Skip to main content
Log in

Evolutionary and expression analysis of a MADS-box gene superfamily involved in ovule development of seeded and seedless grapevines

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

MADS-box transcription factors are involved in many aspects of plant growth and development, such as floral organ determination, fruit ripening, and embryonic development. Yet not much is known about grape (Vitis vinifera) MADS-box genes in a relatively comprehensive genomic and functional way during ovule development. Accordingly, we identified 54 grape MADS-box genes, aiming to enhance our understanding of grape MADS-box genes from both evolutionary and functional perspectives. Synteny analysis indicated that both segmental and tandem duplication events contributed to the expansion of the grape MADS-box family. Furthermore, synteny analysis between the grape and Arabidopsis genomes suggested that several grape MADS-box genes arose before divergence of the two species. Phylogenetic analysis and comparisons of exon–intron structures provided further insight into the evolutionary relationships between the genes, as well as their putative functions. Based on phylogenetic tree analysis, grape MADS-box genes were divided into type I and type II subgroups. Tissue-specific expression analysis suggested roles in both vegetative and reproductive tissue development. Expression analysis of the MADS-box genes following gibberellic acid (GA3) treatment revealed their response to GA3 treatment and that seedlessness caused by GA3 treatment underwent a different mechanism from that of normal ovule abortion. Expression profiling of MADS-box genes from six cultivars suggests their function in ovule development and may represent potential ovule identity genes involved in parthenocarpy. The results presented provide a few candidate genes involved in ovule development for future study, which may be useful in seedlessness-related molecular breeding programs.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Abbreviations

GA3 :

Gibberellic acid

DAF:

Days after full bloom

cDNA:

Complementary DNA

TF:

Transcription factor

PCR:

Polymerase chain reaction

α:

Alpha

β:

Beta

STK :

SEEDSTICK

SHP:

SHATTERPROOF

FBP:

FLORAL BINDING PROTEIN

SVP :

SHORT VEGETATIVE PHASE

ANR1 :

ARABIDOPSIS NITRATE REGULATED 1

AG :

AGAMOUS

SEP:

STRESS ENHANCED PROTEIN

HMM:

Hidden Markov Model

NCBI:

National Center for Biotechnology Information

NJ:

Neighbor-joining

SMART:

Simple modular architecture research tool

GSDS:

Gene structure display server

USP:

Universal stress protein

References

  • Agüero C, Vigliocco A, Abdala G, Tizio R (2000) Effect of gibberellic acid and uniconazol on embryo abortion in the stenospermocarpic grape cultivars Emperatriz and Perlon. Plant Growth Regul 30:9–16

    Article  Google Scholar 

  • Airoldi CA, Davies B (2012) Gene duplication and the evolution of plant MADS-box transcription factors. J Genet Genomics 39:157–165

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla E, Liljegren S, Pelaz S, Gold S, Burgeff C, Ditta G, Vergara-Silva F, Yanofsky M (2000a) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457–466

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pouplana L, Martínez-Castilla L, Yanofsky MF (2000b) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci 97:5328–5333

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Angenent GC, Colombo L (1996) Molecular control of ovule development. Trends Plant Sci 1:228–232

    Article  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh A, Singh V, Tyagi A, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genom 8:242

    Article  Google Scholar 

  • Aswath CR, Kim SH (2005) Another story of MADS-box genes—their potential in plant biotechnology. Plant Growth Regul 46:177–188

    Article  CAS  Google Scholar 

  • Becker A, Theißen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    Article  CAS  PubMed  Google Scholar 

  • Blanc G, Wolfe K (2004a) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blanc G, Wolfe KH (2004b) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bonhomme F, Kurz B, Melzer S, Bernier G, Jacqmard A (2000) Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in regulation of the floral transition in Sinapis alba. Plant J 24:103–111

    Article  CAS  PubMed  Google Scholar 

  • Boss PK, Sensi E, Hua C, Davies C, Thomas MR (2002) Cloning and characterization of grapevine (Vitis vinifera L.) MADS-box genes expressed during inflorescence and berry development. Plant Sci 162:887–895

