  Google Scholar 

  • Grigorova B, Mara C, Hollender C, Sijacic P, Chen XM, Liu ZC (2011) LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138:2451–2456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026

    Article  CAS  PubMed  Google Scholar 

  • Hynes LW, Peng J, Richards DE, Harberd NP (2003) Transgenic expression of the Arabidopsis DELLA proteins GAI and gai confers altered gibberellin response in tobacco. Transgenic Res 12:707–714

    Article  CAS  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurns B, Gouyvenoux M, Ugarte E, Cattonaro G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Kumar RR, Pathak H, Sharma SK, Kala YK, Nirjal MK, Singh GP, Goswami S, Rai RD (2015) Novel and conserved heat-responsive microRNAs in wheat (Triticum aestivum L.). Funct Integr Genomics 15:323–348

    Article  CAS  PubMed  Google Scholar 

  • Lee M, Kim B, Song SK, Heo JO, Yu NI, Lee SA, Kim M, Kim MK, Sohn SO, Lim CE, Chang KS, Lee MM, Lim J (2008) Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. Plant Mol Biol 67:659–670

    Article  CAS  PubMed  Google Scholar 

  • Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X, Ji L, Pan Z, Cao X, Mo B, Zhang F, Raikhel N, Jiang L, Chen X (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim J, Jung JM, Lim CE, Lee MH, Kim BJ, Kim M, Bruce WB, Benfey PN (2005) Conservation and diversification of SCARECROW in maize. Plant Mol Biol 59:619–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Chen YQ (2010) A new mechanism in plant engineering: the potential roles of microRNAs in molecular breeding for crop improvement. Biotechnol Adv 28:301–307

    Article  CAS  PubMed  Google Scholar 

  • Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61:4011–4019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathieu J, Yant LJ, Mürdter F, Küttner F, Schmid M (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7:e1000148

    Article  PubMed  PubMed Central  Google Scholar 

  • Mica E, Piccolo V, Delledonne M, Ferrarini A, Pezzotti M, Casati C, Fabbro CD, Valle G, Policriti A, Morgate M, Pesole G, Pe ME, Horner DS (2009) High throughput approaches reveal splicing of primary microRNA transcripts and tissue specific expression of mature microRNAs in Vitis vinifera. BMC Genomics 10:558

    Article  PubMed  PubMed Central  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    CAS  PubMed  Google Scholar 

  • Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976

    CAS  PubMed  Google Scholar 

  • Petricka JJ, Benfey PN (2008) Root layers: complex regulation of development patterning. Curr Opin Genet Dev 18:354–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramachandran V, Chen X (2008) Small RNA metabolism in Arabidopsis. Trends Plant Sci 13:368–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55:65–76

    Article  CAS  PubMed  Google Scholar 

  • Schott G, Mari-Ordonez A, Himber C, Alioua A, Voinnet O, Dunoyer P (2012) Differential effects of viral silencing suppressors on siRNA and miRNA loading support the existence of two distinct cellular pools of ARGONAUTE1. EMBO J 31:2553–2565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schumacher K, Schmitt TT, Rossberg M, Schmitz G, Theres K (1999) The Lateral supressor (Ls) gene of tomato encodes a member of the VHIID protein family. Proc Natl Acad Sci U S A 96:290–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slewinski TL, Anderson AA, Zhang C, Turgeon R (2012) Scarecrow plays a role in establishing Kranz anatomy in maize leaves. Plant Cell Physiol 53:2030–2037

    Article  CAS  PubMed  Google Scholar 

  • Song CN, Fang JG, Li XY, Liu H, Thomas Chao C (2009) Identification and characterization of 27 conserved microRNAs in citrus. Planta 230:671–685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song CN, Fang JG, Wang C, Guo L, Nicholas KK, Ma Z (2010a) miR-RACE, a new efficient approach to determine the precise sequences of computationally identified trifoliate orange (Poncirus trifoliata) microRNAs. PLoS ONE 5:e10861

    Article  PubMed  PubMed Central  Google Scholar 

  • Song C, Jia Q, Fang J, Li F, Wang C, Zhang Z (2010b) Computational identification of citrus microRNAs and target analysis in citrus expressed sequence tags. Plant Biol 12:927–934

    Article  CAS  PubMed  Google Scholar 

  • Song L, Axtell MJ, Fedoroff NV (2010c) RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr Biol 20:34–41

    Article  Google Scholar 

  • Sun X, Xue B, Jones WT, Rikkerink E, Dunker AK, Uversky VN (2011) A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol Biol 77:205–223

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Korir NK, Han J, Shangguan LF, Kayesh E (2012) Characterization of grapevine microR164 and its target genes. Mol Biol Rep 39:9463–9472

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thiebaut F, Rojas CA, Almeida KL, Grativol C, Domiciano GC, Lamb CRC, De Engler JA, Hemerly AS, Ferreira PCG (2012) Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ 35:502–512

    Article  CAS  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitz Gerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Dematte L, Mraz A, Battolana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326

    Article  PubMed  PubMed Central  Google Scholar 

  • Von Arnim AG, Deng XW (1994) Light inactivation of arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 16:1035–1045

  • Wang L, Mai YX, Zhang YC, Luo Q, Yang HQ (2010) MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL-IV genes regulate shoot branching in Arabidopsis. Mol Plant 3:794–806

    Article  PubMed  Google Scholar 

  • Wang C, Shangguan LF, Kibet KN, Wang X, Han J, Song CN, Fang JG (2011) Characterization of microRNAs identified in a table grapevine cultivar with validation of computationally predicted grapevine miRNAs by miR-RACE. PLoS ONE 6:e21259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Zheng Y, Xin HP, Fang LC, Li SH (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75

    Article  PubMed  Google Scholar 

  • Wilson DN, Chung H, Elliott RC, Bremer E, George D, Koh S (2005) Microarray analysis of postictal transcriptional regulation of neuropeptides. J Mol Neurosci 25:285–298

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, Jiangsu Province, People’s Republic of China

    Xin Sun, Zhengqiang Xie, Cheng Zhang, Qian Mu, Baoju Wang & Jinggui Fang

  2. Department of Agronomy and Horticulture, Jiangsu Polytechnic College of Agriculture and Forestry, Jurong, 212400, Jiangsu Province, People’s Republic of China

    Zhengqiang Xie

  3. Institute of Horticulture, Jiangsu Academy of Agriculture Sciences, Nanjing, 210014, Jiangsu Province, People’s Republic of China

    Weimin Wu

Authors
  1. Xin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhengqiang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qian Mu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weimin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Baoju Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jinggui Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jinggui Fang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig S1

(DOC 171 kb)

Table S1

(XLS 21 kb)

Table S2

(DOC 91 kb)

Table S3

(XLS 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, X., Xie, Z., Zhang, C. et al. A characterization of grapevine of GRAS domain transcription factor gene family. Funct Integr Genomics 16, 347–363 (2016). https://doi.org/10.1007/s10142-016-0479-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-016-0479-y

Keywords

Search

Navigation