Abstract
Main conclusions
This study demonstrated that freeze-induced hydraulic failure varies between two Vitis species that have different xylem vessel frequency and grouping. However, seasonal recovery of young grapevines was similar between the species.
Abstract
Sub-freezing temperatures after budburst represent a major threat for the cultivation of fruit crops in temperate regions. Freeze stress might disrupt xylem hydraulic functionality and plant growth; however, it is unclear if hydraulic traits influence the ability of woody plants to cope with freeze stress. We investigated if a grapevine species (Vitis hybrid) with earlier budburst had anatomical traits that cause higher freeze-induced hydraulic failure but also confer a greater ability for seasonal recovery compared to a Vitis vinifera species. Two-year-old Vitis hybrid and vinifera grapevines were container-grown outdoors, assigned to either a control (n = 40) or a freeze-stressed (n = 40) treatment and exposed to a controlled-temperature (− 4 °C) freeze stress shortly after budburst. We found that the Vitis hybrid had greater stem-specific hydraulic conductivity (Ks) and was more vulnerable to freeze-induced embolism compared to the V. vinifera species, which exhibited a less efficient but safer water transport strategy. Seventy-two hours after the freeze stress, Ks of freeze-stressed V. vinifera was 77.8% higher than that of the control, indicating hydraulic recovery. While the two species did not differ in xylem vessel diameter, Vitis hybrid exhibited higher vessel frequency and percentage of vessel grouping, which could explain its higher Ks and greater freeze-induced Ks loss compared to the V. vinifera vines. While the two species varied in the short-term hydraulic response, they exhibited similar and full hydraulic and vegetative recovery by midseason, including bud freeze tolerance during the following fall and mid-winter.
Similar content being viewed by others
Abbreviations
- C:
-
Control vines
- FS:
-
Freeze-stressed vines
- Kp :
-
Plant hydraulic conductance
- Ks :
-
Stem-specific hydraulic conductivity
- VD:
-
Vessel diameter
- VF:
-
Vessel frequency
- WUE:
-
Water use efficiency
- A:
-
Net assimilation rate
- E:
-
Transpiration rate
References
Atkinson CJ, Else MA, Taylor L, Dover CJ (2003) Root and stem hydraulic conductivity as determinants of growth potential in grafted trees of apple (Malus pumila Mill.). J Exp Bot 54:1221–1229
Basile B, Marsal J, Solari LI, Tyree MT, Bryla DR, Dejong TM (2003) Hydraulic conductance of peach trees grafted on rootstocks with differing size-controlling potentials. J Hort Sci Biotechnol 78:768–774
Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA (2010) The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol 154:1088–1095
Brodersen CR, McElrone AJ, Choat B, Lee EF, Shackel KA, Matthews MA (2013) In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiol 161:1820–1829
Burke MJ, Gusta LV, Quamme HA, Weiser CJ, Li PH (1976) Freezing and injury in plants. Annu Rev Plant Physiol 27:507–528
Candolfi-Vasconcelos MC, Candolfi MP, Koblet W (1994) Retranslocation of carbon reserves from the woody storage tissues into fruit as a response to defoliation stress during the ripening period in Vitis vinifera L. Planta 192:567–573
Centinari M, Smith MS, Londo JP (2016) Assessment of freeze injury of grapevine green tissues in response to cultivars and a cryoprotectant product. HortSci 51:856–860
Centinari M, Gardner DM, Smith DE, Smith MS (2018) Impact of amigo oil and KDL on grapevine post-budburst freeze injury, yield components, and fruit and wine composition. Am J Enol Vitic 69:77–88
Charrier G, Charra-Vaskou K, Kasuga J, Cochard H, Mayr S, Améglio T (2014) Freeze-thaw stress: effects of temperature on hydraulic conductivity and ultrasonic activity in ten woody angiosperms. Plant Physiol 164:992–998
Charrier G, Torres-Ruiz JM, Badel E, Burlett R, Choat B, Cochard H, Delmas CEL, Domec JC, Jansen S, King A, Lenoir N, Martin-StPaul N, Gambetta GA, Delzon S (2016) Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiol 172:1657–1668
Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol 177:608–626
Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation, and seasonal changes in embolism. Tree Physiol 6:393–407