    Article  CAS  Google Scholar 

  • Bouché N, Bouchez D (2001) Arabidopsis gene knockout: phenotypes wanted. Curr Opin Plant Biol 4:111–117

    Article  PubMed  Google Scholar 

  • Cain D, Emershad R, Tarailo R (1983) In-ovulo embryo culture and seedling development of seeded and seedless grapes (Vitis vinifera L.). Vitis 22:9–14

    Google Scholar 

  • Cheng C, Xu X, Singer SD, Li J, Zhang H, Gao M, Wang L, Wang X (2013) Effects of GA3 on antioxidant activity, ovule development and expression of genes related to ovule development in grape. PLoS One 8(11):e80044

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cho S, Jang S, Chae S, Chung K, Moon Y, An G, Jang S (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40:419–429

    Article  CAS  PubMed  Google Scholar 

  • Colombo L, Franken J, Koetje E, van Went J, Dons H, Angenent G, van Tunen A (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7:1859–1868

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Colombo L, Battaglia R, Kater MM (2008) Arabidopsis ovule development and its evolutionary conservation. Trends Plant Sci 13:444–450

    Article  CAS  PubMed  Google Scholar 

  • De Bodt S, Raes J, Peer Y, Theißen G (2003) And then there were many: MADS goes genomic. Trends Plant Sci 8:475–483

    Article  PubMed  Google Scholar 

  • Diaz-Riquelme J, Lijavetzky D, Martinez-Zapater J, Carmona M (2009) Genome-wide analysis of MIKCC-type MADS box genes in grapevine. Plant Physiol 149:354–369

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doyle J, Flagel L, Paterson A, Rapp R, Soltis D, Soltis P, Wendel J (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461

    Article  CAS  PubMed  Google Scholar 

  • Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk P, An G, Colombo L, Kater M (2007) The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J 52:690–699

    Article  CAS  PubMed  Google Scholar 

  • Egea-Cortines M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18:5370–5379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Favaro R, Immink R, Ferioli V, Bernasconi B, Byzova M, Angenent G, Kater M, Colombo L (2002) Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol Genet Genomics 268:152–159

    Article  CAS  PubMed  Google Scholar 

  • Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky M, Kater M, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferrario S, Immink RG, Shchennikova A, Busscher-Lange J, Angenent GC (2003) The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15:914–925

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gaffe J, Lemercier C, Alcaraz J-P, Kuntz M (2011) Identification of three tomato flower and fruit MADS-box proteins with a putative histone deacetylase binding domain. Gene 471:19–26

    Article  CAS  PubMed  Google Scholar 

  • Gramzow L, Ritz MS, Theißen G (2010) On the origin of MADS-domain transcription factors. Trends Genet 26:149–153

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guo R, Xu X, Carole B, Li X, Gao M, Zheng Y, Wang X (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genom 14:554

    Article  CAS  Google Scholar 

  • Guo C, Guo R, Xu X, Gao M, Li X, Song J, Zheng Y, Wang X (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65:1513–1528

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360

    Article  CAS  PubMed  Google Scholar 

  • Henschel K, Kofuji R, Hasebe M, Saedler H, Munster T, Theißen G (2002) Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol 19:801–814

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Hernández T, Martínez-Castilla LP, Alvarez-Buylla ER (2007) Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein–protein interaction domains after major gene duplication events. Mol Biol Evol 24:465–481

    Article  PubMed  Google Scholar 

  • Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, Irish VF (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23:2245–2258

    Article  CAS  PubMed  Google Scholar 

  • Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529

    Article  CAS  PubMed  Google Scholar 

  • Immink RGH, Ferrario S, Busscher-Lange J, Kooiker M, Busscher M, Angenent GC (2003) Analysis of the petunia MADS-box transcription factor family. Mol Genet Genomics 268:598–606

