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Plant Molecular Biology

, Volume 91, Issue 1–2, pp 67–80 | Cite as

Expression of grapevine AINTEGUMENTA-like genes is associated with variation in ovary and berry size

  • Constanza Chialva
  • Estefanía Eichler
  • Cecilia Grissi
  • Claudio Muñoz
  • Sebastian Gomez-Talquenca
  • José M. Martínez-Zapater
  • Diego LijavetzkyEmail author
Article

Abstract

Fruit size is a highly important trait for most fruit and vegetable crops. This trait has been a main selection target and could be involved in divergent selection processes leading to the differentiation between modern table and wine cultivars. Even though its determination is highly influenced by cultural practices, several regions within the grapevine genome have been identified affecting berry size, either directly or indirectly through their effect on seed content. Using grapevine seeded cultivars, we have analyzed the relationship between ovary cell number and the final size of ovaries and berry fruits. We also performed the characterization of the grapevine AINTEGUMENTA-LIKE family, since it is well reported in Arabidopsis that AINTEGUMENTA (ANT) regulates cell proliferation and organ growth in flower organ primordia by maintaining the meristematic competence of cells during organogenesis. Here we show that orthologous grapevine gene expression associate with flower developmental stages suggesting a similar biological role for this gene family in this species. Moreover, we detected a correlation between those organs size and the level of expression of VviANT1 the grapevine homolog of AtANT. This grapevine gene also co-localizes in linkage group 18 with the confidence interval of a previously detected QTL for berry size. Thus our results suggest the involvement of ANT in the regulation of berry size in grapevine.

Keywords

Berry size Cell division Gene expression Ovary size Vitis vinifera AINTEGUMENTA 

Notes

Acknowledgments

We thank Javier Ibañez for his helpful comments and invaluable data, Gerome Grimplet for nomenclature advice and Dante Gamboa for helping us with the histological analysis. This work was funded by The National Agency for Science and Technology Promotion (PICT-2008-00270 and PAE-PICT-2007-02360) and National University of Cuyo (SECTyP-A504A/11 and 06/A587) grants to D.L. Authors would like also to thank COST action FA1106 “Quality fruit”.

Supplementary material

11103_2016_443_MOESM1_ESM.pdf (1.8 mb)
Supplementary material 1 (PDF 1821 kb)

