Short day transcriptomic programming during induction of dormancy in grapevine

Frontiers in Plant Science

Volumn 6, Issue NOVEMBER, 2015, Pages

  Fennell, Anne Y ^a   Schlauch, Karen A ^b   Gouthu, Satyanarayana ^c   Deluc, Laurent G ^c   Khadka, Vedbar ^a   Sreekantan, Lekha ^a   Grimplet, Jerome ^d   Cramer, Grant R ^b   Mathiason, Katherine L ^a  

^a SOUTH DAKOTA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEVADA   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF LA RIOJA   (Spain)

Author keywords

ABA; Bud; Raffinose; Resveratrol; Seyval; Trehalose; Vitis riparia; VitisNet

Indexed keywords

EID: 84947437307     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00834     Document Type: Article

References (89)

1. Aida, M., Ishida, T., Fukai, H., Fujisawa, H., and Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.Plant Cell 9, 841-857. doi: 10.1105/tpc.9.6.841
2. Altick, A., Feng, C. Y., Johnson, A. L., Schlauch., K., and Von Bartheld, C. S. (2012). Differences in gene expression between strabismic and normal human extraocular muscles. Invest. Ophthalmol. Vis. Sci. 53, 5168-5177. doi: 10.1167/iovs.12-9785
3. Anderson, J. V., Gesch, R. W., Jia, Y., Chao, W. S., and Horvath, D. P. (2005). Seasonal shifts in dormancy status, carbohydrate metabolism, and related gene expression in crown buds of leafy spurge. Plant Cell Envir. 28, 1567-1578. doi: 10.1111/j.1365-3040.2005.01393.x
4. Aw, T., Schlauch, K., Keeling, C. I., Young, S., Bearfield, J. C., Blomquist, G. J., et al. (2010). Functional genomics of mountain pine beetle (Dendroctonus ponderosae) midguts and fat bodies. BMC Genomics 11:215. doi: 10.1186/1471-2164-11-215
5. Baldi, P., and Hatfield, G. W. (2002). DNA Microarrays and Gene Expression. Cambridge: University Press.
6. Bedon, F., Bomal, C., Caron, S., Levasseur, C., Boyle, B., Mansfield, S. D., et al. (2010). Subgroup 4 R2R3-MYBs in conifer trees: gene family expansion and contribution to the isoprenoid- and flavonoid-oriented response. J. Exp. Bot. 61, 3847-3864. doi: 10.1093/jxb/erq196
7. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57, 289-300.
8. Böhlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A. M., Jansson, S., Strauss, S. H., et al. (2006). CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040-1043. doi: 10.1126/science.1126038
9. Bomal, C., Duval, I., Giguere, I., Fortin, É., Caron, S., Stewart, D., et al. (2014). Opposite action of R2R3-MYBs from different subgroups on key genes of the shikimate and monolignol pathways in spruce. J. Exp. Bot. 65, 495-408. doi: 10.1093/jxb/ert398
10. Broeckling, C. D., Hulman, D. V., Farag, M. A., Smith, J. T., May, G. D., Mendes, P., et al. (2005). Metabolic profiling of medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitor on metabolism. J. Exp. Bot. 56, 323-336. doi: 10.1093/jxb/eri058
11. Cadman, C. S. C., Toorop, P. E., Hilhorst, H. W. M., and Finch-Savage, W. E. (2006). Gene expression profiles of Arabidops Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 46, 805-822. doi: 10.1111/j.1365-313X.2006.02738.x
12. Chang, S., Puryear, J., and Cairney, J. (1993). A simple efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11, 113-116. doi: 10.1007/BF02670468
13. Chang, X., Heene, E., Qiao, F., and Nick, P. (2011). The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. PLoS ONE 6:e264405. doi: 10.1371/journal.pone.0026405
14. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., and Ecker, J. R. (1997). Activation of the ethylene gas response pathway in Arabidopsis by nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133-1144. doi: 10.1016/S0092-8674(00)80300-1
15. Chen, L., Song, L., Li, S., Zhang, L., Zou, C., and Yu, D. (2012). The role of WRKY transcription factors in plant abiotic stresses. Biochimica et Biophysica Acta 1819, 120-128. doi: 10.1016/j.bbagrm.2011.09.002
