New stable QTLs for berry weight do not colocalize with QTLs for seed traits in cultivated grapevine (Vitis vinifera L.)

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Doligez, Agnès ^a   Bertrand, Yves ^a   Farnos, Marc ^a   Grolier, Michel ^a   Romieu, Charles ^a   Esnault, Florence ^a   Dias, Sonia ^a   Berger, Gilles ^a   François, Pierre ^a   Pons, Thierry ^a   Ortigosa, Patrick ^a   Roux, Catherine ^a   Houel, Cléa ^a   Laucou, Valérie ^a   Bacilieri, Roberto ^a   Péros, Jean Pierre ^a   This, Patrice ^a  

^a UMR AGAP   (France)

Author keywords

Berry weight; Candidate gene; Grapevine; QTL; Quantitative trait locus; Seed number; Seed weight; Vitis vinifera

Indexed keywords

LYCOPERSICON ESCULENTUM; VITACEAE; VITIS; VITIS VINIFERA;

ARTICLE; CHROMOSOME MAP; FRUIT; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHERITANCE; ORGAN SIZE; PHENOTYPE; PLANT SEED; QUANTITATIVE TRAIT; QUANTITATIVE TRAIT LOCUS; VITIS;

CHROMOSOME MAPPING; FRUIT; GENETIC ASSOCIATION STUDIES; INHERITANCE PATTERNS; LOD SCORE; ORGAN SIZE; PHENOTYPE; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; SEEDS; VITIS;

EID: 84890353492     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-217     Document Type: Article

References (106)

1. 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, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449:463-467. 10.1038/nature06148, 17721507.
2. Velasco R, Zharkikh A, Troggio M, Carthwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald 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, Demattè L, Mraz A, et al. A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2007, 12:e1326.
3. Boursiquot JM, Dessup M, Rennes C. Distribution des principaux caractères phénologiques, agronomiques et technologiques chez Vitis vinifera L. Vitis 1995, 34:31-35.
4. Houel C, Martin-Magniette ML, Nicolas SD, Lacombe T, Le Cunff L, Franck D, Torregrosa L, Conéjéro G, Lalet S, This P, Adam-Blondon AF. Genetic variability of berry size in the grapevine (Vitis vinifera L.). Aust J Grape Wine Res 2013, 19:208-220.
5. Coombe BG. The development of fleshy fruits. Annu Rev Plant Physiol 1976, 27:507-528.
6. Mullins MG, Bouquet A, Williams LE. Developmental physiology: flowering and fruiting. Biology of the grapevine 1992, 112-146. Cambridge: University Press, Mullins MG, Bouquet A, Williams LE.
7. Ojeda H, Deloire A, Carbonneau A, Ageorges A, Romieu C. Berry development of grapevines: relations between the growth of berries and their DNA content indicate cell multiplication and enlargement. Vitis 1999, 38:145-150.
8. Friend AP, Trought MCT, Creasy GL. The influence of seed weight on the development and growth of berries and live green ovaries in Vitis vinifera L. cvs. Pinot Noir and Cabernet Sauvignon. Aust J Grape Wine Res 2009, 15:166-174.
9. Ollat N, Diakou-Verdin P, Carde JP, Barrieu F, Gaudillère JP, Moing A. Grape berry development: a review. J Int Sci Vigne Vin 2002, 36:109-131.
10. Chervin C, El-Kereamy A, Roustan JP, Latche A, Lamon J, Bouzayen M. Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 2004, 167:1301-1305.
11. Chervin C, Tira-umphon A, Terrier N, Zouine M, Severac D, Roustan JP. Stimulation of the grape berry expansion by ethylene and effects on related gene transcripts, over the ripening phase. Physiol Plant 2008, 134:534-546. 10.1111/j.1399-3054.2008.01158.x, 18785902.
12. Davies C, Boss PK, Robinson SP. Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 1997, 115:1155-1161. 158580, 12223864.
