Cold Stress-Induced Disease Resistance (SIDR): indirect effects of low temperatures on host-pathogen interactions and disease progress in the grapevine powdery mildew pathosystem

European Journal of Plant Pathology

Volumn 144, Issue 4, 2016, Pages 695-705

  Moyer, Michelle M ^a   Londo, Jason ^b   Gadoury, David M ^c   Cadle Davidson, Lance ^b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c New York State Agricultural Experiment Station   (United States)

Author keywords

Cold shock; Powdery mildew; Stress physiology

Indexed keywords

DISEASE PREVALENCE; DISEASE RESISTANCE; FUNGAL DISEASE; HOST-PATHOGEN INTERACTION; LOW TEMPERATURE; NICHE; PHYSIOLOGICAL RESPONSE; STRESS RESISTANCE; VINE;

AMPELOPSIS; ERYSIPHALES; ERYSIPHE NECATOR; PARTHENOCISSUS; VITACEAE; VITIS;

EID: 84960447285     PISSN: 09291873     EISSN: 15738469     Source Type: Journal    
DOI: 10.1007/s10658-015-0745-1     Document Type: Article

References (68)

1. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., & Genschik, P. (2008). The cold-inducible CBF1 factor–dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell, 20, 2117–2129.
2. Austin, C. N., & Wilcox, W. F. (2011). Effects of fruit-zone leaf removal, training systems, and irrigation on the development of grapevine powdery mildew. American Journal of Enology and Viticulture, 62, 193–198.
3. Austin, C. N., & Wilcox, W. F. (2012). Effects of sunlight exposure on grapevine powdery mildew development. Phytopathology, 102, 857–866.
4. Bendek, C. E., Campbell, P. A., Torres, R., Donoso, A., & Latorre, B. A. (2007). The risk assessment index in grape powdery mildew control decisions and the effect of temperature and humidity on conidial germination of Erysiphe necator. Spanish Journal of Agricultural Research, 5, 522–532.
5. Berry, J., & Bjorkman, O. (1980). Photosynthetic response and adaption to temperature in higher plants. Annual Review of Plant Physiology, 31, 491–543.
6. Bogoni, M., Panont, A., Valenti, L., & Scienza, A. (1993). Effects of soil physical and chemical conditions on grapevine nutritional status. Acta Horticulturae, 383.
7. Buttrose, M. S., & Hale, C. R. (1973). Effect of temperature on development of the grapevine inflorescence after bud burst. American Journal of Enology and Viticulture, 24, 14–16.
8. Caffi, T., Rossi, V., Legler, S. E., & Bugiani, R. (2011). A mechanistic model simulating ascosporic infections by Erysiphe necator, the powdery mildew fungus of grapevine. Plant Pathology, 60, 522–531.
9. Caffi, T., Legler, S. E., & Rossi, V. (2012). Evaluation of a warning system for early-season control of grapevine powdery mildew. Plant Disease, 96, 104–110.
10. Calonnec, A., Cartolaro, P., Naulin, J. M., Bailey, D., & Langlais, M. (2008). A host-pathogen simulation model: powdery mildew of grapevine. Plant Pathology, 57, 493–508.
11. Carroll, J. E., & Wilcox, W. F. (2003). Effects of humidity on the development of grapevine powdery mildew. Phytopathology, 93, 1137–1144.
12. Chellemi, D. O., & Marois, J. J. (1991a). Development of a demographic growth model for Uncinula necator by using a microcomputer spreadsheet program. Phytopathology, 81, 250–254.
13. Chellemi, D. O., & Marois, J. J. (1991b). Effect of fungicide and water on sporulation of Uncinula necator. Plant Disease, 75, 455–457.
14. Chellemi, D. O., & Marois, J. J. (1991c). Sporulation of Uncinula necator on grape leaves as influenced by temperature and cultivar. Phytopathology, 81, 197–201.
15. Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B.-h., Hong, X., Agarwal, M., & Zhu, J.-K. (2003). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes and Development, 17, 1043–1054.
16. Choudhury, R. A., McRoberts, N., & Gubler, W. D. (2014). Effects of punctuated heat stress on the grapevine powdery mildew pathogen, Erysiphe necator. Phytopathologia Mediterranea, 53, 148–158.
17. Crosatti, C., Rizza, F., Badeck, F. W., Mazzucotelli, E., & Cattivelli, L. (2013). Harden the chloroplast to protect the plant. Physiologia Plantarum, 147, 55–63.
18. Delp, C. J. (1954). Effect of temperature and humidity on the grape powdery mildew fungus. Phytopathology, 44, 615–626.
19. Diehl, H. J., & Heintz, C. (1987). Studies on the generative reproduction of grapevine powdery mildew (Uncinula necator Berk.). Vitis, 26, 114–122.
20. Dry, P. R., & Loveys, B. R. (1998). Factors influencing grapevine vigour and the potential for control with partial rootzone drying. Australian Journal of Grape and Wine Research, 4, 140–148.
