Winter Injury to Grapevine Secondary Phloem and Cambium Impairs Budbreak, Cambium Activity, and Yield Formation

Abstract

Vitis vinifera is a species of temperate origin that reactivates the dormant secondary phloem from the previous year at the resumption of growth in spring. Following harsh winters, grapevines may display a set of symptoms including delayed and heterogeneous budbreak, dieback with shoot renewal from the trunk base or sudden death of the plant. Although it was suggested that these symptoms may be associated with freeze damage to the secondary phloem, there is no experimental evidence that quantifies tissue responses to freezing and their consequences for the plant. This work evaluated how different severities of cold damage to the secondary phloem during the dormant season impacted the anatomical, physiological, and agronomic responses of grapevines during the subsequent growing season. Single-node cane sections were subjected to a range of freezing temperatures that damaged only the phloem, and changes in anatomy and physiology were monitored. In addition, the consequences of natural winter freezes for yield formation of field-grown plants were evaluated. Our results suggest that the more severe a freeze event is, the greater will be the degree of secondary phloem disorganization, leading to delays in budbreak and subsequent phenological stages, and in cambial activity. Winter freezes also led to a loss of plant vigor and a reduction in cluster number, berries per cluster, and fruit sugar content. We conclude that winter freeze events can produce hidden damage in grapevine perennial tissues, which may compromise subsequent growth and productivity depending on the severity of the damage.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Ahmedullah M (1985) An analysis of winter injury to grapevines as a result of two severe winters in Washington. Fruit Var J 39(4):29–34

    Google Scholar 

  2. Aloni R, Peterson CA (1991) Seasonal changes in callose levels and fluorescein translocation in the phloem of Vitis vinifera L. IAWA J 12(3):223–234. https://doi.org/10.1163/22941932-90001247

    Article  Google Scholar 

  3. Aloni R, Raviv A, Peterson CA (1991) The role of auxin in the removal of dormancy callose and resumption of phloem activity in Vitis vinifera. Can J Bot 69(8):1825–1832. https://doi.org/10.1139/b91-232

    CAS  Article  Google Scholar 

  4. Bates TR, Dunst RM, Joy P (2002) Seasonal dry matter, starch, and nutrient distribution in ‘Concord’ grapevine roots. HortScience 37(2):313–316. https://doi.org/10.21273/HORTSCI.37.2.313

    Article  Google Scholar 

  5. Brusky-Odneal M (1983) Winter bud injury of grapevines 1981–1982. Fruit Var J 37(2):45–51

    Google Scholar 

  6. Caspari HW, Lang A, Alspach P (1998) Effects of girdling and leaf removal on fruit set and vegetative growth in grape. Am J Enol Vitic 49(4):359–366

    Google Scholar 

  7. Chen JJ, Zhang J, He XQ (2014) Tissue regeneration after bark girdling: an ideal research tool to investigate plant vascular development and regeneration. Physiol Plant 151(2):147–155. https://doi.org/10.1111/ppl.12112

    CAS  Article  PubMed  Google Scholar 

  8. Cragin J, Serpe M, Keller M, Shellie K (2017) Dormancy and cold hardiness transitions in wine grape cultivars Chardonnay and Cabernet Sauvignon. Am J Enol Vitic 68(2):195–202. https://doi.org/10.5344/ajev.2016.16078

    Article  Google Scholar 

  9. Davis JD, Evert RF (1968) Seasonal development of the secondary phloem in Populus tremuloides. Bot Gaz 129(1):1–8

    Article  Google Scholar 

  10. Davis JD, Evert RF (1970) Seasonal cycle of phloem development in woody vines. Bot Gaz 131(2):128–138

    Article  Google Scholar 

  11. Delpierre N, Vitasse Y, Chuine I, Guillemot J, Bazot S, Rathgeber CB (2016) Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models. Ann For Sci 73(1):5–25. https://doi.org/10.1007/s13595-015-0477-6

    Article  Google Scholar 

  12. Derr WF, Evert RF (1967) The cambium and seasonal development of the phloem in Robinia pseudoacacia. Am J Bot 54(2):147–153. https://doi.org/10.1002/j.1537-2197.1967.tb06903.x

    Article  Google Scholar 

  13. Di Rienzo JA, Guzman AW, Casanoves F (2002) A multiple-comparisons method based on the distribution of the root node distance of a binary tree. J Agric Biol Environ Stat 7:129–142. https://doi.org/10.1198/10857110260141193