Coombe BG (1995) Adoption of a system for identifying grapevine growth strategies. Aust J Grape Wine Res 1:100–110
Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372
Elsner EA, Jubb GL Jr (1988) Leaf area estimation of concord grape leaves from simple linear measurements. Am J Enol Vitic 39:95–97
Fennell A (2004) Freezing tolerance and injury in grapevine. J Crop Improv 10:201–235
Friend AP, Trought MCT, Stushnoff C, Wells GH (2011) Effect of delaying budburst on shoot development and yield of Vitis vinifera L. Chardonnay ‘Mendoza’ after a spring freeze event. Aust J Grape Wine Res 17:378–382
Frioni T, Green A, Emling JE, Zhuang S, Palliotti A, Sivilotti P, Falchi R, Sabbatini P (2017) Impact of spring freeze on yield, vine performance and fruit quality of Vitis interspecific hybrid Marquette. Sci Hort 219:302–309
Fuller MP, Hamed F, Wisniewski M, Glenn DM (2003) Protection of plants from frost using hydrophobic particle film and acrylic polymer. Ann Appl Biol 143:93–97
García de Cortázar-Atauri I, Brisson N, Gaudillere JP (2009) Performance of several models for predicting budburst date of grapevine (Vitis vinifera L.). Int J Biometerol 53:317–326
Hemstad PR, Luby JJ (2000) Utilization of Vitis riparia for the development of new wine varieties with resistance to disease and extreme cold. Acta Hort 528:487–490
Hemstad PR, Luby JJ (2003) La Crescent, a new cold hardy high quality, white wine variety. Acta Hort 603:719–722
Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121
Jacobsen AL, Pratt RB, Tobin MF, Hacke UG, Ewers FW (2012) A global analysis of xylem vessel length in woody plants. Am J Bot 99:1583–1591
Jacobsen AL, Rodriguez-Zaccaro FD, Lee TF, Valdovinos J, Toschi HS, Martinez JA, Pratt RB (2015) Grapevine xylem development, architecture, and function. In: Hacke Uwe (ed) Functional and ecological xylem anatomy. Springer International Publishing, Cham, pp 133–162
Johnson DE, Howell GS (1981) Factors influencing critical temperatures for spring freeze injury to developing primary shoots on Concord grapevines. Am J Enol Vitic 32:144–149
Keller M (2015) The science of grapevines—anatomy and physiology, 2nd edn. Elsevier Academic Press, London
Knipfer T, Eustis A, Brodersen C, Walker AM, McElrone AJ (2015) Grapevine species from varied native habitats exhibit differences in embolism formation/repair associated with leaf gas exchange and root pressure. Plant Cell Environ 38:1503–1513
Knipfer T, Cuneo IF, Brodersen CR, McElrone AJ (2016) In situ visualization of the dynamics in xylem embolism formation and removal in the absence of root pressure: a study on excised grapevine stems. Plant Physiol 171:1024–1036
Kriedmann PE, Kliewer WM, Harris JM (1970) Leaf age and photosynthesis in Vitis vinifera L. Vitis 9:97–104
Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) Multi-factor treatment designs with multiple error terms. SAS for Mixed Models. SAS Institute Inc., Cary, pp 124–139
Londo J, Johnson LM (2014) Variation in the chilling requirement and budburst rate of wild Vitis species. Environ Exp Bot 106:138–147
Lovisolo C, Schubert A (1998) Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. J Exp Bot 49:693–700
Lovisolo C, Perrone I, Hartung W, Schubert A (2008) An abscisic acid-related reduced transpiration promotes gradual embolism repair when grapevines are rehydrated after drought. New Phytol 180:642–651
Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H, Schubert A (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update. Funct Plant Biol 37:98–116
Marini RP (1999) Are nonsignificant differences really not significant? HortSci 34:761–762
Massey FJ Jr (1951) The Kolmogorov–Smirnov test for goodness of fit. J Am Stat Assoc 46:68–78
Meinzer FC, McCulloh KA, Lachenbruch B, Woodruff DR, Johnson DM (2010) The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecologia 164:287–296
Melcher PJ, Holbrook NM, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem hydraulic conductivity in the laboratory and field. Methods Ecol Evol 3:685–694
Mills LJ, Ferguson JC, Keller M (2006) Cold hardiness evaluation of grapevine buds and cane tissues. Am J Enol Vitic 57:194–200
Molitor D, Caffarra A, Sinigoj P, Pertot I, Hoffmann L, Junk J (2014) Late frost injury risk for viticulture under future climate conditions: a case study for the Luxembourgish winegrowing region. Aust J Grape Wine Res 20:160–168