16. Chen, Q., Yang, L., Ahmad, P., Wan, X., and Hu, X. (2010). Proteomic profiling and redoz status alteration of recalcitrant tea (Camellia sinensis) seed in response to desiccation. Planta 233, 583-592. doi: 10.1007/s00425-010-1322-7
17. Contento, A. L., Kim, S. J., and Bassham, D. C. (2004). Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol. 135, 2330-2347. doi: 10.1104/pp.104.044362
18. Cooke, J. E., Eriksson, M. E., and Juntilla, O. (2012). The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ. 35, 1707-1728. doi: 10.1111/j.1365-3040.2012.02552.x
19. Cramer, G. R., Ergül, A., Grimplet, J., Tillett, R. L., Tattersall, E. A., Bohlman, M. C., et al. (2007). Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct. Integr. Genomics 7, 111-134. doi: 10.1007/s10142-006-0039-y
20. Debast, S., Nunes-Nesi, A., Hajirezaei, M. R., Hofmann, J., Sonnewald, U., Fernie, A. R., et al. (2011). Altering Trehalose-6-Phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol. 156, 1754-1771. doi: 10.1104/pp.111.179903
21. Degu, A., Hochberg, U., Sikron, N., and Venturini, L. (2014). Metabolite and transcript profiling of berry skin during fruit development elucidates differential regulation between Cabernet Sauvignon and Shiraz cultivars at branching points in the polyphenol pathway. BMC Plant Biol. 14, 188. doi: 10.1186/s12870-014-0188-4
22. Deluc, L. G., Decendit, A., Papstamoulis, Y., Merillon, J.-M., Cushman, J. C., and Cramer, G. R. (2011). Water deficit increases stilbene metabolism in Cabernet Sauvignon berries. J. Agric. Food Chem. 59, 289-297. doi: 10.1021/jf1024888
23. Deluc, L. G., Quilici, D. R., Decendit, A., Grimplet, J., Wheatley, M. D., Schlauch, K. A., et al. (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 doi: 10.1186/1471-2164-10-212
24. Díaz-Riquelme, J., Grimplet, J., Martínez-Zapater, J. M., and Carmona, M. J. (2012). Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol. 12:181. doi: 10.1186/1471-2229-12-181
25. El Kayal, W., Allen, C. C. G., Ju, C. J.-T., Adams, E., King-Jones, S., Zaharia, L. I., et al. (2011). Molecular events of apical bud formation in white spruce, Picea glauca. Plant Cell Environ. 34, 480-500. doi: 10.1111/j.1365-3040.2010.02257.x
26. Fang, L. Y., Hou, L., Wang, H., Xin, N., Wang, S., and Li., S. (2014). Myb14, a direct activator of STS, is associated with resveratrol content variation in berry skin in two grape cultivars. Plant Cell Rep. 33, 1629-1640. doi: 10.1007/s00299-014-1642-3
27. Farmer, E. E., and Mueller, M. J. (2013). ROS-mediated lipid perozidation and RES-activated signaling. Ann. Rev. Plant Biol. 64, 429-450. doi: 10.1146/annurev-arplant-050312-120132
28. Fennell, A. (2004). Freezing tolerance and injury in grapevines. J. Crop Improvement10, 201-235. doi: 10.1300/J411v10n01_09
29. Fennell, A., and Hoover, E. (1991). Photoperiod influences growth, bud dormancy and cold acclimation in Vitis labruscana and V. riparia. J. Amer. Soc. Hort. Sci. 116, 270-273.
30. Fennell, A., and Mathiason, K. (2002). "Early acclimation response in grapes (Vitis)," in Plant Cold Hardiness, eds P. Li and T. Palva (New York, NY: Kluwer Academic/Plenum Publishers), 93-107.
31. Forde, B. G., and Lea, P. J. (2007). Glutamate in plants: metabolism regulation and signaling. J. Expt. Bot. 58, 2339-2358. doi: 10.1093/jxb/erm121
32. Garris, A., Clark, L., Owens, C., McKay, S., Luby, J., Mathiason, K., et al. (2009). Mapping of photoperiod-induced growth cessation in the wild grape V. riparia. J. Amer. Soc. Hort. Sci. 134, 261-272.
33. Gautier, L., Cope, L., Bolstad, B., and Irizarry, R. A. (2004). Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307-415. doi: 10.1093/bioinformatics/btg405
34. Gordon, A. D. (1999). Classification. 2nd Edn. Boca Raton, FL; London; New York, NY; Washington, D.C.: Chapman & Hall/RC.