    Article  Google Scholar 

  14. Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2017) InfoStat versión 2016. Grupo InfoStat, FCA. Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar

  15. Eichhorn KW, Lorenz DH (1977) Phenological development stages of the grape vine. Nachr Dtsch Pflanzenschutzd 29(8):119–120

    Google Scholar 

  16. Eltom M, Trought M, Winefield C (2013) The effects of cane girdling before budbreak on shoot growth, leaf area and carbohydrate content of Vitis vinifera L. Sauvignon Blanc grapevines. Funct Plant Biol 40(7):749–757. https://doi.org/10.1071/FP12278

    CAS  Article  PubMed  Google Scholar 

  17. Esau K (1948) Phloem structure in the grapevine, and its seasonal changes. Hilgardia 18(5):217–296. https://doi.org/10.3733/hilg.v18n05p217

    Article  Google Scholar 

  18. Evert RF (1960) Phloem structure in Pyrus communis L. and its seasonal changes. Calif Univ Publ Bot 32:127–194

    Google Scholar 

  19. Fuller MP, Telli G (1999) An investigation of the frost hardiness of grapevine (Vitis vinifera) during bud break. Ann Appl Biol 135:589–595. https://doi.org/10.1111/j.1744-7348.1999.tb00891.x

    Article  Google Scholar 

  20. Goffinet M (2004) Anatomy of grapevine winter injury and recover. Cornell University Department of Horticultural Sciences, NY State Agricultural Experiment Station, Geneva

    Google Scholar 

  21. Gonzalez Antivilo F, Paz RC, Keller M, Borgo R, Tognetti J, Roig Juñent F (2017) Macro-and microclimate conditions may alter grapevine deacclimation: variation in thermal amplitude in two contrasting wine regions from North and South America. Int J Biometeorol 61(12):2033–2045. https://doi.org/10.1007/s00484-017-1400-7

    Article  Google Scholar 

  22. Gonzalez Antivilo F, Paz RC, Echeverria M, Keller M, Tognetti J, Borgo R, Roig Juñent F (2018) Thermal history parameters drive changes in physiology and cold hardiness of young grapevine plants during winter. Agric For Meteorol 262:227–236. https://doi.org/10.1016/j.agrformet.2018.07.017

    Article  Google Scholar 

  23. Greer DH, Sicard SM (2009) The net carbon balance in relation to growth and biomass accumulation of grapevines (Vitis vinifera cv. Semillon) grown in a controlled environment. Funct Plant Biol 36(7):645–653. https://doi.org/10.1071/FP09037

    Article  PubMed  Google Scholar 

  24. Hill AW (1908) The histology of the sieve-tubes of angiosperms. Ann Bot 22(86):245–290

    Article  Google Scholar 

  25. Howell GS, Shaulis N (1980) Factors influencing within-vine variation in the cold resistance of cane and primary bud tissues. Am J Enol Vitic 31(2):158–161

    Google Scholar 

  26. Hunter JJ (2000) Implications of seasonal canopy management and growth compensation in grapevine. S Afr J Enol Vitic 21(2):81–91. https://doi.org/10.21548/21-2-2215

    Article  Google Scholar 

  27. Hunter JJ, Ruffner HP, Volschenk CG (1995) Starch concentrations in grapevine leaves, berries and roots and the effect of canopy management. S Afr J Enol Vitic 16(2):35–40. https://doi.org/10.21548/16-2-2270

    CAS  Article  Google Scholar 

  28. Keller M, Mills LJ (2007) Effect of pruning on recovery and productivity of cold-injured merlot grapevines. Am J Enol Vitic 58(3):351–357

    Google Scholar 

  29. Keming C, Pengzhe L, Qinghua L, Zhengli L (1989) Regeneration of vascular tissues in Broussonetia papyrifera stems after removal of the xylem. IAWA J 10(2):193–199. https://doi.org/10.1163/22941932-90000488

    Article  Google Scholar 

  30. Lang GA (1987) Endo-, para-and ecodormancy: physiological terminology and classification for dormancy research. HortScience 22(3):271–277

    Google Scholar 

  31. Lang GA, Early JD, Arroyave NJ, Darnell RL, Martin GC, Stutte GW (1985) Dormancy: toward a reduced, universal terminology. HortScience 20(5):809–811