    CAS  PubMed  Google Scholar 

  • Immink R, Nougalli Tonaco I, de Folter S, Shchennikova A, van Dijk A, Busscher-Lange J, Borst J, Angenent G (2009) SEPALLATA3: the ‘glue’ for MADS box transcription factor complex formation. Genome Biol 10:R24

    Article  PubMed Central  PubMed  Google Scholar 

  • Immink RGH, Kaufmann K, Angenent GC (2010) The ‘ABC’ of MADS domain protein behaviour and interactions. Semin Cell Dev Biol 21:87–93

    Article  CAS  PubMed  Google Scholar 

  • Jager M, Hassanin A, Manuel M, Le Guyader H, Deutsch J (2003) MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Mol Biol Evol 20:842–854

    Article  CAS  PubMed  Google Scholar 

  • Jaillon O, Aury J, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Johansen B, Pedersen LB, Skipper M, Frederiksen S (2002) MADS-box gene evolution—structure and transcription patterns. Mol Phylogenet Evol 23:458–480

    Article  CAS  PubMed  Google Scholar 

  • Kapazoglou A, Engineer C, Drosou V, Kalloniati C, Tani E, Tsaballa A, Kouri ED, Ganopoulos I, Flemetakis E, Tsaftaris AS (2012) The study of two barley Type I-like MADS-box genes as potential targets of epigenetic regulation during seed development. BMC Plant Biol 12:166

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kimura PH, Okamoto G, Hirano K (1996) Effects of gibberellic acid and streptomycin on pollen germination and ovule and seed development in Muscat Bailey A. Am J Enol Vitic 47:152–156

    CAS  Google Scholar 

  • Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M (2003) Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol 20:1963–1977

    Article  CAS  PubMed  Google Scholar 

  • Ledbetter C, Burgos L (1994) Inheritance of stenospermocarpic seedlessness in Vitis vinifera L. J Hered 85:157–160

    Google Scholar 

  • Ledbetter C, Ramming D (1989) Seedlessness in grapes. Hort Rev 11:159–184

    Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lightfoot DJ, Malone KM, Timmis JN, Orford SJ (2008) Evidence for alternative splicing of MADS-box transcripts in developing cotton fibre cells. Mol Genet Genomics 279:75–85

    Article  CAS  PubMed  Google Scholar 

  • Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770

    Article  CAS  PubMed  Google Scholar 

  • Lyons E, Pedersen B, Kane J, Alam M, Ming R, Tang H, Wang X, Bowers J, Paterson A, Lisch D, Freeling M (2008) Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol 148:1772–1781

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  CAS  PubMed  Google Scholar 

  • Mejia N, Soto B, Guerrero M, Casanueva X, Houel C, de los Angeles Miccono M, Ramos R, Le Cunff L, Boursiquot J-M, Hinrichsen P, Adam-Blondon A-F (2011) Molecular, genetic and transcriptional evidence for a role of VvAGL11 in stenospermocarpic seedlessness in grapevine. BMC Plant Biol 11:57

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Melzer R, Verelst W, Theißen G (2009) The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro. Nucleic Acids Res 37:144–157

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mesejo C, Martínez-Fuentes A, Reig C, Agustí M (2008) Gibberellic acid impairs fertilization in Clementine mandarin under cross-pollination conditions. Plant Sci 175:267–271

    Article  CAS  Google Scholar 

  • Messenguy F, Dubois E (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316:1–21

    Article  CAS  PubMed  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel mads domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moore S, Vrebalov J, Payton P, Giovannoni J (2002) Use of genomics tools to isolate key ripening genes and analyse fruit maturation in tomato. J Exp Bot 53:2023–2030

    Article  CAS  PubMed  Google Scholar 

  • Okamoto G, Miura K (2005) Effect of pre-bloom GA application on pollen tube growth in cv. Delaware grape pistils. Vitis-Geilweilerhof 44:157

