Annual patterns of xylem embolism in high-yield apple cultivars
Barbara Beikircher A B and Stefan Mayr A
+ Author Affiliations
- Author Affiliations
A University of Innsbruck, Institute of Botany, Sternwartestrasse 15, 6020 Innsbruck, Austria.
B Corresponding author. Email: barbara.beikircher@uibk.ac.at
Functional Plant Biology 44(6) 587-596 https://doi.org/10.1071/FP16048
Submitted: 5 February 2016 Accepted: 20 February 2017 Published: 31 March 2017
Journal Compilation © CSIRO Publishing 2017 Open Access CC BY-NC-ND
Abstract
Temperate angiosperm species show pronounced annual patterns in xylem embolism. In this study, we investigated whether high-yield cultivars of Malus domestica Borkh. growing under optimised soil water conditions follow similar patterns to wild-type plants, and evaluated crucial factors for the formation of winter embolism and the subsequent restoration of the hydraulic system in spring. In five different cultivars growing at three different sites, various hydraulic and microclimatic parameters were monitored over three successive years. In all cultivars on all sites and in all years, the percentage loss of hydraulic conductivity (PLC) increased in autumn with freeze–thaw events and accumulated over winter. Maximum values were reached in late winter and differed significantly among cultivars. In spring, the hydraulic system was restored and PLC remained negligible during summer. Embolism formation in autumn was significantly correlated with the occurrence of freeze–thaw events, whereas further conductivity losses over winter were related to winter desiccation and influenced by climatic and cultivar-specific parameters. Restoration of the hydraulic system in spring was strongly linked to a decrease in the starch content of wood and buds, and soil temperature. Despite high soil water availability, hydraulic recovery took several weeks and was not completed before bud break. Spring is thus a critical phase for temperate angiosperms, especially for high-yield cultivars with risky hydraulic strategies.
Additional keywords: conductance, Malus domestica, refilling, starch, xylem pressure.
References
Allen RG, Pereira LS, Raes D, Smith M (1998) ‘Crop evapotranspiration – guidelines for computing crop water requirements.’ (Food and Agricultural Organisation of the United Nations: Rome)Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Functional Ecology 21, 211–218.
| Low temperature limits of root growth in deciduous and evergreen temperate tree species.Crossref | GoogleScholarGoogle Scholar |
Ameglio T, Bodet C, Lacointe A, Cochard H (2002) Winter embolism, mechanism of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. Tree Physiology 22, 1211–1220.
| Winter embolism, mechanism of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees.Crossref | GoogleScholarGoogle Scholar |
Beikircher B, Mayr S (2008) The hydraulic architecture of Juniperus communis L. ssp. communis: shrubs and trees compared. Plant, Cell & Environment 31, 1545–1556.
| The hydraulic architecture of Juniperus communis L. ssp. communis: shrubs and trees compared.Crossref | GoogleScholarGoogle Scholar |
Beikircher B, Mayr S (2013) Winter peridermal conductance of apple trees: lammas shoots and spring shoots compared. Trees 27, 707–715.
| Winter peridermal conductance of apple trees: lammas shoots and spring shoots compared.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2srntV2jug%3D%3D&md5=70bc8dd7f26e700d1363862f3a8af145CAS |
Beikircher B, Mayr S (2015) Avoidance of harvesting and sampling artefacts in hydraulic analyses: a protocol tested on Malus domestica. Tree Physiology 36, 797–803.
| Avoidance of harvesting and sampling artefacts in hydraulic analyses: a protocol tested on Malus domestica.Crossref | GoogleScholarGoogle Scholar |
Beikircher B, De Cesare C, Mayr S (2013) Hydraulics of high-yield orchard trees: a case study of three Malus domestica cultivars. Tree Physiology 33, 1296–1307.
| Hydraulics of high-yield orchard trees: a case study of three Malus domestica cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2msQ%3D%3D&md5=867b026fdfb9b9700360235f682593beCAS |
Beikircher B, Mittmann C, Mayr S (2016) Prolonged soil frost affects hydraulics and phenology of apple trees. Frontiers in Plant Science 7, 867
| Prolonged soil frost affects hydraulics and phenology of apple trees.Crossref | GoogleScholarGoogle Scholar |
Brodersen CR, McElrone AJ (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Frontiers in Plant Science 4, 108
| Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants.Crossref | GoogleScholarGoogle Scholar |
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 Physiology 154, 1088–1095.