    Google Scholar 

  32. Levitt J (1980) Responses of plants to environmental stress, volume 1: chilling, freezing, and high temperature stresses. Academic Press, New York

    Google Scholar 

  33. Lindén L (2002) Measuring cold hardiness in woody plants. Doctoral Thesis. University of Helsinki, Finland

  34. Marchi S, Tognetti R, Minnocci A, Borghi M, Sebastiani L (2008) Variation in mesophyll anatomy and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus persica) and an evergreen sclerophyllous Mediterranean shrub (Olea europaea). Trees 22(4):559. https://doi.org/10.1007/s00468-008-0216-9

    CAS  Article  Google Scholar 

  35. Meiering AG, Paroschy JH, Peterson RL, Hostetter G, Neff A (1980) Mechanical freezing injury in grapevine trunks. Am J Enol Vitic 31(1):81–89

    Google Scholar 

  36. Mills LJ, Ferguson JC, Keller M (2006) Cold-hardiness evaluation of grapevine buds and cane tissues. Am J Enol Vitic 57:194–200

    Google Scholar 

  37. Moran RE, Sun Y, Geng F, Zhang D, Fazio G (2011) Cold temperature tolerance of trunk and root tissues in one-or two-year-old apple rootstocks. HortScience 46(11):1460–1464. https://doi.org/10.21273/HORTSCI.46.11.1460

    Article  Google Scholar 

  38. Pang Y, Zhang J, Cao J, Yin SY, He XQ, Cui KM (2008) Phloem transdifferentiation from immature xylem cells during bark regeneration after girdling in Eucommia ulmoides Oliv. J Exp Bot 59(6):1341–1351. https://doi.org/10.1093/jxb/ern041

    CAS  Article  PubMed  Google Scholar 

  39. Pierquet P, Stushnoff C (1980) Relationship of low temperature exotherms to cold injury in Vitis riparia Michx. Am J Enol Vitic 31(1):1–6

    Google Scholar 

  40. Pratt C, Pool RM (1981) Anatomy of recovery of canes of Vitis vinifera L. from simulated freezing injury. Am J Enol Vitic 32(3):223–227

    Google Scholar 

  41. Prislan P, Čufar K, Koch G, Schmitt U, Gričar J (2013) Review of cellular and subcellular changes in the cambium. IAWA journal 34(4):391–407. https://doi.org/10.1163/22941932-00000032

    Article  Google Scholar 

  42. Proebsting EL, Ahmedullah M, Brummund VP (1980) Seasonal changes in low temperature resistance of grape buds. Am J Enol Vitic 31(4):329–336

    Google Scholar 

  43. Raitio H (1992) Anatomical symptoms in the wood of Scots pine damaged by frost and pine bark bugs. Flora 186(3–4):187–193. https://doi.org/10.1016/S0367-2530(17)30535-2

    Article  Google Scholar 

  44. Rathgeber CB, Cuny HE, Fonti P (2016) Biological basis of tree-ring formation: a crash course. Front Plant Sci 7:734. https://doi.org/10.3389/fpls.2016.00734

    Article  PubMed  PubMed Central  Google Scholar 

  45. Scholefield PB, Neales TP, May P (1978) Carbon balance of the sultana vine (Vitis vinifera L.) and the effects of autumn defoliation by harvest pruning. Aust J Plant Physiol 5:561–570. https://doi.org/10.1071/PP9780561

    CAS  Article  Google Scholar 

  46. Sidlowski JJ (1977) Physiological and ultrastructural investigations of callused grape trunk girdles. Doctoral Thesis. University of Arizona, United States

  47. ImagePro 4.5 Media Cybernetics. Silver Spring: Media Cybernetics (2002) http://www.mediacy.com/action.htm

  48. Strik BC, Connelly AE, Lombard PB (1992) Assessment of winter injury of grapevines in Oregon. AGRIS 901:1–30

    Google Scholar 

  49. Todaro TM, Dami IE (2017) Cane morphology and anatomy influence freezing tolerance in Vitis vinifera Cabernet franc. Int J Fruit Sci 17(4):391–406. https://doi.org/10.1080/15538362.2017.1330667

