Selection of candidate genes for grape proanthocyanidin pathway by an integrative approach

Plant Physiology and Biochemistry

Volumn 72, Issue , 2013, Pages 87-95

  Carrier, Grégory ^a,c,d   Huang, Yung Fen ^a,b,e   Le Cunff, Loïc ^a,c   Fournier Level, Alexandre ^a   Vialet, Sandrine ^b   Souquet, Jean Marc ^b   Cheynier, Véronique ^b   Terrier, Nancy ^b   This, Patrice ^a  

^a UMR AGAP   (France)

^b SPO   (France)

^c UMT Geno Vigne   (France)

^d IFREMER   (France)

^e OTTAWA RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

Association genetics; Candidate genes; Proanthocyanidin biosynthesis; QTLs; Transcriptomics; Vitis vinifera L.

Indexed keywords

VITACEAE; VITIS VINIFERA;

PROANTHOCYANIDIN;

ARTICLE; ASSOCIATION GENETICS; CANDIDATE GENES; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROANTHOCYANIDIN BIOSYNTHESIS; QTLS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; VITIS; VITIS VINIFERA L.;

ASSOCIATION GENETICS; CANDIDATE GENES; PROANTHOCYANIDIN BIOSYNTHESIS; QTLS; TRANSCRIPTOMICS; VITIS VINIFERA L.;

GENE EXPRESSION REGULATION, PLANT; PROANTHOCYANIDINS; SIGNAL TRANSDUCTION; VITIS;

EID: 84886588163     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.04.014     Document Type: Article

References (58)