13. Scienza A, Miravallec C, Fregoni M. Relationship between seed number, gibberellin and abcissic acid levels and ripening in Cabernet Sauvignon grape berries. Vitis 1978, 17:361-368.
14. Moreno D, Berli F, Piccoli P, Bottini R. Gibberellins and abscisic acid promote carbon allocation in roots and berries of grapevines. J Plant Growth Regul 2011, 30:220-228.
15. Cadot Y, Miñana-Castelló MT, Chevalier M. Anatomical, histological, and histochemical changes in grape seeds from Vitis vinifera L. cv cabernet franc during fruit development. J Agric Food Chem 2006, 54:9206-9215. 10.1021/jf061326f, 17117811.
16. Ledbetter CA, Ramming DW. Seedlessness in grapes. Horticultural Review 1989, 11:159-184.
17. Striem MJ, Ben-Hayyim G, Spiegel-Roy P. Identifying molecular genetic markers associated with seedlessness in grape. J Am Soc Hortic Sci 1996, 121:758-763.
18. Staudt G, Schneider W, Leidel J. Phases of berry growth in Vitis vinifera. Ann Bot 1986, 58:789-800.
19. Boselli M, Volpe B, Di Vaio C. Effect of seed number per berry on mineral composition of grapevine (Vitis vinifera L.) berries. J Hortic Sci 1995, 70:509-515.
20. Ebadi A, May P, Coombe BG. Effect of short-term temperature and shading on fruit-set, seed and berry development in model vines of V. vinifera, cvs Chardonnay and Shiraz. Aust J Grape Wine Res 1996, 2:2-9.
21. May P. From bud to berry, with special reference to inflorescence and bunch morphology in Vitis vinifera L. Aust J Grape Wine Res 2000, 6:82-98.
22. Petrie PR, Trought MCT, Howell GS. Fruit composition and ripening of Pinot Noir (Vitis vinifera L.) in relation to leaf area. Aust J Grape Wine Res 2000, 6:46-51.
23. Walker RR, Deidre HB, Clingeleffer PR, Kerridge GH, Rühl EH, Nicholas PR. Shiraz berry size in relation to seed number and implications for juice and wine composition. Aust J Grape Wine Res 2005, 11:2-8.
24. Wagner R, Antcliff J. A study of sexual progenies of Bicane x Sultanina (Vitis vinifera L.): evidence for genetic differences between Sultana clones in berry weight. Proceedings of the IIIrd Symposium on Grape Genetics and Breeding 1980, 65-77.
25. Doligez A, Bouquet A, Danglot Y, Lahogue F, Riaz S, Meredith CP, Edwards KJ, This P. Genetic mapping of grapevine (Vitis vinifera L.) applied to the detection of QTLs for seedlessness and berry weight. Theor Appl Genet 2002, 105:780-795. 10.1007/s00122-002-0951-z, 12582493.
26. Fanizza G, Lamaj F, Costantini L, Chaabane R. QTL analysis for fruit yield components in table grapes (Vitis vinifera). Theor Appl Genet 2005, 111:658-664. 10.1007/s00122-005-2016-6, 15995866.
27. Cabezas JA, Cervera MT, Ruiz-Garcia L, Carreño J, Martinez-Zapater JM. A genetic analysis of seed and berry weight in grapevine. Genome 2006, 49:1572-1585. 10.1139/g06-122, 17426772.
28. Mejia N, Gebauer M, Muñoz L, Hewstone N, Muñoz C, Hinrichsen P. Identification of QTLs for seedlessness, berry size, and ripening date in a seedless x seedless table grape progeny. Am J Enol Vitic 2007, 58:499-507.
29. Costantini L, Battilana J, Lamaj F, Fanizza G, Grando MS. Berry and phenology-related traits in grapevine (Vitis vinifera L.): from quantitative trait loci to underlying genes. BMC Plant Biol 2008, 8:38. 10.1186/1471-2229-8-38, 2395262, 18419811.