    CAS  Google Scholar 

  • Parenicova L, de Folter S, Kieffer M, Horner D, Favalli C, Busscher J, Cook H, Ingram R, Kater M, Davies B (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peng J, Harberd NP (2002) The role of GA-mediated signalling in the control of seed germination. Curr Opin Plant Biol 5:376–381

    Article  CAS  PubMed  Google Scholar 

  • Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2009) DOG 1.0: illustrator of protein domain structures. Cell Res 19:271–273

    Article  CAS  PubMed  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277

    Article  CAS  PubMed  Google Scholar 

  • Rounsley S, Ditta G, Yanofsky M (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saedler H, Becker A, Winter K, Kirchner C, Theißen G (2001) MADS-box genes are involved in floral development and evolution. Acta Biochim Pol 48:351–358

    CAS  PubMed  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Soltis DE, Ma H, Frohlich MW, Soltis PS, Albert VA, Oppenheimer DG, Altman NS, dePamphilis C, Leebens-Mack J (2007) The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression. Trends Plant Sci 12:358–367

    Article  CAS  PubMed  Google Scholar 

  • Sugiura A, Inaba A (1966) Studies on the mechanism of gibberellin-induced seedlessness of Delaware grapes. I. Effect of pre-bloom gibberellin treatment on pollen germination. J Jpn Soc Hort Sci 35:233–241

    Article  Google Scholar 

  • Theißen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85

    Article  PubMed  Google Scholar 

  • Theißen G, Saedler H (2001) Plant biology: floral quartets. Nature 409:469–471

    Article  PubMed  Google Scholar 

  • Theißen G, Kim J, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516

    Article  PubMed  Google Scholar 

  • Tsaftaris A, Pasentsis K, Makris A, Darzentas N, Polidoros A, Kalivas A, Argiriou A (2011) The study of the E-class SEPALLATA3-like MADS-box genes in wild-type and mutant flowers of cultivated saffron crocus (Crocus sativus L.) and its putative progenitors. J Plant Physiol 168:1675–1684

    Article  CAS  PubMed  Google Scholar 

  • Varoquaux F, Blanvillain R, Delseny M, Gallois P (2000) Less is better: new approaches for seedless fruit production. Trends Biotechnol 18:233–242

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Vannozzi A, Wang G, Liang Y, Tornielli GB, Zenoni S, Cavallini E, Pezzotti M, Cheng Z (2014) Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Horticulture Research. doi:10.1038/hortres.2014.16

    Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  CAS  PubMed  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci 109:1187–1192

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu Z, Zhang Q, Sun L, Du D, Cheng T, Pan H, Yang W, Wang J (2014) Genome-wide identification, characterisation and expression analysis of the MADS-box gene family in Prunus mume. Mol Genet Genomics 289:903–920

  • Yang Y, Jack T (2004) Defining subdomains of the K domain important for protein-protein interactions of plant MADS proteins. Plant Mol Biol 55:45–59

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Fanning L, Jack T (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J 33:47–59

    Article  PubMed  Google Scholar 

  • Zhang Y, Gao M, Singer S, Fei Z, Wang H, Wang X (2012) Genome-wide identification and analysis of the tify gene family in grape. PLoS One 7:e44465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao Y, Li X, Chen W, Peng X, Cheng X, Zhu S, Cheng B (2011) Whole-genome survey and characterization of MADS-box gene family in maize and sorghum. Plant Cell Tissue Organ Cult 105:159–173

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China grant no. 31272136, 948 Project from the Ministry of Agriculture of China grant no. 2012-S12 and the Program for Innovative Research Team of Grape Germplasm Resources and Breeding grant no. 2013KCT-25 to X W. We thank PlantScribe (www.plantscribe.com) for editing this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiping Wang.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 197 kb)

Supplementary material 2 (PPT 5261 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Yin, X., Cheng, C. et al. Evolutionary and expression analysis of a MADS-box gene superfamily involved in ovule development of seeded and seedless grapevines. Mol Genet Genomics 290, 825–846 (2015). https://doi.org/10.1007/s00438-014-0961-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-014-0961-y

Keywords

Navigation