21. Ferguson, J. C., Tarara, J. M., Mills, L. J., Grove, G. G., & Keller, M. (2011). Dynamic thermal time model of cold hardiness for dormant grapevine buds. Annals of Botany (London), 107, 389–396.
22. Ferguson, J. C., Moyer, M. M., Mills, L. J., Hoogenboom, G., & Keller, M. (2014). Modeling dormant bud cold hardiness and budbreak in 23 Vitis genotypes reveals variation by region of origin. American Journal of Enology and Viticulture, 65, 59–71.
23. Ferrini, F., Mattii, G. B., & Nicese, F. P. (1995). Effect of temperatre on key physiological responses of grapevine leaf. American Journal of Enology and Viticulture, 46, 375–379.
24. 2 uptake when photosynthesis in grapevine leaves is inhibited following low night temperatures and/or water stress. Plant Physiology, 121, 675–684.
25. Gadoury, D. M., & Pearson, R. C. (1988). Initiation, development, dispersal and survival of cleistothecia of Uncinula necator in New York vineyards. Phytopathology, 78, 1413–1421.
26. Gadoury, D. M., & Pearson, R. C. (1990). Germination of ascospores and infection of Vitis by Uncinula necator. Phytopathology, 80, 1198–1203.
27. Gadoury, D. M., Pearson, R. C., Seem, R. C., & Park, E. W. (1997a). Integrating the control programs for fungal diseases of grapevine in the northeastern United States. Viticultural and Enological Sciences, 52, 140–147.
28. Gadoury, D. M., Seem, R. C., Magarey, P. A., Emmett, R., & Magarey, R. (1997b). Effects of environment and fungicides on epidemics of grape powdery mildew: considerations for practical model development and disease management. Viticultural and Enological Sciences, 52, 225–229.
29. Gadoury, D. M., Seem, R. C., Ficke, A., & Wilcox, W. F. (2003). Ontogenic resistance to powdery mildew in grape berries. Phytopathology, 93, 547–555.
30. Greer, D. H., & Weedon, M. M. (2013). The impact of high temperatures on Vitis vinifera cv. Semillon grapevine performance and berry ripening. Frontiers in Plant Science, 4, 1–9.
31. Haake, V., Cook, D., Riechmann, J. L., Pineda, O., Thomashow, M. F., & Zhang, J. Z. (2002). Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiology, 130, 639–648.
32. Hall, T. W., & Mahaffee, W. F. (2001). Impact of vine shelter use on development of grape powdery mildew. American Journal of Enology and Viticulture, 52, 204–209.
33. Heintz, C., & Blaich, R. (1990). Ultastructural and histochemical studies on interactions between Vitis vinifera L. and Uncinula necator (Schw.) burr. New Phytologist, 115, 107–117.
34. Hendrickson, L., Ball, M. C., Wood, J. T., Chow, W. S., & Furbank, R. T. (2004). Low temperature effects on photosynthesis and growth of grapevine. Plant, Cell and Environment, 27, 795–809.
35. Jailloux, F., Willocquet, L., Chapuis, L., & Froidefond, G. (1999). Effect of weather factors on the release of ascospores of Uncinula necator, the cause of grape powdery mildew, in Bordeaux region. Canadian Journal of Botany, 77, 1044–1051.
36. Jones, G. V., & Davis, R. E. (2000). Climate influences on grapevine phenology, grape composition and wine production and quality for Bordeaux, France. American Journal of Enology and Viticulture, 51, 249–261.
37. Kast, W.K., & Bleyer, K. (2010). The expert system OiDiag-2.2- a useful tool for the precise scheduling of sprays against powdery mildew of vine (Erysiphe necator) Schwein. Proc. 6th International Workshop on Grapevine Downy and Powdery Mildew, Bordeaux 2010. In A. Calonnec et al. (Ed), Bordeaux: INRA-INITA.
38. Keller, M., & Tarara, J. M. (2010). Warm spring temperatures induce persistent season-long changes in shoot development in grapevines. Annals of Botany, 106, 131–141.
39. Keller, M., Rogiers, S. Y., & Schultz, H. R. (2003). Nitrogen and ultaviolet radiation modify grapevine susceptibility to powdery mildew. Vitis, 42, 87–94.
40. Knight, M. R., & Knight, H. (2012). Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytologist, 195, 737–751.
41. Knight, M. R., Campbell, A. K., Smith, S. M., & Trewavas, A. J. (1991). Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature, 352, 524–526.
42. Kohorn, B. D. (2000). Plasma membrane-cell wall contacts. Update on Cell Biology, 124, 31–38.
43. Legler, S. E., Caffi, T., & Rossi, V. (2012a). A nonlinear model for temperature-dependent development of Erysiphe necator chamosthecia on grapevine leaves. Plant Pathology, 61, 96–105.
44. Legler, S.E., Caffi, T., & Rossi, V. (2012b). Sanitation and disease modeling can help powdery mildew control in organic viticulture (abstr.). Phytopathology.
