Skip to main content

Candidate genes within a 143 kb region of the flower sex locus in Vitis

Abstract

Wild Vitis species are dioecious plants, while the cultivated counterpart, Vitis vinifera subspec. vinifera, generally shows hermaphroditic flowers. In Vitis the genetic determinants of flower sex have previously been mapped to a region on chromosome 2. In a combined strategy of map-based cloning and the use of the publicly available grapevine reference genome sequence, the structure of the grapevine flower sex locus has been elucidated with the subsequent identification of candidate genes which might be involved in the development of the different flower sex types. In a fine mapping approach, the sex locus in grapevine was narrowed down using a population derived from a cross of a genotype with a Vitis vinifera background (‘Schiava Grossa’ × ‘Riesling’) with the male rootstock cv. ‘Börner’ (V. riparia × V. cinerea). A physical map of 143 kb was established from BAC clones spanning the 0.5 cM region defined by the closest flanking recombination break points. Sequencing and gene annotation of the entire region revealed several candidate genes with a potential impact on flower sex formation. One of the presumed candidate genes, an adenine phosphoribosyltransferase, was analysed in more detail. The results led to the development of a marker for the presence or absence of the female alleles, while the male and hermaphroditic alleles are still to be differentiated. The impact of other candidate genes is discussed, especially with regard to plant hormone actions. The markers developed will permit the selection of female breeding lines which do not require laborious emasculation thus considerably simplifying grapevine breeding. The genetic finger prints displayed that our cultivated grapevines frequently carry a female allele while homozygous hermaphrodites are rare.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Adam-Blondon A-F, Roux C, Claux D, Butterlin G, Merdinoglu D, This R (2004) Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grape genetics. Theor Appl Genet 109:1017–1027

    PubMed  Article  CAS  Google Scholar 

  • Allen M, Qin W, Moreau F, Moffatt B (2002) Adenine phosphoribosyltransferase isoforms of Arabidopsis and their potential contributions to adenine and cytokinin metabolism. Physiol Plant 115:56–68

    PubMed  Article  CAS  Google Scholar 

  • Antcliff AJ (1980) Inheritance of sex in Vitis. Ann Amelior Plantes 30:113–122

    Google Scholar 

  • Argos P, Hanei M, Wilson JM, Kelley WN (1983) A possible nucleotide binding domain in the tertiary fold of phosphoribosyltransferases. J Biol Chem 258:6450–6457

    PubMed  CAS  Google Scholar 

  • Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18:1038–1051

    PubMed  Article  CAS  Google Scholar 

  • Boualem A, Fergany M, Fernandez R, Troadec C, Martin A, Morin H, Sari M-A, Collin F, Flowers JM, Pitrat M, Purugganan MD, Dogimont C, Bendahmane A (2008) A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321:836–338

    Google Scholar 

  • Boualem A, Troadec C, Kovalski I, Sari MA, Perl-Treves R, Bendahmane A (2009) A conserved ethylene biosynthesis enzyme leads to andromonoecy in two Cucumis species. PLoS One 4:e6144

    PubMed  Article  Google Scholar 

  • Caporali E, Spada A, Marziani G, Failla O, Scienza A (2003) The arrest of development of abortive reproductive organs in the unisexual flower of Vitis vinifera ssp. silvestris. Sex Plant Reprod 15:291–300

    Google Scholar 

  • Carbonneau A (1983) Male and female sterility in the genus Vitis. I: Modeling of their inheritance. Agronomie 3:635–644

    Article  Google Scholar 

  • Chandler JW (2011) The hormonal regulation of flower development. J Plant Growth Regul 30:242–254

    Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65:972–979

    PubMed  Article  Google Scholar 

  • Dalbó MA, Ye GN, Weeden NG, Steinkellner H, Sefc KM, Reisch BI (2000) A gene controlling sex in grapevines placed on a molecular-based genetic map. Genome 43:333–340

    PubMed  Article  Google Scholar 

  • Durand B, Durand R (1991a) Sex determination and reproductive organ differentiation in Mercurialis. Plant Sci 80:49–65

    Article  Google Scholar 

  • Durand B, Durand R (1991b) Male sterility and restored fertility in annual mercuries, relations with sex differentiation. Plant Sci 80:107–118