| The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2nsbfL&md5=6a19490f4780f2dcd63235d0df7e6771CAS |
Charrier G, Charra-Vaskou K, Kasuga J, Cochard H, Mayr S, Ameglio T (2014) Freeze–thaw stress: effects of temperature on hydraulic conductivity and ultrasonic activity in ten woody angiosperms. Plant Physiology 164, 992–998.
| Freeze–thaw stress: effects of temperature on hydraulic conductivity and ultrasonic activity in ten woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks1Smu7k%3D&md5=249f27c454a61e82fe4ec837a2e1e467CAS |
Choat B, Medek DE, Stuart SA, Pasquet-Kok J, Egerton JJG, Salari H, Sack L, Ball MC (2011) Xylem traits mediate a trade-off between resistance to freeze–thaw-induced embolism and photosynthetic capacity in overwintering evergreens. New Phytologist 191, 996–1005.
| Xylem traits mediate a trade-off between resistance to freeze–thaw-induced embolism and photosynthetic capacity in overwintering evergreens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1WmsbbM&md5=865289d2a39894b6656f8b43a25a69d0CAS |
Christensen-Dalsgaard KK, Tyree MT (2014) Frost fatigue and spring recovery of xylem vessels in three diffuse-porous trees in situ. Plant, Cell & Environment 37, 1074–1085.
| Frost fatigue and spring recovery of xylem vessels in three diffuse-porous trees in situ.Crossref | GoogleScholarGoogle Scholar |
Cobb AR, Choat B, Holbrook NM (2007) Dynamics of freeze–thaw embolism in Smilax rotundifolia (Smilacaceae). American Journal of Botany 94, 640–649.
| Dynamics of freeze–thaw embolism in Smilax rotundifolia (Smilacaceae).Crossref | GoogleScholarGoogle Scholar |
Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiology 6, 393–407.
| Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FosVWqtA%3D%3D&md5=78b8f2ca94ce6429fb85c559292ac3bbCAS |
Cochard H, Lemoine D, Ameglio T, Granier A (2001) Mechanism of xylem recovery from winter embolism in Fagus sylvatica. Tree Physiology 21, 27–33.
| Mechanism of xylem recovery from winter embolism in Fagus sylvatica.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvksleisA%3D%3D&md5=f42623ba2bdfbf2a9e867145d59066e6CAS |
Essiamah S, Eschrich W (1985) Changes of starch content in the storage tissues of deciduous trees during winter and spring. IAWA Journal 6, 97–106.
| Changes of starch content in the storage tissues of deciduous trees during winter and spring.Crossref | GoogleScholarGoogle Scholar |
Ewers FW, Ameglio T, Cochard H, Beaujard F, Martignac M, Vandame M, Bodet C, Cruiziat P (2001) Seasonal variation in xylem pressure of walnut trees: root and stem pressures. Tree Physiology 21, 1123–1132.
| Seasonal variation in xylem pressure of walnut trees: root and stem pressures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrjsV2rtw%3D%3D&md5=6c8f47fc8dcec278b26fed8b2ca692cfCAS |
Hacke U, Sauter JJ (1996) Xylem dysfunction during winter and recovery of hydraulic conductivity in diffuse-porous and ring-porous trees. Oecologia 105, 435–439.
| Xylem dysfunction during winter and recovery of hydraulic conductivity in diffuse-porous and ring-porous trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cznsFKntg%3D%3D&md5=6919721215c322f8a41a5c96950fa3ceCAS |
Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA (2001) Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiology 125, 779–786.
| Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhs1Klsb8%3D&md5=4811ef4784566b72e9ea49f3991a8d5eCAS |
Hao GY, Wheeler JK, Holbrook NM, Goldstein G (2013) Investigating xylem embolism formation, refilling and water storage in tree trunks using frequency domain reflectometry. Journal of Experimental Botany 64, 2321–2332.
