Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape

Planta

Volumn 232, Issue 1, 2010, Pages 219-234

  Gambetta, Gregory A ^a   Matthews, Mark A ^a   Shaghasi, Tarana H ^a   McElrone, Andrew J ^a   Castellarin, Simone D ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF UDINE   (Italy)

Author keywords

Hormone action; Nonclimacteric fruit; Vitis vinifera; Water deficit

Indexed keywords

ABSCISIC ACID;

ARTICLE; CARBOHYDRATE METABOLISM; GENE EXPRESSION PROFILING; GENETICS; GRAPE; METABOLISM; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VALIDATION STUDY;

ABSCISIC ACID; CARBOHYDRATE METABOLISM; GENE EXPRESSION PROFILING; PHYLOGENY; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VITIS;

VITACEAE; VITIS VINIFERA;

EID: 77952511469     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1165-2     Document Type: Article

References (87)

1. Antolin MC, Santesteban H, Maria ES, Aguirreolea J, Sanchez-Diaz M (2008) Involvement of abscisic acid and polyamines in berry ripening of Vitis vinifera (L.) subjected to water deficit irrigation. Aust J Grape Wine Res 14: 123-133.
2. Bogs J, Jaffe FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143: 1347-1361.
3. Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043.
4. Bradford KJ (1990) A water relations analysis of seed-germination rates. Plant Physiol 94: 840-849.
5. Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15: 2165-2180.
6. Castellarin SD, Matthews MA, Di Gaspero G, Gambetta GA (2007a) Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227: 101-112.
7. Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007b) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 30: 1381-1399.
8. Chernys JT, Zeevaart JA (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124: 343-353.
9. Chervin C, El-Kereamy A, Roustan JP, Latche A, Lamon J, Bouzayen M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 167: 1301-1305.
10. Conde C, Agasse A, Glissant D, Tavares R, Geros H, Delrot S (2006) Pathways of glucose regulation of monosaccharide transport in grape cells. Plant Physiol 141: 1563-1577.
11. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38: 366-379.
12. Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115: 1155-1161.
13. Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8: 429.
14. Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Merillon JM, Cushman JC, Cramer GR (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics 10: 212.
15. Doyle JA (1998) Phylogeny of vascular plants. Annu Rev Ecol Syst 29: 567-599.
16. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42: 443-461.
17. Draghici S, Khatri P, Eklund AC, Szallasi Z (2006) Reliability and reproducibility issues in DNA microarray measurements. Trends Genet 22: 101-109.
18. Eriksson O, Friis EM, Lofgren P (2000) Seed size, fruit size, and dispersal systems in angiosperms from the early cretaceous to the late tertiary. Am Nat 156: 47-58.
19. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206.
20. Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 59: 2299-2308.
21. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. J Exp Bot 55: 253-264.
22. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl): S170-S180.
23. Hammargren J, Rosenquist S, Jansson C, Knorpp C (2008) A novel connection between nucleotide and carbohydrate metabolism in mitochondria: sugar regulation of the Arabidopsis nucleoside diphosphate kinase 3a gene. Plant Cell Rep 27: 529-534.
24. Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engstrom P, Soderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139: 509-518.
25. Hiratsuka S, Onodera H, Kawai Y, Kubo T, Itoh H, Wada R (2001) ABA and sugar effects on anthocyanin formation in grape berry cultured in vitro. Sci Hortic 90: 121-130.
26. Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12: 343-351.
27. Hugueney P, Provenzano S, Verries C, Ferrandino A, Meudec E, Batelli G, Merdinoglu D, Cheynier V, Schubert A, Ageorges A (2009) A novel cation-dependent o-methyltransferase involved in anthocyanin methylation in grapevine. Plant Physiol 150: 2057-2070.
28. Iandolino AB, da Silva FG, Lim H, Choi H, Williams LE, Cook DR (2004) High-quality RNA, cDNA, and derived EST libraries from grapevine (Vitis vinifera L.). Plant Mol Biol Rep 22: 269-278.
29. Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11: 550-558.
30. 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, 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 ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P, Public F-I (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: U463-U465.
31. Johannesson H, Wang Y, Hanson J, Engstrom P (2003) The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol 51: 719-729.
32. Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215: 924-933.
33. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7: 235-246.
34. Koyama K, Sadamatsu K, Goto-Yamamoto N (2009) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct Integr Genomics (PMID: 19841954).
35. Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI (2006) The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol 140: 127-139.
36. Larronde F, Krisa S, Decendit A, Cheze C, Merillon JM (1998) Regulation of polyphenol production in Vitis vinifera cell suspension cultures by sugars. Plant Cell Rep 17: 946-950.
37. Leclercq J, Adams-Phillips LC, Zegzouti H, Jones B, Latche A, Giovannoni JJ, Pech JC, Bouzayen M (2002) LeCTR1, a tomato CTR1-like gene, demonstrates ethylene signaling ability in Arabidopsis and novel expression patterns in tomato. Plant Physiol 130: 1132-1142.
38. Lee YH, Chun JY (1998) A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol Biol 37: 377-384.
39. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49: 199-222.
40. Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264: 1448-1452.
41. Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759-771.
42. Lieberman M, Baker JE, Sloger M (1977) Influence of plant hormones on ethylene production in apple, tomato, and avocado slices during maturation and senescence. Plant Physiol 60: 214-217.
43. Lisso J, Altmann T, Mussig C (2006) Metabolic changes in fruits of the tomato dx mutant. Phytochemistry 67: 2232-2238.
44. Lohani S, Trivedi PK, Nath P (2004) Changes in activities of cell wall hydrolases during ethylene-induced ripening in banana: effect of 1-MCP, ABA and IAA. Postharvest Biol Technol 31: 119-126.
45. Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179: 1004-1016.
46. Lund ST, Peng FY, Nayar T, Reid KE, Schlosser J (2008) Gene expression analyses in individual grape (Vitis vinifera L.) berries during ripening initiation reveal that pigmentation intensity is a valid indicator of developmental staging within the cluster. Plant Mol Biol 68: 301-315.
47. Matsushima J, Hiratsuka S, Taniguchi N, Wada R, Suzaki N (1989) Anthocyanin accumulation and sugar content in the skin of grape cultivar Olympia treated with ABA. J Jpn Soc Hortic Sci 58: 551-555.
48. Matthews MA, Anderson MM (1988) Fruit ripening in Vitis vinifera L-responses to seasonal water deficits. Am J Enol Vitic 39: 313-320.
49. Matthews MA, Anderson MM, Schultz HR (1987) Phenologic and growth responses to early and late season water deficits in Cabernet franc. Vitis 26: 147-160.
50. Mei Z, Ping L, Guanglian Z, Xiangxin L (2009) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166(12): 1241-1252.
51. Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455.
52. Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T (2007) ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J 50: 935-949.
53. Okamoto G, Kuwamura T, Hirano K (2004) Effects of water deficit stress on leaf and berry ABA and berry ripening in Chardonnay grapevines (Vitis vinifera). Vitis 43: 15-17.
54. Owen SJ, Lafond MD, Bowen P, Bogdanoff C, Usher K, Abrams SR (2009) Profiles of abscisic acid and its catabolites in developing merlot grape (Vitis vinifera) berries. Am J Enol Vitic 60: 277-284.
55. Pan QH, Li MJ, Peng CC, Zhang N, Zou X, Zou KQ, Wang XL, Yu XC, Wang XF, Zhang DP (2005) Abscisic acid activates acid invertases in developing grape berry. Physiol Plant 125: 157-170.
56. Pan QH, Yu XC, Zhang N, Zou X, Peng CC, Wang XL, Zou KQ, Zhang DP (2006) Activity, but not expression, of soluble and cell wall-bound acid invertases is induced by abscisic acid in developing apple fruit. J Integr Plant Biol 48: 536-549.