References

  1. Aida M, Beis D, Heidstra R et al (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120CrossRefPubMedGoogle Scholar
  2. Alercia A, Becher R, Boursiquot JM et al (2009) OIV Descriptor list for grape varieties and Vitis species, 2nd edn. The International Organisation of Vine and Wine, ParisGoogle Scholar
  3. Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250CrossRefPubMedGoogle Scholar
  4. Auge GA, Rugnone ML, Cortés LE et al (2012) Phytochrome A increases tolerance to high evaporative demand. Physiol Plant 146:228–235CrossRefPubMedGoogle Scholar
  5. Baggiolini M (1952) Les stades repe`res dans le developpement annuel de la vigne et leur utilisation pratique. Rev Rom Agric Vitic Arbor 8:4–6Google Scholar
  6. Bandupriya HDD, Gibbings JG, Dunwell JM (2013) Isolation and characterization of an AINTEGUMENTA-like gene in different coconut (Cocos nucifera L.) varieties from Sri Lanka. Tree Genet Genomes 9:813–827CrossRefGoogle Scholar
  7. Boutilier K, Offringa R, Sharma VK et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cabezas JA, Cervera MT, Ruiz-Garcia L et al (2006) A genetic analysis of seed and berry weight in grapevine. Genome 49:1572–1585CrossRefPubMedGoogle Scholar
  9. Carbonell-Bejerano P, Santa María E, Torres-Pérez R et al (2013) Thermotolerance responses in ripening berries of Vitis vinifera L. cv Muscat Hamburg. Plant Cell Physiol 54:1200–1216CrossRefPubMedGoogle Scholar
  10. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585CrossRefPubMedGoogle Scholar
  11. Conde C, Silva P, Fontes N et al (2007) Biochemical changes throughout grape berry development and fruit and wine quality. Food 1:1–22Google Scholar
  12. Coombe BG (1973) The regulation of set and development of the grape berry. Acta Hortic. International Society for Horticultural Science (ISHS), Leuven, Belgium, pp 261–274Google Scholar
  13. Coombe BG (1992) Research on development and ripening of the grape berry. Am J Enol Vitic 43:101–110Google Scholar
  14. Costantini L, Battilana J, Lamaj F et al (2008) Berry and phenology-related traits in grapevine (Vitis vinifera L.): from quantitative trait loci to underlying genes. BMC Plant Biol 8:38CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dash M, Malladi A (2012) The AINTEGUMENTA genes, MdANT1 and MdANT2, are associated with the regulation of cell production during fruit growth in apple (Malus × domestica Borkh). BMC Plant Biol 12:98CrossRefPubMedPubMedCentralGoogle Scholar
  16. Di Rienzo JA, Casanoves F, Balzarini MG et al (2011) InfoStat versión 2011Google Scholar
  17. Diaz-Riquelme J, Lijavetzky D, Martinez-Zapater JM, Carmona MJ (2009) Genome-wide analysis of MIKCC-type MADS box genes in grapevine. Plant Physiol 149:354–369CrossRefPubMedPubMedCentralGoogle Scholar
  18. Doligez A, Bouquet A, Danglot Y et al (2002) Genetic mapping of grapevine (Vitis vinifera L.) applied to the detection of QTLs for seedlessness and berry weight. Theor Appl Genet 105:780–795CrossRefPubMedGoogle Scholar
  19. Doligez A, Bertrand Y, Farnos M et al (2013) New stable QTLs for berry weight do not colocalize with QTLs for seed traits in cultivated grapevine (Vitis vinifera L.). BMC Plant Biol 13:217CrossRefPubMedPubMedCentralGoogle Scholar
  20. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  21. Elliott RC, Betzner AS, Huttner E et al (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168CrossRefPubMedPubMedCentralGoogle Scholar
  22. Esau K (1977) Anatomy of seed plants. Wiley, New YorkGoogle Scholar
  23. Fasoli M, Dal Santo S, Zenoni S et al (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell. doi: 10.1105/tpc.112.100230 PubMedPubMedCentralGoogle Scholar
  24. Fernandez L, Romieu C, Moing A et al (2006) The grapevine fleshless berry mutation. A unique genotype to investigate differences between fleshy and nonfleshy fruit. Plant Physiol 140:537CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fernandez L, Chaïb J, Martinez-Zapater J-M et al (2013) Mis-expression of a PISTILLATA-like MADS box gene prevents fruit development in grapevine. Plant J 73:918–928CrossRefPubMedGoogle Scholar
  26. Fischer BM, Salakhutdinov I, Akkurt M et al (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515CrossRefPubMedGoogle Scholar
  27. Galinha C, Hofhuis H, Luijten M et al (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057CrossRefPubMedGoogle Scholar
  28. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl):S170–S180CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gray JD, Coombe BG (2009) Variation in Shiraz berry size originates before fruitset but harvest is a point of resynchronisation for berry development after flowering. Aust J Grape Wine Res 15:156–165CrossRefGoogle Scholar
  30. Grimplet J, Adam-Blondon A-F, Bert P-F et al (2014) The grapevine gene nomenclature system. BMC Genom 15:1077CrossRefGoogle Scholar
  31. Horstman A, Willemsen V, Boutilier K, Heidstra R (2014) AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks. Trends Plant Sci 19:146–157CrossRefPubMedGoogle Scholar
  32. Houel C, Martin-Magniette M-L, Nicolas SD et al (2013) Genetic variability of berry size in the grapevine (Vitis vinifera L.). Aust J Grape Wine Res 19:208–220CrossRefGoogle Scholar
  33. Houel C, Chatbanyong R, Doligez A et al (2015) Identification of stable QTLs for vegetative and reproductive traits in the microvine (Vitis vinifera L.) using the 18 K Infinium chip. BMC Plant Biol 15:205CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467CrossRefPubMedGoogle Scholar