1. Dixon R.A., Xie D.Y., Sharma S.B. Proanthocyanidins - a final frontier in flavonoid research?. New Phytol. 2005, 165:9-28.
2. Aron P.M., Kennedy J.A. Flavan-3-ols: nature, occurrence and biological activity. Mol. Nutr. Food Res. 2008, 52:79-104.
3. Kajita K., Kumazawa S., Nakayama T. Steric effects on interaction of tea catechins with lipid bilayers. Biosci. Biotechnol. Biochem. 2001, 65:2638-2643.
4. Kajiya K., Kumazawa S., Nakayama T. Effects of external factors on the interaction of tea catechins with lipid bilayers. Biosci. Biotechnol. Biochem. 2002, 66:2330-2335.
5. da Silva Porto P., Laranjinha J., de Freitas V. Antioxidant protection of low density lipoprotein by procyanidins: structure/activity relationships. Biochem. Pharmacol. 2003, 66:947-954.
6. Vidal S., Francis L., Guyot S., Marnet N., Kwiatkowski M., Gawel R., Cheynier V., Waters E.J. The mouth-feel properties of grape and apple proanthocyanidins in a wine-like medium. J.Sci. Food Agric. 2003, 83:564-573.
7. Terrier N., Ollé D., Verries C., Cheynier V. Biochemical & molecular aspects of flavan-3-ol synthesis during berry development. Grapevine Molecular Physiology & Biotechnology 2009, 365-388. Springer Book. Roubelakis (Ed.).
8. Bogs J., Downey M.O., Harvey J.S., Ashton A.R., Tanner G.J., Robinson S.P. Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiol. 2005, 139:652-663.
9. Bogs J., Jaffe F.W., Takos A.M., Walker A.R., Robinson S.P. The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol. 2007, 143:1347-1361.
10. Terrier N., Torregrosa L., Ageorges A., Vialet S., Verries C., Cheynier V., Romieu C. Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol. 2009, 149:1028-1041.
11. Hichri I., Heppel S.C., Pillet J., Leon C., Czemmel S., Delrot S., Lauvergeat V., Bogs J. The basic Helix-Loop-Helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Mol. Plant 2010, 3:509-523.
12. J. Matus, M. Poupin, P. Cañón, E. Bordeu, J. Alcalde, P. Arce-Johnson, Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.), Plant Mol. Biol. 72, 607-620.
13. Lepiniec L., Debeaujon I., Routaboul J.-M., Baudry A., Pourcel L., Nesi N., Caboche M. Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 2006, 57:405-430.
14. Eisenberg D., Marcotte E.M., Xenarios I., Yeates T.O. Protein function in the post-genomic era. Nature 2000, 405:823-826.
15. Kikuchi S., Satoh K., Nagata T., Kawagashira N., Doi K., Kishimoto N., Yazaki J., Ishikawa M., Yamada H., Ooka H., Hotta I., Kojima K., Namiki T., Ohneda E., Yahagi W., Suzuki K., Li C.J., Ohtsuki K., Shishiki T., Analysis G., Otomo Y., Murakami K., Iida Y., Sugano S., Fujimura T., Suzuki Y., Tsunoda Y., Kurosaki T., Kodama T., Masuda H., Kobayashi M., Xie Q., Lu M., Narikawa R., Sugiyama A., Mizuno K., Yokomizo S., Niikura J., Ikeda R., Ishibiki J., Kawamata M., Yoshimura A., Miura J., Kusumegi T., Oka M., Ryu R., Ueda M., Matsubara K., Riken, Kawai J., Carninci P., Adachi J., Aizawa K., Arakawa T., Fukuda S., Hara A., Hashidume W., Hayatsu N., Imotani K., Ishii Y., Itoh M., Kagawa I., Kondo S., Konno H., Miyazaki A., Osato N., Ota Y., Saito R., Sasaki D., Sato K., Shibata K., Shinagawa A., Shiraki T., Yoshino M., Hayashizaki Y. The rice full-length cDNA. Consortium, collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 2003, 301:376-379.
16. Cheung H.H., Lee T.L., Rennert O.M., Chan W.Y. DNA methylation of cancer genome. Birth Defects Res. Part C 2009, 87:335-350.
17. Borst M.H., Benigni A., Remuzzi G. Primer: strategies for identifying genes involved in renal disease. Nat. Clin. Pract. Nephrol. 2008, 4:265-276.
18. Huang Y.F., Doligez A., Fournier-Level A., Le Cunff L., Bertrand Y., Canaguier A., Morel C., Miralles V., Veran F., Souquet J.M., Cheynier V., Terrier N., This P. Dissecting genetic architecture of grape proanthocyanidin composition through quantitative trait locus mapping. BMC Plant Biol. 2012, 12:30.
19. Liu R., Vitte C.M., Ma J., Mahama A.A., Dhliwayo T., Lee M., Bennetzen J.L. AGeneTrek analysis of the maize genome. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:11844-11849.
20. Jaillon O., Aury J.M., 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., 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 M.E., Valle G., Morgante M., Caboche M., Adam-Blondon A.F., Weissenbach J., Quetier F., Wincker P. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449:463-467.
21. Price A.H. Believe it or not, QTLs are accurate !. Trends Plant Sci. 2006, 11:213-216.
22. Druka A.F.J., Lundqvist U., Bonar N., Alexander J., Guzy-wrobelska J., Ramsay L., Druka I., Grant L., Macaulay M., Vendramin V., Shahinnia F., Radovic S., Houston K., Harrap D., Cardle L., Marshall D., Morgante M., Stein N., Waugh R. Exploiting induced variation to dissect quantitative traits in barley. Biochem. Soc. Trans. 2010, 38:386-688.
23. Xing Y., Zhang Q. Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 2010, 61:421-442.
24. Neale D.B., Savolainen O. Association genetics of complex traits in conifers. Trends Plant Sci. 2004, 9:325-330.
25. Yu J., Pressoir G., Briggs W.H., Vroh Bi I., Yamasaki M., Doebley J.F., McMullen M.D., Gaut B.S., Nielsen D.M., Holland J.B., Kresovich S., Buckler E.S. Aunified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 2006, 38:203-208.
26. J.A. Rafalski, Association genetics in crop improvement, Curr. Opin. Plant Biol. 13, 174-180.
27. Fournier-Level A., Le Cunff L., Gomez C., Doligez A., Ageorges A., Roux C., Bertrand Y., Souquet J.M., 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.
28. Emanuelli F., Battilana J., Costantini L., Le Cunff L., Boursiquot J.M., This P., Grando M. Acandidate gene association study on muscat flavor in grapevine (Vitis vinifera L.). BMC Plant Biol. 2010, 10:241.