    Article  CAS  Google Scholar 

  • Fraser L, Tsang G, Datson P, Hilario E, Silva H, McNeilage M (2009) A mapping approach to define the genetic structure of the sex-determining locus in the dioecious species Actinidia chinensis. Acta Hortic 839:561–566

    CAS  Google Scholar 

  • Gaillard C, Moffatt BA, Blacker M, Laloue M (1998) Male sterility associated with APRT deficiency in Arabidopsis thaliana results from a mutation in the gene APT1. Mol Gen Genet 257:348–353

    PubMed  Article  CAS  Google Scholar 

  • Hansen BG, Kliebenstein DJ, Halkier BA (2007) Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 50:902–910

    PubMed  Article  CAS  Google Scholar 

  • Hedrick UP, Anthony RD (1915) Inheritance of certain characters of grapes. J Agric Res 4:315–330

    Google Scholar 

  • Hershey HV, Taylor MW (1986) Nucleotide sequence and deduced amino acid sequence of the Escherichia coli adenine phosphoribosyltransferase and comparison with other analogous enzymes. Gene 43:287–293

    PubMed  Article  CAS  Google Scholar 

  • Hove-Jensen B, Harlow KW, King CJ, Switzer RL (1986) Phosphoribosyl-pyrophosphate synthetase of Escherichia coli: properties of the purified enzyme and primary structure of the prs gene. J Biol Chem 261:6765–6771

    PubMed  CAS  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, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero 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, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P; French-Italian Public Consortium for Grapevine Genome Characterization (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin colour. Science 304:982–982

    Google Scholar 

  • Koch M, Vorwerk S, Masur C, Sharifi-Sirchi G, Olivieri N, Schlaich NL (2006) A role for a flavin-containing mono-oxygenase in resistance against microbial pathogens in Arabidopsis. Plant J 47:629–639

    PubMed  Article  CAS  Google Scholar 

  • Laloue M, Pethe C (1982) Dynamics of cytokinin metabolism in tobacco cells. In: Wearing PF (ed) Plant growth substances. Academic Press, London, pp 185–196

    Google Scholar 

  • Lemke L, Rex M, Zyprian E, Töpfer R (2011) A simple, inexpensive and environmentally friendly method for high throughput DNA extraction from grapevine (Vitis spp.). Vitis 50:7–10

    CAS  Google Scholar 

  • Li Z, Huang S, Liu S, Pan J, Zhang Z, Tao Q, Shi Q, Jia Z, Zhang W, Chen H, Si L, Zhu L, Cai R (2009) Molecular isolation of the M gene suggests that a conserved-residue conversion induces the formation of bisexual flowers in cucumber plants. Genetics 182:1381–1385

    PubMed  Article  CAS  Google Scholar 

  • Lijavetzky D, Ruiz-García L, Cabezas JA, De Andrés MT, Bravo G, Ibáñez A, Carreño J, Cabello F, Ibáñez J, Martínez-Zapater JM (2006) Molecular genetics of berry colour variation in table grape. Mol Gen Genomics 276:427–435

    Article  CAS  Google Scholar 

  • Lowe KM, Walker MA (2006) Genetic map of the interspecific grape rootstock cross Ramsey (Vitis champinii) × Riparia Gloire (Vitis riparia). Theor Appl Genet 112:1582–1592

    PubMed  Article  CAS  Google Scholar 

  • Lu C, Jeong D-H, Kulkarni K, Pillay M, Nobuta K, German R,Thatcher SR, Maher C, Zhang L, Ware D, Liu B, Cao X, Meyers BC, Green PJ (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci USA 105:4951–4956

    Google Scholar 

  • Marguerit E, Boury C, Manicki A, Donnart M, Butterlin G, Némorin A, Wiedemann-Merdinoglu S, Merdinoglu D, Ollat N, Decroocq S (2009) Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 118:1261–1278

    PubMed  Article  Google Scholar 

  • Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461:1135–1139

    PubMed  Article  CAS  Google Scholar 

  • Mishina TE, Zeier J (2006) The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol 141:1666–1675