  35. Jofuku KD (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jung S, Ficklin SP, Lee T et al (2014) The genome database for rosaceae (GDR): year 10 update. Nucleic Acids Res 42:D1237–D1244CrossRefPubMedPubMedCentralGoogle Scholar
  37. Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153CrossRefPubMedPubMedCentralGoogle Scholar
  38. Krizek BA (1999) Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs. Dev Genet 25:224–236CrossRefPubMedGoogle Scholar
  39. Krizek BA (2003) AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain. Nucleic Acids Res 31:1859–1868CrossRefPubMedPubMedCentralGoogle Scholar
  40. Krizek BA, Sulli C (2006) Mapping sequences required for nuclear localization and the transcriptional activation function of the Arabidopsis protein AINTEGUMENTA. Planta 224:612–621CrossRefPubMedGoogle Scholar
  41. Ledbetter CA, Burgos L (1994) Inheritance of stenospermocarpic seedlessness in Vitis vinifera L. J Hered 85:157–160Google Scholar
  42. Licausi F, Giorgi FM, Zenoni S et al (2010) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genom 11:719CrossRefGoogle Scholar
  43. Lijavetzky D, Almagro L, Belchi-Navarro S et al (2008) Synergistic effect of methyljasmonate and cyclodextrin on stilbene biosynthesis pathway gene expression and resveratrol production in Monastrell grapevine cell cultures. BMC Res Notes 1:132CrossRefPubMedPubMedCentralGoogle Scholar
  44. Litt A (2007) An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int J Plant Sci 168:73–91CrossRefGoogle Scholar
  45. Liu J, Chen N, Chen F et al (2014) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genom 15:281CrossRefGoogle Scholar
  46. Ma W, Kong Q, Arondel V et al (2013) WRINKLED1, a ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp. PLoS ONE 8:e68887CrossRefPubMedPubMedCentralGoogle Scholar
  47. Masaki T, Mitsui N, Tsukagoshi H et al (2005) ACTIVATOR of Spomin:LUC1/WRINKLED1 of Arabidopsis thaliana transactivates sugar-inducible promoters. Plant Cell Physiol 46:547–556CrossRefPubMedGoogle Scholar
  48. Mejia N, Gebauer M, Munoz L et al (2007) Identification of QTLs for seedlessness, berry size, and ripening date in a seedless × seedless table grape progeny. Am J Enol Vitic 58:499–507Google Scholar
  49. Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947CrossRefPubMedPubMedCentralGoogle Scholar
  50. Myles S, Boyko AR, Owens CL et al (2011) Genetic structure and domestication history of the grape. Proc Natl Acad Sci 108:3530–3535CrossRefPubMedPubMedCentralGoogle Scholar
  51. Nicolas P, Lecourieux D, Gomès E et al (2013) The grape berry-specific basic helix–loop–helix transcription factor VvCEB1 affects cell size. J Exp Bot 64:991–1003CrossRefPubMedPubMedCentralGoogle Scholar
  52. Nole-Wilson S, Krizek BA (2000) DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA. Nucleic Acids Res 28:4076–4082CrossRefPubMedPubMedCentralGoogle Scholar
  53. Nole-Wilson S, Tranby TL, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57:613–628CrossRefPubMedGoogle Scholar
  54. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182CrossRefPubMedPubMedCentralGoogle Scholar
  55. Okamuro JK, Caster B, Villarroel R et al (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci 94:7076–7081CrossRefPubMedPubMedCentralGoogle Scholar
  56. Reeves PH, Ellis CM, Ploense SE et al (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8:e1002506CrossRefPubMedPubMedCentralGoogle Scholar
  57. Reid KE, Olsson N, Schlosser J et al (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27CrossRefPubMedPubMedCentralGoogle Scholar
  58. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedGoogle Scholar
  59. Rigal A, Yordanov YS, Perrone I et al (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sasaki T, Burr B (2000) International Rice Genome Sequencing Project: the effort to completely sequence the rice genome. Curr Opin Plant Biol 3:138–141CrossRefPubMedGoogle Scholar
  61. Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208CrossRefPubMedGoogle Scholar
  62. Tamura K, Stecher G, Paterson D et al (2013) MEGA6: molecular evolutionary genetics analysis software version 6.0. Comput Appl Biosci 30:2725–2729Google Scholar
  63. Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16:S181–S189CrossRefPubMedPubMedCentralGoogle Scholar
  64. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  65. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604CrossRefPubMedGoogle Scholar
  66. Vitulo N, Forcato C, Carpinelli EC et al (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol 14:99CrossRefPubMedPubMedCentralGoogle Scholar
  67. Yang HF, Kou YP, Gao B et al (2014) Identification and functional analysis of BABY BOOM genes from Rosa canina. Biol Plant 58:427–435CrossRefGoogle Scholar
  68. Zhuang J, Peng R-H, Cheng Z-M et al (2009) Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. Sci Hortic (Amsterdam) 123:73–81CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Constanza Chialva
    • 1
  • Estefanía Eichler
    • 1
  • Cecilia Grissi
    • 1
  • Claudio Muñoz
    • 1
  • Sebastian Gomez-Talquenca
    • 2
  • José M. Martínez-Zapater
    • 3
  • Diego Lijavetzky
    • 1
    Email author
  1. 1.Instituto de Biología Agrícola de Mendoza (IBAM), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Universidad Nacional de Cuyo (FCA-UNCuyo)Chacras de CoriaArgentina
  2. 2.Plant Virology LaboratoryEEA Mendoza INTALuján de CuyoArgentina
  3. 3.Instituto de Ciencias de la Vid y del Vino (CSIC-Universidad de La Rioja-Gobierno de La Rioja)LogroñoSpain

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