57. Parikh HR, Nair GM, Modi VV (1990) Some structural-changes during ripening of mangoes (Mangifera indica Var Alphonso) by abscisic-acid treatment. Ann Bot 65: 121-127.
58. Peppi MC, Fidelibus M, Dokoozlian N, Walker MA (2006) Abscisic acid applications improve the color of crimson seedless table grapes. Am J Enol Vitic 57: 388A.
59. Peppi MC, Walker MA, Fidelibus MW (2008) Application of abscisic acid rapidly upregulated UFGT gene expression and improved color of grape berries. Vitis 47: 11-14.
60. Pirie A, Mullins MG (1976) Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissues treated with sucrose, nitrate, and abscisic acid. Plant Physiol 58: 468-472.
61. Poupin MJ, Federici F, Medina C, Matus JT, Timmermann T, Arce-Johnson P (2007) 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 404: 10-24.
62. Ravi N, Wan KT, Swindle K, Hamilton PD, Duan G (2006) Development of techniques to compare mechanical properties of reversible hydrogels with spherical, square columnar and ocular lens geometry. Polymer 47: 4203-4209.
63. Rieu I, Powers SJ (2009) Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21: 1031-1033.
64. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709.
65. Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29: 426-434.
66. Rubio S, Rodrigues A, Saez A, Dizon MB, Galle A, Kim TH, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150: 1345-1355.
67. Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37: 354-369.
68. Soderman E, Mattsson J, Engstrom P (1996) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10: 375-381.
69. Soderman E, Hjellstrom M, Fahleson J, Engstrom P (1999) The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Mol Biol 40: 1073-1083.
70. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140: 637-646.
71. Sun CX, Palmqvist S, Olsson H, Boren M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15: 2076-2092.
72. Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 140: 150-158.
73. Telef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, Gallusci P (2006) Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol 62: 453-469.
74. Thomas TR, Matthews MA, Shackel KA (2006) Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. Plant Cell Environ 29: 993-1001.
75. Thomas TR, Shackel KA, Matthews MA (2008) Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening. Planta 228: 1067-1076.
76. Trainotti L, Pavanello A, Casadoro G (2005) Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits? J Exp Bot 56: 2037-2046.
77. Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58: 3299-3308.
78. Velasco R, Zharkikh A, Troggio M, Cartwright 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, Dematte L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2: e1326.
79. Vitrac X, Larronde F, Krisa S, Decendit A, Deffieux G, Merillon JM (2000) Sugar sensing and Ca2+-calmodulin requirement in Vitis vinifera cells producing anthocyanins. Phytochemistry 53: 659-665.
80. Wada H, Shackel KA, Matthews MA (2008) Fruit ripening in Vitis vinifera: apoplastic solute accumulation accounts for pre-veraison turgor loss in berries. Planta 227: 1351-1361.
81. Wada H, Matthews MA, Shackel KA (2009) Seasonal pattern of apoplastic solute accumulation and loss of cell turgor during ripening of Vitis vinifera fruit under field conditions. J Exp Bot 60: 1773-1781.
82. Welbaum GE, Tissaoui T, Bradford KJ (1990) Water relations of seed development and germination in muskmelon (Cucumis melo L.). 3. Sensitivity of germination to water potential and abscisic-acid during development. Plant Physiol 92: 1029-1037.
83. Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Aust J Grape Wine Res 15: 195-204.
84. Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12: 9-26.
85. Xue T, Wang D, Zhang S, Ehlting J, Ni F, Jakab S, Zheng C, Zhong Y (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genomics 9: 550.
86. Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140: 558-579.
87. Yun JJ, Heisler LE, Hwang II, Wilkins O, Lau SK, Hyrcza M, Jayabalasingham B, Jin J, McLaurin J, Tsao MS, Der SD (2006) Genomic DNA functions as a universal external standard in quantitative real-time PCR. Nucleic Acids Res 34: e85.