45. Mellersh, D. G., & Heath, M. C. (2001). Plasma membrane - cell wall ashesion is required for expression of plant defense responses during fungal penetration. The Plant Cell, 13, 413–424.
46. Merry, A. M., Evans, K. J., Corkrey, R., & Wilson, S. J. (2013). Coincidence of maximum severity of powdery mildew on grape leaves and the carbohyrdrate sink-to-source transition. Plant Pathology (Oxford), 62, 842–850.
47. Miura, K., & Furumoto, T. (2013). Cold signaling and cold response in plants. International Journal of Molecular Sciences, 14, 5312–5337.
48. Miura, K., & Hasegawa, P. M. (2008). Regulation of cold signaling by sumoylation of ICE1. Plant Signaling & Behavior, 3, 52–53.
49. Miura, K., Jin, J. B., Lee, J., Yoo, C. Y., Stirm, V., Miura, T., Ashworth, E. N., Bressan, R. A., Yun, D.-J., & Hasegawa, P. M. (2007). SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. The Plant Cell, 19, 1403–1414.
50. Mizoi, J., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2012). AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)- Gene Regulatory Mechanisms, 1819, 86–96.
51. Moyer, M. M., Gadoury, D. M., Cadle-Davidson, L., Dry, I. B., Magarey, P. A., Wilcox, W. F., & Seem, R. C. (2010). Effects of acute low temperature events on the development of Erysiphe necator and susceptibility of Vitis vinifera. Phytopathology, 100, 1240–1249.
52. Moyer, M. M., Gadoury, D. M., Wilcox, W. F., & Seem, R. C. (2014). Release of Erysiphe necator ascospores and impact of early-season disease pressure on Vitis vinifera fruit infection. American Journal of Enology and Viticulture, 65, 315–324.
53. Novillo, F., Medina, J., & Salinas, J. (2007). Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proceedings of the National Academy of Sciences, 104, 21002–21007.
54. Novillo, F., Medina, J., Rodríguez-Franco, M., Neuhaus, G., & Salinas, J. (2011). Genetic analysis reveals a complex regulatory network modulating CBF gene expression and Arabidopsis response to abiotic stress. Journal of Experimental Botany, 293–304.
55. Öquist, G., & Huner, N. P. A. (2003). Photosynthesis of overwintering evergreen plants. Annual Review of Plant Biology, 54, 329–355.
56. Örvar, B. L., Sangwan, V., Omann, F., & Dhindsa, R. S. (2000). Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. The Plant Journal, 23, 785–794.
57. Palusa, S. G., Ali, G. S., & Reddy, A. S. N. (2007). Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. The Plant Journal, 49, 1091–1107.
58. Parker, A. K., De Cortázar-Atauri, I. G., Van Leeuwen, C., & Chuine, I. (2011). General phenological model to characterise the timing of flowering and veraison of Vitis vinifera L. Australian Journal of Grape and Wine Research, 17, 206–216.
59. Peduto, F., Backup, P., Hand, E. K., Janousek, C. N., & Gubler, W. D. (2013). Effect of high temperature and exposure time on Erysiphe necator growth and reproduction: Revisions to the UC Davis powdery pildew risk index. Plant Disease, 97, 1438–1447.
60. Rossi, V., Caffi, T., & Legler, S. E. (2010). Dynamics of ascospore maturation and discharge in Erysiphe necator, the causal agent of grape powdery mildew. Phytopathology, 100, 1321–1329.
61. Rumbolz, J., Kassemeyer, H. H., Steinmetz, V., Deising, H. B., Mendgen, K., Mathys, D., Wirtz, S., & Guggenheim, R. (2000). Differentiation of infection structures of the powdery mildew fungus Uncinula necator and adhesion to the host cuticle. Canadian Journal of Botany, 78, 409–421.
62. Sall, M. A. (1980). Epidemiology of grape powdery mildew: a model. Phytopathology, 70, 338–342.
63. Seem, R. C. (1984). Disease incidence and severity relationships. Annual Review of Phytopathology, 22, 133–150.
64. Tonkinson, C. L., Lyndon, R. F., Arnold, G. M., & Lenton, J. R. (1997). The effects of temperature and the Rht3 dwarfing gene on growth, cell extension, and gibberellin content and responsiveness in the wheat leaf. Journal of Experimental Botany, 48, 963–970.
65. Vanderplank, J. E. (1982). Host-pathogen interactions in plant disease. New York: Academic Press, Inc.
66. Xiao, H., Tattersall, E. A. R., Siddiqua, M. K., Cramer, G. R., & Nassuth, A. (2008). CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant, Cell & Environment, 31, 1–10.
67. Zhang, Y., Mechlin, T., & Dami, I. E. (2011). Foliar application of abscisic acid induces dormancy responses in greenhouse-grown grapevines. Hortscience, 46, 1271–1277.
68. Zhou, X., Wang, G., Sutoh, K., Zhu, J.-K., & Zhang, W. (2008). Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1779, 780–788.