    PubMed  Article  CAS  Google Scholar 

  • Moffatt BA, Somerville C (1988) Positive selection for male-sterile mutants of Arabidopsis lacking adenine phosphoribosyltransferase activity. Plant Physiol 86:1150–1154

    PubMed  Article  CAS  Google Scholar 

  • Moffatt BA, Pethe C, Laloue M (1991) Metabolism of benzyladenine is impaired in a mutant of Arabidopsis thaliana lacking adenine phosphoribosyltransferase activity. Plant Physiol 95:900–908

    PubMed  Article  CAS  Google Scholar 

  • Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    PubMed  Article  CAS  Google Scholar 

  • Negi SS, Olmo HP (1966) Sex conversion in a male Vitis vinifera L. by a kinin. Science 152:1624–1625

    PubMed  Article  CAS  Google Scholar 

  • Negi SS, Olmo HP (1971) Induction of sex conversion in male Vitis. Vitis 10:1–19

    Google Scholar 

  • Riaz S, Dangl GS, Edwards KJ, Meredith CP (2004) A microsatellite marker based framework linkage map of Vitis vinifera L. Theor Appl Genet 108:864–887

    PubMed  Article  CAS  Google Scholar 

  • Riaz S, Krivanek AF, Xyu K, Walker MA (2006) Refined mapping of the Pierce’s disease resistance locus, PdR1, and Sex on an extended genetic map of Vitis rupestris × V. arizonica. Theor Appl Genet 113:1317–1329

    PubMed  Article  CAS  Google Scholar 

  • Telgmann-Rauber A, Jamsari A, Kinney MS, Pires JC, Jung C (2007) Genetic and physical maps around the sex-determining M-locus of the dioecious plant asparagus. Mol Gen Genomics 278:221–234

    Article  CAS  Google Scholar 

  • Valleau WD (1916) Inheritance of sex in the grape. Am Nat 50:554–564

    Article  Google Scholar 

  • Van Ooijen JW (2006) JoinMap®4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., Wageningen, The Netherlands

  • Wu T, Qin Z, Zhou X, Feng Z, Du Y (2010) Transcriptome profile analysis of floral sex determination in cucumber. J Plant Physiol 167:905–913

    PubMed  Article  CAS  Google Scholar 

  • Xing Q, Ru Z, Li J, Zhou C, Jin D, Sun Y, Wang B (2005) Cloning a second form of adenine phosphoribosyl transferase gene (TaAPT2) from wheat and analysis of its association with thermo-sensitive genic male sterility (TGMS). Plant Sci 169:37–45

    Article  CAS  Google Scholar 

  • Zhang C, Guinel F, Moffatt BA (2002) A comparative ultrastructural study of pollen development in Arabidopsis thaliana wild type and an APT1-deficient mutant. Protoplasma 219:59–71

    PubMed  Article  Google Scholar 

  • Zhang J, Hausmann L, Eibach R, Welter L, Toepfer R, Zyprian E (2009) A framework map from grapevine V3125 (Vitis vinifera ‘Schiava grossa’ × ‘Riesling’) × rootstock cultivar ‘Börner’ (Vitis riparia × Vitis cinerea) to localize genetic determinants of phylloxera root resistance. Theor Appl Genet 119:1039–1051

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Zhou C-J, Li J, Zou J-C, Liang F-S, Ye C-J, Jin D-M, Wenig M-L, Wang B (2006) Cloning and characterization of a second form of the rice adenine phosphoribosyl transferase gene (OsAPT2) and its association with TGMS. Plant Mol Biol 60:365–376

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully thank the German Federal Ministry of Education and Research (BMBF) for funding this project (grant no. 0315460A and 0315460B). Our further thanks go to Andreas Preiss for technical assistance, Dr. Rudolf Eibach and his team, Dr. Erika Maul, and Friederike Rex for helpful discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Iris Fechter.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 209 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fechter, I., Hausmann, L., Daum, M. et al. Candidate genes within a 143 kb region of the flower sex locus in Vitis . Mol Genet Genomics 287, 247–259 (2012). https://doi.org/10.1007/s00438-012-0674-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-012-0674-z

Keywords

  • Vitis
  • Flower sex
  • Candidate genes
  • Plant hormones