    Article  Google Scholar 

  50. Turgeon R (2006) Phloem loading: how leaves gain their independence. Bioscience 56(1):15–24. https://doi.org/10.1641/0006-3568(2006)056%5b0015:PLHLGT%5d2.0.CO;2

    Article  Google Scholar 

  51. Wample RL, Wolf TK (1996) Practical considerations that impact vine cold hardiness. In: Henick-Kling T, Wolf TE, Harkness EM (eds) Proceedings of the 4th international symposium cool climate viticulture and enology. New York State Agri-cultural Experiment Station, Geneva, New York, pp 23–28

  52. Weiser CJ (1970) Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169(3952):1269–1278. https://doi.org/10.1126/science.169.3952.1269

    CAS  Article  PubMed  Google Scholar 

  53. Williams LE, Retzlaff WA, Yang W, Biscay PJ, Ebisuda N (2000) Effect of girdling on leaf gas exchange, water status, and non-structural carbohydrates of field-grown Vitis vinifera L. (cv. Flame Seedless). Am J Enol Vitic 51(1):49–54

    CAS  Google Scholar 

  54. Wolfe W (2001) Vine and vineyard management following low temperature injury. In: Proceedings of the ASEV 50th anniversary annual meeting, Seattle, Washington, 19–23 June, 2000. American Society for Enology and Viticulture, ASEV, pp 101–110

  55. Zabadal TJ, Dami IE, Goffinet MC, Martinson TE, Chien ML (2007) Winter injury to grapevines and methods of protection. Michigan State University Extension, Lansing

    Google Scholar 

  56. Zapata C, Deléens E, Chaillou S, Magné C (2004a) Partitioning and mobilization of starch and N reserves in grapevine (Vitis vinifera L.). J Plant Physiol 161(9):1031–1040. https://doi.org/10.1016/j.jplph.2003.11.009

    CAS  Article  PubMed  Google Scholar 

  57. Zapata C, Deléens E, Chaillou S, Magné C (2004b) Mobilization and distribution of starch and total N in two grapevine cultivars differing in their susceptibility to shedding. Funct Plant Biol 31(11):1127–1135. https://doi.org/10.1071/FP04028

    CAS  Article  PubMed  Google Scholar 

  58. Zhang J, Gao G, Chen JJ, Taylor G, Cui KM, He XQ (2011) Molecular features of secondary vascular tissue regeneration after bark girdling in Populus. New Phytol 192(4):869–884. https://doi.org/10.1111/j.1469-8137.2011.03855.x

    CAS  Article  PubMed  Google Scholar 

  59. Zufferey V, Murisier F, Vivin P, Belcher S, Lorenzini F, Spring JL, Viret O (2012) Carbohydrate reserves in grapevine (Vitis vinifera L. ‘Chasselas’): the influence of the leaf to fruit ratio. Vitis 51(3):103–110

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Agencia Nacional de Promoción Científica y Tecnológica, Argentina (ANPCyT); Universidad Nacional de Cuyo (UNCuyo) [PRH, 2007]; and Concejo Nacional de Investigaciones Científicas y Técnicas (CONICET) [PhD fellowship, 2016–2018]. We thank the staff of the Plant Physiology Department and Biological Chemistry of Agronomy Faculty of UNCuyo Mendoza (especially Bruno Cavagnaro and Emiliano Malovini); Viticulture Laboratory at Washington State (especially Lynn Mills, John Ferguson, and Alan Kawakami), DAAC (especially Inés Krause, Laura Ventura, Daniel Ferrero, Vanina Gonzalez, and Natalia Astorga); INTA EEA Mendoza Ecophysiology Department (especially Jorge Perez Peña, Eugenia Galat Giorgi, and Jorge Prieto); IANIGLA CCT-Mendoza (especially Federico Gonzalez and Silvina Lassa); and Facundo Bonamaizon for sharing their knowledge, equipment, and technical support. Moreover, we thank all the students that participated in this research. Mercier Plant Nursery supplied the plant material for this research, and Floralis provided access to laboratory infrastructure and equipment.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Francisco Gonzalez Antivilo.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure 1

Supplementary material 1 (TIFF 4843 kb) . Photographs of phloem damage due to winter freeze events in field-grown V. vinifera grapevines in the province of Mendoza, Argentina. A) Plant with successive retraining attempts following trunk death. B) plant with dead cordons requiring renewal. C) Young plant and D) mature plant with dead trunk and regrowth of suckers at the base of the trunk; E) trunk with dead (brown) phloem and live (green) xylem. Authors photos.