35. Grimplet, J., Cramer, G. R., Dickerson, J. A., Mathiason, K., Hemert, J. V., and Fennell, A. (2009). VitisNet: "Omics" Integration through Grapevine Molecular Networks. PLoS ONE 4, e8365. doi: 10.1371/journal.pone.0008365
36. Grimplet, J., Hemert, J. V., Carbonell-Bejerano, P., Díaz-Riquelme, J., Dickerson, J. A., Fennell, A., et al. (2012). Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences. BMC Res. Notes 5:213.doi: 10.1186/1756-0500-5-213
37. Hachez, C., Zelazny, E., and Chaumont, F. (2006). Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochim. et Biophys. Acta 8, 1142-1166. doi: 10.1016/j.bbamem.2006.02.017
38. Hamman, R. A., Dami, I. E., Walsh, T. M., and Stushnoff, C. M. (1996). Seasonal carbohydrate changes and cold hardiness of Chardonnay and Riesling grapevines. Am. J. Enol. Vitic. 47, 31-36.
39. Horvath, D. P., Chao, W. S., Suttle, J. C., Thimmapuram, J., and Anderson, J. V. (2008). Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.).BMC Genomics 9:536. doi: 10.1186/1471-2164-9-536
40. Irizarry, R. A., Hobbs, R., Collin, R., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., et al. (2003). Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264. doi: 10.1093/biostatistics/4.2.249
41. Jensen, M. K., Kjaersgaard, T., Nielsen, M. M., Galberg, P., Petersen, K., O'shea, C., et al. (2013). The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signaling. Biochem. J. 426, 183-196. doi: 10.1042/BJ20091234
42. Jiménez, S., Li, Z., Reighard, G. L., and Bielenberg, D. G. (2010). Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant. BMC Plant Biol. 10, 25-35. doi: 10.1186/1471-2229-10-25
43. Johnson, W. E., Li, C., and Rabinovic, A. (2007). Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8, 118-127. doi: 10.1093/biostatistics/kxj037
44. Jones, K. S., Paroschy, J., McKersie, B. D., and Bowley, S. R. (1999). Carbohydrate composition and freezing tolerance of canes and buds in Vitis vinifera. J. Plant Physiol. 155, 101-106. doi: 10.1016/S0176-1617(99)80146-1
45. Kerr, M. K., Martin, M., and Churchill, G. A. (2000). Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819-837. doi: 10.1089/10665270050514954
46. Knudsen, S. (2002). A Biologist's Guide to the Analysis of DNA Microarray Data. New York, NY: John Wiley & Sons.
47. Koike, M., Takezawa, D., Arakawa, K., and Yoshida, S. (1997). Accumulation of 19-kDa Plasma Membrane polypeptide during induction of freezing tolerance in wheat suspension-cultured cells by abscisic acid. Plant Cell Physiol. 38, 707-716. doi: 10.1093/oxfordjournals.pcp.a029224
48. Krochko, J. E., Abrams, G. D., Loewen, M. K., Abrams, S. R., and Cutler, A. J. (1998). (+)-abscisic acid 8'-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol. 118, 849-860. doi: 10.1104/pp.118.3.849
49. Kuhn, A., Schlauch, K., Lao, R., Halayko, A., Gerthoffer, W. T., and Singer, C. A. (2010). MicroRNA expression in human airway smooth muscle cells: role of miR-25 in regulation of airway smooth muscle phenotype. Am. J. Respir. Cell Mol. Biol. 42, 506-513. doi: 10.1165/rcmb.2009-0123OC
50. Langcake, P., and Pryce, R. J. (1976). The production of resveratrol by Vitis viniferaand other members of the Vitaceae as a response to infection or injury. Physiol. Plant Pathol. 9, 77-86. doi: 10.1016/0048-4059(76)90077-1
51. Lau, S., and Deng, X. W. (2010). Plant hormone signaling lightens up: integrators of light and hormone. Curr. Opin. Plant Biol. 13, 571-577. doi: 10.1016/j.pbi.2010.07.001
52. Less, H., and Galilli, G. (2008). Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol. 147, 316-220. doi: 10.1104/pp.108.115733
53. Liu, Y., Koornneef, M., and Soppe, W. J. J. (2007). The absend of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19, 433-444. doi: 10.1105/tpc.106.049221
54. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev, V., et al. (2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. 2, ra45. doi: 10.1126/scisignal.2000448
55. Mullins, M. G., Bouquet, A., and Williams, L. E. (1992). Biology of the Grapevine.Cambridge: Cambridge University Press.
56. Oh, S., Park, S., and Han, K. H. (2003). Transcriptional regulation of secondary growth in Arabidopsis thaliana. J. Exp. Bot. 54, 2709-2722. doi: 10.1093/jxb/erg304
57. Olsen, J. E., Junttila, O., Nilsen, J., Eriksson, M. E., Martinussen, I., Olsson, O., et al. (1997). Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Plant J. 12, 1339-1350. doi: 10.1046/j.1365-313x.1997.12061339.x
58. Owen, S. J., and Abrams, S. R. (2009). "Measurement of plant hormones by liquid chromatography-mass spectrometry in plant hormones" in Methods and Protocols, eds. S. Cutler and D. Bonetta (New York, NY: Humana Press), 495.
59. Park, M.-R., Yun, K.-Y., Mohanty, B., Herath, V., Xu, F., Wijaya, E., et al. (2010). Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. Plant Cell Environ. 33, 2209-2230. doi: 10.1111/j.1365-3040.2010.02221.x
60. Pasquali, G., Biricolti, S., Locatelli, F., Baldoni, E., and Mattana, M. (2008). Osmyb4expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep. 27, 1677-1686. doi: 10.1007/s00299-008-0587-9
61. Paul, M. J., Primavesi, L. F., Jhurreea, D., and Zhang, Y. (2008). Trehalose metabolism and signaling. Annu. Rev. Plant Biol. 59, 417-441. doi: 10.1146/annurev.arplant.59.032607.092945
62. Puranik, S., Pranav, P. S., Srivastava, P. S., and Prasad, M. (2012). NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 17, 369-381. doi: 10.1016/j.tplants.2012.02.004
63. Resman, L., Howe, G., Jonsen, D., Englund, M., Druart, N., Schrader, J., et al. (2010). Components acting downstream of short day perception regulate differential cessation of cambial activity and associated responses in early and late clones of hybrid poplar.Plant Physiol. 154, 1294-1303. doi: 10.1104/pp.110.163907
64. Rhode, A., Prinsen, E., De Rycke, R., Engler, G., Van Montagu, M., and Boerjan, W. (2002). PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14, 1885-1901. doi: 10.1105/tpc.003186
65. Rinne, P. L. H., Kaikuranta, P. M., and van der Schoot, C., (2001). The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J., 26, 249-264. doi: 10.1046/j.1365-313X.2001.01022.x
66. Ruonala, R., Rinne, P. L. H., Baghour, M., Moritz, T., Tuominen, H., and Kangajärvi, J. (2006). Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J. 46, 628-640. doi: 10.1111/j.1365-313X.2006.02722.x
67. Ruonala, R., Rinne, P. L. H., Kangasjärvi, J., and van der Schoot, C. (2008). CENL1expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell 20, 59-74. doi: 10.1105/tpc.107.056721
68. Rushton, P. J., Somssich, I. E., Ringler, P., and Shen, Q. J. (2010). WRKY transcription factors. Trends Plant Sci. 15, 247-258. doi: 10.1016/j.tplants.2010.02.006
69. Ruttink, T., Arend, M., Morreel, K., Storme, V., Rombauts, S., Fromm, J., et al. (2007). A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19, 2370-2390. doi: 10.1105/tpc.107.052811
70. Santamaría, M. E., Rodríuez, R., Cañal, M. J., and Toorop, P. E. (2011). Transcriptome analysis of chestnut (Castanea sativa) tree buds suggests a putative role for epigenetic control of bud dormancy. Ann. Bot. 108, 485-498. doi: 10.1093/aob/mcr185
71. Schnabel, B. J., and Wample, R. L. (1987). Dormancy and cold hardiness in Vitis vinifera L. cv. White Riesling as influenced by photoperiod and temperature. Amer. J. Enol. Vitic. 34, 265-272.
72. Solano, R., Stepanova, A., Chao, Q., and Ecker, J. R. (1998). Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 1703-3714. doi: 10.1101/gad.12.23.3703