30. Meijia N, Soto B, Guerrero M, Casanueva X, Houel C, De los Angeles Miccono M, Ramos R, Le Cunff L, Boursiquot JM, Hinrichsen P, Adam-Blondon AF. Molecular, genetic and transcriptional evidence for a role of VvaGL11 in stenospermocarpic seedlessness in grapevine. BMC Plant Biol 2011, 11:57. 10.1186/1471-2229-11-57, 3076230, 21447172.
31. Wei X, Sykes SR, Clingeleffer PR. An investigation to estimate genetic parameters in CSIRO's table grape breeding program 2: quality characteristics. Euphytica 2002, 128:343-351.
32. Ebadi A, Moghadam JE, Fatahi R. Evaluation of 22 populations achieved from controlled crossing between some seeded x seedless grapevine cultivars. Sci Hortic 2009, 119:371-376.
33. Wagner R. Study of phenotypic variation by analysing data gathered together by O.I.V. on new varieties of table grapes. Proceedings of the Vth Symposium on Grape Genetics and Breeding 1989, 178-186.
34. Coombe BG. Relationship of growth and development to changes in sugars, auxins, and gibberellins in fruit of seeded and seedless varieties of Vitis vinifera. Plant Physiol 1960, 35:241-250. 10.1104/pp.35.2.241, 405950, 16655336.
35. Perez FJ, Viani C, Retamales J. Bioactive gibberellins in seeded and seedless grapes: identification and changes in content during berry development. Am J Enol Vitic 2000, 51:315-318.
36. Weaver RJ, Pool RM. Relation of seededness and ringing to gibberellin-like activity in berries of Vitis vinifera. Plant Physiol 1965, 40:770-776. 10.1104/pp.40.4.770, 550375, 16656155.
37. Considine JA, Coombe BG. The interaction of gibberellic acid and 2-(chloroethyl) trimethyl ammonium chloride on fruit cluster development in Vitis vinifera L. (m. dt. Zus.). Vitis 1972, 11:108-123.
38. Eibach R. Investigations about the influence of some physiological and phenological characteristics on quality and their heredity. Proceedings of the Vth Symposium on Grape Genetics and Breding 1989, 149-158.
39. Daulta BS, Bakhshi JC, Chandra S. Evaluation of vinifera varieties for genotypic and phenotypic variability. Indian J Hortic 1972, 29:150-157.
40. Golodriga PI, Trochine LP. Héritabilité des caractères quantitatifs chez la vigne. Proceedings of the IInd Symposium on Grape Genetics and Breeding 1978, 113-117.
41. Firoozabady E, Olmo HP. Heritability and correlation studies of certain quantitative traits in table grapes, Vitis spp. Vitis 1987, 26:132-146.
42. Singh R, Jalikop SH. Studies on variability in grape. Indian J Hortic 1986, 43:207-215.
43. Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R, Zyprian EM. Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 2004, 108:501-515. 10.1007/s00122-003-1445-3, 14574452.
44. Houel C, Bounon R, Chaïb J, Guichard C, Péros JP, Bacilieri R, Dereeper A, Canaguier A, Lacombe T, N'Diaye A, Le Paslier MC, Vernerey MS, Coriton O, Brunel D, This P, Torregrosa L, Adam-Blondon AF. Patterns of sequence polymorphism in the fleshless berry locus in cultivated and wild Vitis vinifera accessions. BMC Plant Biol 2010, 10:284. 10.1186/1471-2229-10-284, 3022909, 21176183.
45. Houel C. Caractérisation de la variation phénotypique de la taille de la baie chez la vigne Vitis vinifera L. et approches de génétique d'association et recherche de traces de sélection pour ce caractère. PhD thesis 2011, Université d'Evry Val d'Essonne, France, Ecole doctorale des Génomes aux Organismes.