Supplementary Figure 2

Supplementary material 2 (TIFF 2383 kb) . Sketch of methodology used to determine the effects of simulated freezing events on anatomical and phenological responses of single-node cuttings of V. vinifera cv. Malbec. Tests were conducted before budbreak in samples collected from the field. DAY 1: a) Twenty dormant canes were collected from a commercial vineyard and kept in airtight bags with moist paper in a Styrofoam box for transport to the laboratory, where the canes were processed immediately. b) Basal cane portions (buds 1 through 8) were divided into 3-cm sections and mixed to obtain a composite sample. Five sections were randomly selected from the composite sample and wrapped in aluminum foil. In total, ten packages were made. c) Each package was tagged and assigned to a simulated freezing event from -2 to -18 °C at 2 °C increments. A control treatment was maintained at room temperature. d) Packages were placed inside a freezer controlled by a data-logger-computer. e) Once the temperature had dropped from ambient to 10 °C, a drop rate of -2 °C/h was maintained down to -19 °C. The temperature was recorded in real-time with an integrated DS18B20 sensor. f) Once a package reached its target temperatures it was removed from the freezer and deposited in a box at 7 °C for 24 hours. Then, packages were maintained at 20 °C for another 24 h. g) Samples were examined for brown discoloration under a stereoscope to determine if phloem and xylem tissues were alive or dead. The proportion of live tissue was recorded for each target temperature to determine phloem LT50. DAY 2: Eighty dormant canes were collected as described for DAY 1. h) Based on the LT50 obtained on DAY 1, three temperature treatments were applied, one coincident with LT50 (FTMed) and two other treatments below and above this measurement (sublethal: FTLow; and superlethal: FTHigh). Untreated samples were considered the control (Ctr). i) Single-node cuttings (n = 50) were subjected to the same type of freezing simulation but with different target temperatures. After the simulated freezing events, the cuttings were kept in trays with water at 20 °C and a photoperiod of 16 h to assess phenological development (n = 20) and anatomical changes (n = 30). j) Phenology was evaluated visually every 3 days. k) Anatomy was studied in cuttings sampled every 7 days and fixed prior to sectioning. FT means Freezing treatment.

Supplementary Figure 3

Supplementary material 3 (TIFF 1446 kb) . Classification criteria for different phases of cambium activity used in this study. Phase 0: dormant cambium; Phase 1: beginning of cell division; Phase 2: cell elongation; Phase 3: cell wall thickening and lignification. Micrographs in 40× magnification, bars indicate 200 μm. p = phloem; c = cambium; x = xylem. Authors photos.

Supplementary Figure 4

Supplementary material 4 (TIFF 1419 kb) . Sketch of sampling protocol in a commercial vineyard to evaluate trunk damage and vegetative and reproductive responses of V. vinifera cv. Malbec grapevines in the province of Mendoza, Argentina. a) Grapevines prior to budbreak. b) Tangential cuts in vine trunks to determine phloem damage by visual observation. c) Healthy plants with live xylem and live (green) phloem. d) Damaged plants with dead (brown) phloem and live xylem. e and f) Plants were tagged for subsequent evaluation at harvest. g and h) Yield and vigor measurements were made at harvest.

Supplementary Figure 5

Supplementary material 5 (TIFF 9426 kb) . Photos of typical differences in vigor and yield of V. vinifera cv. Malbec grapevines tagged prior to budbreak and grown in a commercial vineyard in the province of Mendoza, Argentina. A and C) “No cold damage”: Healthy plants with shoots of normal vigor and yield formation. B and D) “Phloem damage”: Plants affected by cold damage to the trunk phloem with stunted shoots and reduced yield. Authors photos.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gonzalez Antivilo, F., Paz, R.C., Tognetti, J. et al. Winter Injury to Grapevine Secondary Phloem and Cambium Impairs Budbreak, Cambium Activity, and Yield Formation. J Plant Growth Regul 39, 1095–1106 (2020). https://doi.org/10.1007/s00344-019-10051-w

Download citation

Keywords

  • Vitis vinifera
  • Freeze damage
  • Phenology
  • Secondary phloem
  • Cambial activity
  • Cold hardiness