Mosedale JR, Wilson RJ, Maclean IMD (2015) Climate change and crop exposure to adverse weather: changes to frost risk and grapevine flowering conditions. PLoS One 10:e0141218. https://doi.org/10.1371/journal.pone.0141218
Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylems cavitation? Trees 15:14–24
Nesbitt ML, Ebel RC, Findley D, Wilkins B, Woods F, Himelrick D (2002) Assays to assess freeze injury of Satsuma mandarin. HortSci 37:871–877
Pearce RS (2001) Plant freezing and injury. Ann Bot 87:417–424
Pearce RS, Fuller MP (2001) Freezing of barley studied by infrared video thermography. Plant Physiol 125:227–240
Pitterman J, Sperry JS (2003) Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiol 23:907–914
Rodrigo J (2000) Spring frosts in deciduous fruit trees—morphological damage and flower hardiness. Sci Hort 85:155–173
Salleo S, Trifilò P, Esposito S, Nardini A, Lo Gullo MA (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Funct Plant Biol 36:815–825
Smith MS, Fridley JD, Yin J, Bauerle TL (2013) Contrasting xylem vessel constraints on hydraulic conductivity between native and non-native woody understory species. Front Plant Sci 4:486. https://doi.org/10.3389/fpls.2013.00486
Sperry JS, Pockman WT (1993) Limitaiton of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant Cell Environ 16:279–287
Sperry JS, Holbrook NM, Zimmermann HM, Tyree MT (1987) Spring filling of xylem vessels in wild grapevine. Plant Physiol 83:414–417
Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ 11:35–40
Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistivity in xylem conduits. Plant Cell Environ 28:456–465
Tramontini S, Lovisolo C (2016) Embolism formation and removal in grapevines: a phenomenon affecting hydraulics and transpiration upon water stress. In: Gerós H, Chaves MM, Medrano GH, Delrot S (eds) Grapevine in a changing environment: a molecular and ecophysiological perspective. Wiley & Sons Ltd, West Sussex, pp 135–147
Trifilò P, Lo Gullo MA, Nardini A, Pernice F, Salleo S (2007) Rootstock effects on xylem conduit dimensions and vulnerability to cavitation of Olea europaea L. Trees 21:549–556
Tsuda M, Tyree MT (2000) Plant hydraulic conductance measured by the high pressure flow meter in crop plants. J Exp Bot 51:823–828
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 11:345–360
Umebayashi T, Utsumi Y, Koga S, Murata I, Fukada K (2016) Differences in drought- and freeze-induced embolisms in deciduous ring-porous plant species in Japan. Planta 244:753–760
Van Ieperen W, Nijsse J, Keijzer CJ, Van Meeteren U (2001) Induction of air embolism in xylem conduits of pre-defined diameter. J Exp Bot 52:981–991
Wisniewski M, Glenn DM, Gusta LV, Fuller M, Duman J, Griffith M (2003) Using infrared thermography to study ice nucleation and propagation in plants. Acta Hort 618:485–492
Yin J, Fridley JD, Smith MS, Bauerle TL (2016) Xylem vessel traits predict leaf phenology of native and non-native understorey species of temperate deciduous forests. Funct Ecol 30:206–214
Zhang L, Marguerit E, Rossdeutsch L, Ollat N, Gambetta GA (2016) The influence of grapevine rootstocks on scion growth and drought resistance. Theor Exp Plant Physiol 28:143–157
Zimmermann MH (1983) Xylem structure and the assent of sap. Springer-Verlag, Berlin
Acknowledgements
This study was funded through The Pennsylvania State University College of Agriculture Student Competitive Grants Program, by the USDA National Institute of Food and Agriculture Federal Appropriations under Project PEN0 4628 and Accession number 101,413, and by the Pennsylvania Wine Marketing and Research Board. The authors thank Selene Burgio and Marine Galanopoulo for assistance in conducting this research, Annika Huber and Jingjing Yin for assistance with hydraulic methods and measurements, and J.C. Moser and Donald Smith for technical support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Smith, M.S., Centinari, M. Young grapevines exhibit interspecific differences in hydraulic response to freeze stress but not in recovery. Planta 250, 495–505 (2019). https://doi.org/10.1007/s00425-019-03183-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-019-03183-6