29. Fernandez L., Torregrosa L., Segura V., Bouquet A., Martinez-Zapater J.M. Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. Plant J. 2010, 61:545-557.
30. Ageorges A., Fernandez L., Vialet S., Merdinoglu D., Terrier N., Romieu C. Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci. 2006, 170:372-383.
31. Becher M., Talke I.N., Krall L., Krämer U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 2004, 37:251-268.
32. Khater F., Fournand D., Vialet S., Meudec E., Cheynier V., Terrier N. Identification and functional characterization of cDNAs coding for hydroxybenzoate/hydroxycinnamate glucosyltransferases co-expressed with genes related to proanthocyanidin biosynthesis. J.Exp. Bot. 2012, 63:1201-1214.
33. Ko J.H., Kim J.H., Jayanty S.S., Howe G.A., Han K.H. Loss of function of COBRA, a determinant of oriented cell expansion, invokes cellular defence responses in Arabidopsis thaliana. J.Exp. Bot. 2006, 57:2923-2936.
34. Li A.S., Steffens J.C. An acyltransferase catalyzing the formation of diacylglucose is a serine carboxypeptidase-like protein. Proc. Nat. Acad. Sci. U.S.A. 2000, 97:6902-6907.
35. Lehfeldt C., Shirley A.M., Meyer K., Ruegger M.O., Cusumano J.C., Viitanen P.V., Strack D., Chapple C. Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell 2000, 12:1295-1306.
36. Matus J., Aquea F., Arce-Johnson P. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol. 2008, 8:83.
37. Jin H., Cominelli E., Bailey P., Parr A., Mehrtens F., Jones J., Tonelli C., Weisshaar B., Martin C. Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J. 2000, 19:6150-6161.
38. Colquhoun T.A., Kim J.Y., Wedde A.E., Levin L.A., Schmitt K.C., Schuurink R.C., Clark D.G. PhMYB4 fine-tunes the floral volatile signature of Petunia x hybrida through PhC4H. J.Exp. Bot. 2011, 62:1133-1143.
39. Komarova N.Y., Thor K., Gubler A., Meier S., Dietrich D., Weichert A., Suter Grotemeyer M., Tegeder M., Rentsch D. AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol. 2008, 148:856-869.
40. Nesi N., Jond C., Debeaujon I., Caboche M., Lepiniec L. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 2001, 13:2099-2114.
41. Grimplet J., Deluc L., Tillett R., Wheatley M., Schlauch K., Cramer G., Cushman J. Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics 2007, 8:187.
42. Polesani M., Bortesi L., Ferrarini A., Zamboni A., Fasoli M., Zadra C., Lovato A., Pezzotti M., Delledonne M., Polverari A. General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V.riparia) grapevine species. BMC Genomics 2010, 11:117.
43. Wayne M.L., McIntyre L.M. Combining mapping and arraying: an approach to candidate gene identification. Proc. Nat. Acad. Sci. U.S.A. 2002, 99:14903-14906.
44. Chen X., Hackett C.A., Niks R.E., Hedley P.E., Booth C., Druka A., Marcel T.C., Vels A., Bayer M., Milne I., Morris J., Ramsay L., Marshall D., Cardle L., Waugh R. An eQTL analysis of partial resistance to Puccinia hordei in barley. PLoS One 2010, 5:e8598.
45. Qi X., Bakht S., Leggett M., Maxwell C., Melton R., Osbourn A. Agene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc. Nat. Acad. Sci. U.S.A. 2004, 101:8233-8238.
46. Brest P., Lapaquette P., Souidi M., Lebrigand K., Cesaro A., Vouret-Craviari V., Mari B., Barbry P., Mosnier J.-F., Hebuterne X., Harel-Bellan A., Mograbi B., Darfeuille-Michaud A., Hofman P. Asynonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat. Genet. 2011, 43:242-245.
47. Akagi T., Ikegami A., Suzuki Y., Yoshida J., Yamada M., Sato A., Yonemori K. Expression balances of structural genes in shikimate and flavonoid biosynthesis cause a difference in proanthocyanidin accumulation in persimmon (Diospyros kaki Thunb.) fruit. Planta 2009, 230:899-915.
48. Arbilly M., Pisanté A., Devor M., Darvasi A. An integrative approach for the identification of quantitative trait loci. Anim. Genet. 2006, 37:7-9.
49. Spence J., Liang T., Foroud T., Lo D., Carr L. Expression profiling and QTL analysis: a powerful complementary strategy in drug abuse research. Addict. Biol. 2005, 10:47-51.
50. Barnaud A., Lacombe T., Doligez A. Linkage disequilibrium in cultivated grapevine, Vitis vinifera L. Theor. Appl. Genet. 2006, 112:708-716.
51. Fournand D., Vicens A., Sidhoum L., Souquet J.M., Moutounet M., Cheynier V. Accumulation and extractability of grape skin tannins and anthocyanins atdifferent advanced physiological stages. J.Agric. Food Chem. 2006, 54:7331-7338.
52. Adam-Blondon A.F., Roux C., Claux D., Butterlin G., Merdinoglu D., This P. Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grape genetics. Theor. Appl. Genet. 2004, 109:1017-1027.
53. Le Cunff L., Fournier-Level A., Laucou V., Vezzulli S., Lacombe T., Adam-Blondon A.F., Boursiquot J.M., This P. Construction of nested genetic core collections to optimize the exploitation of natural diversity in Vitis vinifera L. subsp sativa. BMC Plant Biol. 2008, 8.
54. Kang H.M., Zaitlen N.A., Wade C.M., Kirby A., Heckerman D., Daly M.J., Eskin E. Efficient control of population structure in model organism association mapping. Genetics 2008, 178:1709-1723.
55. Pritchard J.K., Stephens M., Rosenberg N.A., Donnelly P. Association mapping in structured populations. Am. J. Hum. Genet. 2000, 67:170-181.
56. Loiselle B.A., Sork V.L., John N., Catherine G. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am. J. Bot. 1995, 82:1420-1425.
57. Hardy O.J., Vekemans X. Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2002, 2:618-620.
58. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J.Roy. Stat. Soc. Ser. B Stat. Methodol. 1995, 57:289-300.