73. Sonnewald, S., and Sonnewald, U. (2014). Regulation of potato tuber sprouting.Planta 239, 27-38. doi: 10.1007/s00425-013-1968-z
74. Sreekantan, L., Mathiason, K., Grimplet, J., Schlauch, K., Dickerson, J., and Fennell, A. (2010). Differential floral development and gene expression in grapevines during long and short photoperiods suggests a role for floral genes in dormancy transitioning.Plant Mol. Bio. 73, 191-205. doi: 10.1007/s11103-010-9611-x
75. Stekel, D. (2003). Microarray Bioinformatics. Cambridge; New York, NY; Melbourne, VIC; Madrid; Cape Town; Singapore; Sao Paulo: Cambridge University Press.
76. Stoev, K. D., Manarov, P. T., and Benchev, I. B. (1960). Sugars and free amino acids during ripeningand dormancy of the grape plant. Fiziol. Rast. 7, 145-150.
77. Stushnoff, C., Remmele, R. L., Esensee, V., and McNeil, M. (1993). "Low temperature induced biochemical mechanisms: implications for cold acclimation and de-acclimation," in Interacting Stresseson Plants in a Changing Climate, Vol. 116, eds M. B. Jackson and C. R. Black (Berlin; Heidelberg: Springer-Verlag), 647-657.
78. Subramanian, A., Kuehn, H., Gould, J., Tamayo, P., and Mesirov, J. P. (2007). GSEA-P: a desktop application for gene set enrichment analysis. Bioinformatics 23, 3251-3253. doi: 10.1093/bioinformatics/btm369
79. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550. doi: 10.1073/pnas.0506580102
80. Tattersall, E. A., Grimplet, J., DeLuc, L., Wheatley, M. D., Vincent, D., Osborne, C., et al. (2007). Transcript abundance profiles reveal larger and more complex responses of grapevine to chilling compared to osmotic and salinity stress. Funct. Integr. Genomics 7, 317-333. doi: 10.1007/s10142-007-0051-x
81. Ueno, S., Klopp, C., Leplé, J. C., Derory, J., Noirot, C., Léger, V., et al. (2013). Transcriptional profiling of bud dormancy induction and release in oak by next-generation sequencing. BMC Genomics 14, 236-250. doi: 10.1186/1471-2164-14-236
82. Wake, C. M. F., and Fennell, A. (2000). Morphological, physiological and dormancy responses of three Vitis genotypes to short photoperiod. Physiol. Plant 109, 203-210 doi: 10.1034/j.1399-3054.2000.100213.x
83. Wang, M., Vannozzi, A., Wang, G., Liang, Y.-H., Tornielli, G. B., Zenoni, S., et al. (2014). Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Hort. Res. 1, 14016. doi: 10.1038/hortres.2014.16
84. Wang, W., Tang, K., Yang, H. R., Wen, P. F., Zhang, P., Wang, H. L., et al. (2010). Distribution of resveratrol and stilbene synthase in young grape plants (Vitis viniferaL. cv. Cabernet Sauvignon) and the effect of UV-C on its accumulation. Plant Physiol. Biochem. 48, 142-152. doi: 10.1016/j.plaphy.2009.12.002
85. Wood, M., Rae, G. M., Wu, R.-M., Walton, E. T., Xue, B., Hellens, R. P., et al. (2013).Actinidia DRM1 An intrinsically disordered protein whose mRNA expression is inversely correlated with spring budbreak in kiwifruit. PLoS ONE 8:e57354. doi: 10.1371/journal.pone.0057354
86. You, J., Zhang, L., Song, B., Qi, X., and Chan, Z. (2015). Systematic analysis and identification of stress-responsive genes of the NAC gene family in Brachypodium distachyon. PLoS ONE 10:e0122027. doi: 10.1371/journal.pone.0122027
87. Zheng, C., Halaly, T., Kwame Acheampong, A., Takebayashi, Y., Jikumaru, Y., Kamiya, Y., et al. (2015). Abscisic Acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J. Exp. Bot. 66, 1527-1542. doi: 10.1093/jxb/eru519
88. Zhong, R., Lee, C., and Ye, Z.-H. (2010). Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci. 15, 625-632. doi: 10.1016/j.tplants.2010.08.007
89. Zhou, X., He, F., Liu, F., Zheng, X., Di, C., Zhou, S., et al. (2007). "Integration of cold signal transduction pathway related to ABA 8'- hydroxylase in Arabidopsis," inBiotechnology and Sustainable Agriculture 2006 and Beyond, ed Z. Xu (Dordrecht: Springer), 414-474.