46. Bouquet A, Danglot Y. Inheritance of seedlessness in grapevine (Vitis vinifera L.). Vitis 1996, 35:35-42.
47. Doligez A, Audiot E, Baumes R, This P. QTLs for muscat flavor and monoterpenic odorant content in grapevine (Vitis vinifera L.). Mol Breed 2006, 18:109-125.
48. Doligez A, Bertrand Y, Dias S, Grolier M, Ballester JF, Bouquet A, This P. QTLs for fertility in table grape (Vitis vinifera L.). Tree Genet Genomes 2010, 6:413-422.
49. Huang YF, Doligez A, Fournier-Level A, Le Cunff L, Bertrand Y, Canaguier A, Morel C, Miralles V, Veran F, Souquet JM, Cheynier V, Terrier N, This P. Dissecting genetic architecture of grape proanthocyanidin composition through quantitative trait locus mapping. BMC Plant Biol 2012, 12:30. 10.1186/1471-2229-12-30, 3312867, 22369244.
50. R Development Core Team R: a language and environment for statistical computing 2011, Vienna, Austria: R Foundation for Statistical Computing, ISBN 3-900051-07-0, URL http://www.R-project.org/, R Development Core Team.
51. Royston P. Remark AS R94: a remark on algorithm AS 181: the W test for normality. Appl Stat 1995, 44:547-551.
52. Wang S, Basten CJ, Zeng ZB. Windows QTL Cartographer 2.0. User Manual. 2004, Department of Statistics, North Carolina State University, http://statgen.ncsu.edu/qtlcart/WinQTLCart.pdf.
53. Basten CJ, Weir BS, Zeng ZB. Zmap-a QTL cartographer. Proceedings of the 5th World Congress on Genetics Applied to Livestock Production: Computing Strategies and Software 1994, 65-66. Guelph, Ontario, Canada: Organizing Committee of the 5th World Congress on Genetics Applied to Livestock Production, Smith C, Gavora JS, Benkel B, Chesnais J, Fairfull W, Gibson JP, Kennedy BW, Burnside EB.
54. Basten CJ, Weir BS, Zeng ZB. QTL Cartographer, Version 1.17: a Reference Manual and Tutorial for QTL Mapping. 2003, Raleigh, NC: Department of Statistics, North Carolina State University.
55. Van Ooijen JW, Maliepaard C. MapQTLTM version 3.0: Software for the calculation of QTL positions on genetic maps. 1996, CPRO-DLO, http://www.kyazma.nl/index.php/mc.MapQTL/.
56. Segura V, Denancé C, Durel C, Costes E. Wide range QTL analysis for complex architectural traits in a 1-year-old apple progeny. Genome 2007, 50:159-171. 10.1139/G07-002, 17546081.
57. De Franceschi P, Stegmeir T, Cabrera A, van der Knaap E, Rosyara UR, Sebolt AM, Dondini L, Dirlewanger E, Quero-Garcia J, Campoy JA, Iezzoni AF. Cell number regulator genes in Prunus provide candidate genes for the control of fruit size in sweet and sour cherry. Mol Breeding 2013, 32:311-326.
58. Chakrabarti M, Zhang N, Sauvage C, Muños S, Blanca J, Cañizares J, Diez MJ, Schneider R, Mazourek M, McClead J, Causse M, van der Knaap E. A cytochrome P450 regulates a domestication trait in cultivated tomato. P Natl Acad Sci USA 2013, 110:17125-17130.
59. Price AH. Believe it or not, QTLs are accurate!. Trends Plant Sci 2006, 11:213-216. 10.1016/j.tplants.2006.03.006, 16617032.
60. Guo M, Rupe MA, Dieter JA, Zou JJ, Spielbauer D, Duncan KE, Howard RJ, Hou ZL, Simmons CR. Cell number regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 2010, 22:1057-1073. 10.1105/tpc.109.073676, 2879740, 20400678.
61. Poupin M, Federici F, Medina C, Matus J, Timmermann T, Arce-Johnson P. Isolation of the three grape sub-lineages of B-class MADS-box TM6, PISTILLATA and APETALA3 genes which are differentially expressed during flower and fruit development. Gene 2007, 404:10-24. 10.1016/j.gene.2007.08.005, 17920788.
62. Fernandez L, Torregrosa L, Terrier N, Sreekantan L, Grimplet J, Davies C, Thomas MR, Romieu C, Ageorges A. Identification of genes associated with flesh morphogenesis during grapevine fruit development. Plant Mol Biol 2007, 63:307-323. 10.1007/s11103-006-9090-2, 17268889.
63. Schlosser J, Olsson N, Weis M, Reid K, Peng F, Lund S, Bowen P. Cellular expansion and gene expression in the developing grape (Vitis vinifera L.). Protoplasma 2008, 232:255-265. 10.1007/s00709-008-0280-9, 18421552.
64. Lijavetzky D, Carbonell-Bejerano P, Grimplet J, Bravo G, Flores P, Fenoll J, Hellin P, Oliveros J, Martinez-Zapater J. Berry flesh and skin ripening features in Vitis vinifera as assessed by transcriptional profiling. PLoS ONE 2012, 7:e39547. 10.1371/journal.pone.0039547, 3386993, 22768087.
65. Guillaumie S, Fouquet R, Kappel C, Camps C, Terrier N, Moncomble D, Dunlevy J, Davies C, Boss P, Delrot S. Transcriptional analysis of late ripening stages of grapevine berry. BMC Plant Biol 2011, 11:165. 10.1186/1471-2229-11-165, 3233516, 22098939.
66. Nunan KJ, Davies C, Robinson SP, Fincher GB. Expression patterns of cell wall-modifying enzymes during grape berry development. Planta 2001, 214:257-264. 10.1007/s004250100609, 11800390.
67. Boss PK, Sensi E, Hua C, Davies C, Thomas MR. Cloning and characterisation of grapevine (Vitis vinifera L.) MADS-box genes expressed during inflorescence and berry development. Plant Sci 2002, 162:887-895.
68. Yang G, Cao X, Fang J, Huang Z, Tao J, Wang C. Sub-cellular localization and expression analysis of genes involved in grapevine floral development. Sci Agric Sin 2011, 44:641-650.
69. Frary A, Nesbitt TC, Frary A, Grandillo S, van der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 2000, 289:85-88. 10.1126/science.289.5476.85, 10884229.
70. Segura V, Durel C, Costes E. Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: QTL mapping. Tree Genet Genomes 2009, 5:165-179.
71. Fournier-Level A, Le Cunff L, Gomez C, Doligez A, Ageorges A, Roux C, Bertrand Y, Souquet JM, Cheynier V, This P. Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L. ssp. sativa) berry: a quantitative trait locus to quantitative trait nucleotide integrated study. Genetics 2009, 183:1127-1139. 10.1534/genetics.109.103929, 2778965, 19720862.
72. Duchene E, Butterlin G, Dumas V, Merdinoglu D. Towards the adaptation of grapevine varieties to climate change: QTLs and candidate genes for developmental stages. Theor Appl Genet 2012, 124:623-635. 10.1007/s00122-011-1734-1, 22052019.
73. Broman KW, Wu H, Sen T, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics 2003, 19:889-890. 10.1093/bioinformatics/btg112, 12724300.
74. Dalbo MA, Ye GN, Weeden NF, Steinkellner H, Sefc KM, Reisch BI. A gene controlling sex in grapevines placed on a molecular marker-based genetic map. Genome 2000, 43:333-340. 10.1139/g99-136, 10791822.
75. Lowe KM, Walker MA. Genetic linkage map of the interspecific grape rootstock cross Ramsey (Vitis champinii) x Riparia Gloire (Vitis riparia). Theor Appl Genet 2006, 112:1582-1592. 10.1007/s00122-006-0264-8, 16607514.
76. Riaz S, Krivanek AF, Xu K, Walker MA. Refined mapping of Pierce's disease resistance locus, PdR1, and sex on an extended genetic map of Vitis rupestris x V. arizonica. Theor Appl Genet 2006, 113:1317-1329. 10.1007/s00122-006-0385-0, 16960717.
77. Marguerit E, Boury C, Manicki A, Donnart M, Butterlin G, Nemorin A, Wiedemann-Merdinoglu S, Merdinoglu D, Ollat N, Decroocq S. Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 2009, 118:1261-1278. 10.1007/s00122-009-0979-4, 19238349.
78. Appazova AO. Induction of parthenocarpy in grape. Doklady TSKhA 1977, 231:102-105.
79. Uzun I, Agaoglu S, Soylemezoglu G. Ampelographic characteristics and isozymic analysis of wild grapevines (Vitis vinifera ssp. silvestris Gmel.) in southwestern Turkey. Proceedings of the International symposium on in situ conservation of plant genetic diversity, 4-8 November 1996; Antalya, Turkey 1998, 163-169. Ankara; Turkey: Central Research Institute for Field Crops, Zencirci N, Kaya Z, Anikster Y, Adams WT.
80. Hofacker W. Investigations into seed weight and seed number of grapevine and their influence on berry weight. Mitt Klosterneuburg Rebe Wein Obstb Fruchteverwert 2003, 53:235-242.
81. Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia JM, Ware D, Bustamante CD, Buckler ES. Genetic structure and domestication history of the grape. Proc Natl Acad Sci USA 2011, 108:3530-3535. 10.1073/pnas.1009363108, 3048109, 21245334.
82. Grassi F, Labra M, Imazio S, Spada A, Sgorbati S, Scienza A, Sala F. Evidence of a secondary grapevine domestication centre detected by SSR analysis. Theor Appl Genet 2003, 107:1315-1320. 10.1007/s00122-003-1321-1, 13679993.
83. Riahi L, Laucou V, Le Cunff L, Zoghlami N, Boursiquot J, Lacombe T, El-Heit K, Mliki A, This P. Highly polymorphic nSSR markers: a useful tool to assess origin of North African cultivars and to provide additional proofs of secondary grapevine domestication events. Sci Hortic 2012, 141:53-60.
84. Gillapsy G, Ben-David H, Gruissem W. Fruits: a developmental perspective. Plant Cell 1993, 5:1439-1451. 160374, 12271039.
85. Robinson SP, Davies C. Molecular biology of grape berry ripening. Aust J Grape Wine Res 2000, 6:175-188.
86. Espinoza A, Contreras D, Orellana M, Perez R, Aguirre C, Castro A, Riquelme A, Fichet T, Pinto M, Hinrichsen P. Modulation by gibberellic acid of aquaporin genes expression during berry development of grapevine (Vitis vinifera L.). Acta Hort 2009, 355-362.
87. Shelden M, Howitt S, Kaiser B, Tyerman S. Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. Funct Plant Biol 2009, 36:1065-1078.
88. Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M. Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-seq. Plant Physiol 2010, 152:1787-1795. 10.1104/pp.109.149716, 2850006, 20118272.
89. Kaps ML, Cahoon GA. Growth and fruiting of container-grown Seyval blanc grapevines modified by changes in crop level, leaf number and position, and light exposure. Am J Enol Vitic 1992, 43:191-199.
90. Peng F, Reid K, Liao N, Schlosser J, Lijavetzky D, Holt R, Martinez Zapater J, Jones S, Marra M, Bohlmann J, Lund S. Generation of ESTs in Vitis vinifera wine grape (Cabernet Sauvignon) and table grape (Muscat Hamburg) and discovery of new candidate genes with potential roles in berry development. Gene 2007, 402:40-50. 10.1016/j.gene.2007.07.016, 17761391.
91. Boss PK, Thomas MR. Association of dwarfism and floral induction with a grape 'green revolution' mutation. Nature 2002, 416:847-850. 10.1038/416847a, 11976683.
92. Diaz-Riquelme J, Lijavetzky D, Martinez-Zapater JM, Carmona MJ. Genome-wide analysis of MIKC C-type MADS box genes in grapevine. Plant Physiol 2009, 149:354-369. 10.1104/pp.108.131052, 2613716, 18997115.
93. Davies C, Wolf T, Robinson S. Three putative sucrose transporters are differentially expressed in grapevine tissues. Plant Sci (Limerick) 1999, 147:93-100.
94. Nicolas P, Lecourieux D, Gomès E, Delrot S, Lecourieux F. The grape berry-specific basic helix-loop-helix transcription factor VvCEB1 affects cell size. J Exp Bot 2013, 64:991-1003. 10.1093/jxb/ers374, 3580811, 23314819.
95. Ito T, Meyerowitz EM. Overexpression of a gene encoding a cytochrome p450, CYP78A9, induces large and seedless fruit in Arabidopsis. Plant Cell 2000, 12:1541-1550. 149068, 11006330.
96. Suzuki M, Kamide Y, Nagata N, Seki H, Ohyama K, Kato H, Masuda K, Sato S, Kato T, Tabata S, Yoshida S, Muranaka T. Loss of function of 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfing, early senescence and male sterility, and reduced sterol levels. Plant J 2004, 37:750-761. 10.1111/j.1365-313X.2004.02003.x, 14871314.
97. Wang XC, Ren GH, Fang JG, Lia Y, Liu H, Wu WM, Zhao MZ. Cloning, subcellular localization and expression analysis of genes related to the synthesis of gibberellin from grapevine. Sci Agric Sin 2012, 45:2224-2231.
98. Davies C, Robinson SP. Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening: cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. Plant Physiol 2000, 122:803-812. 10.1104/pp.122.3.803, 58916, 10712544.
99. Shangguan L, Han J, Fang J, Wang X, Leng X. Identification of grape (Vitis vinifera L.) genes from EST sequences responding to exogenous gibberellins treatment. J Agric Biotech 2012, 20:135-145.
100. Silverstone AL, Tseng TS, Swain SM, Dill A, Jeong SY, Olszewski NE, Sun TP. Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis. Plant Physiol 2007, 143:987-1000. 1803720, 17142481.
101. Nishimura T, Wada T, Yamamoto KT, Okada K. The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 2005, 17:2940-2953. 10.1105/tpc.105.036533, 1276021, 16227452.
102. Boss PK, Vivier M, Matsumoto S, Dry IB, Thomas MR. A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development. Plant Mol Biol 2001, 45:541-553. 10.1023/A:1010634132156, 11414613.
103. Ishimaru M, Smith D, Gross K, Kobayashi S. Expression of three expansin genes during development and maturation of Kyoho grape berries. J Plant Physiol 2007, 164:1675-1682. 10.1016/j.jplph.2006.07.017, 17175064.
104. Hanania U, Velcheva M, Sahar N, Flaishman M, Or E, Degani O, Perl A. The ubiquitin extension protein S27a is differentially expressed in developing flower organs of Thompson seedless versus Thompson seeded grape isogenic clones. Plant Cell Rep 2009, 28:1033-1042. 10.1007/s00299-009-0715-1, 19479258.
105. Fillion L, Ageorges A, Picaud S, Coutos-Thevenot P, Lemoine R, Romieu C, Delrot S. Cloning and expression of a hexose transporter gene expressed during the ripening of grape berry. Plant Physiol 1999, 120:1083-1093. 10.1104/pp.120.4.1083, 59342, 10444092.
106. Wang S, Yu Y, Zhang C, Xu W, Wang Y. Molecular cloning and characterization of a novel gene encoding an EF-hand calcium-binding protein related to fruit seedlessness of grapevine. Sci Hortic 2011, 130:708-714.