| Investigating xylem embolism formation, refilling and water storage in tree trunks using frequency domain reflectometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvV2ntbs%3D&md5=9938324a7a3bd647f87667263259b93dCAS |
Holbrook NM, Zwieniecki MA (1999) Embolism repair and xylem tension: do we need a miracle? Plant Physiology 120, 7–10.
| Embolism repair and xylem tension: do we need a miracle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1Sru74%3D&md5=a35976b460e52436200482473bce753aCAS |
Kozlowski TT, Kramer PJ, Pallardy SG (1991) ‘The physiological ecology of woody plants.’ (Academic Press: San Diego)
Larcher W (2003) ‘Physiological plant ecology.’ (Springer-Verlag: Berlin)
Mayr S, Charra-Vaskou K (2007) Winter at the alpine timberline causes complex within-tree patterns of water potential and embolism in Picea abies. Physiologia Plantarum 131, 131–139.
| Winter at the alpine timberline causes complex within-tree patterns of water potential and embolism in Picea abies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSqtLjE&md5=9c49b68b0b54c3150e137c9ef20102b1CAS |
Mayr S, Schwienbacher F, Bauer H (2003) Winter at the alpine timberline. Why does embolism occur in Norway spruce but not in stone pine? Plant Physiology 131, 780–792.
| Winter at the alpine timberline. Why does embolism occur in Norway spruce but not in stone pine?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjsLo%3D&md5=afad1dacf301686755c47e73be054891CAS |
Mayr S, Cochard H, Ameglio T, Kikuta SB (2007) Embolism formation during freezing in the wood of Picea abies. Plant Physiology 143, 60–67.
| Embolism formation during freezing in the wood of Picea abies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Ogsw%3D%3D&md5=37741d5e4a1a6ef826708a4b122600a0CAS |
Mayr S, Schmid P, Laur J, Rosner S, Charra-Vaskou K, Dämon B, Hacke UG (2014) Uptake of water via branches helps timberline conifers refill embolized xylem in late winter. Plant Physiology 164, 1731–1740.
| Uptake of water via branches helps timberline conifers refill embolized xylem in late winter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsV2js74%3D&md5=5e0596dd0356feb254c792fd0e4297e8CAS |
Naor A, Girona J (2012) Apple. In ‘Crop yield response to water’. (Eds P Steduto, TC Hsiao, E Fereres, D Raes.) pp. 332–345. (Food and Agricultural Organization of the United Nations: Rome)
Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Science 180, 604–611.
| Refilling embolized xylem conduits: is it a matter of phloem unloading?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFyhs7g%3D&md5=28db9c438e9bc36c9ac545c538bb72dbCAS |
Pallardy SG (2008) ‘Physiology of woody plants.’ (Elsevier: London)
Pittermann J, Sperry JS (2006) Analysis of freeze–thaw embolism in conifers. The interaction between cavitation pressure and tracheid size. Plant Physiology 140, 374–382.
| Analysis of freeze–thaw embolism in conifers. The interaction between cavitation pressure and tracheid size.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCgt7w%3D&md5=b3db21fc59df22b820d50595876a283aCAS |
Salleo S, Lo Gullo MA, Trifiló P, Nardini A (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell & Environment 27, 1065–1076.
| New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L.Crossref | GoogleScholarGoogle Scholar |
Salleo S, Trifilo P, Lo Gullo MA (2006) Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel). Functional Plant Biology 33, 1063–1074.
| Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel).Crossref | GoogleScholarGoogle Scholar |
Secchi F, Zwieniecki MA (2012) Analysis of xylem sap from functional (nonembolized) and nonfunctional (embolized) vessels of Populus nigra: chemistry of refilling. Plant Physiology 160, 955–964.
| Analysis of xylem sap from functional (nonembolized) and nonfunctional (embolized) vessels of Populus nigra: chemistry of refilling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFaksbbF&md5=98b6f7fa76d3703f541633d9dc995077CAS |
Sevanto S, Holbrook NM, Ball MC (2012) Freeze/thaw-induced embolism: probability of critical bubble formation depends on speed of ice formation. Frontiers in Plant Science 3, 107
| Freeze/thaw-induced embolism: probability of critical bubble formation depends on speed of ice formation.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Sullivan JEM (1992) Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous and conifer species. Plant Physiology 100, 605–613.
| Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous and conifer species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cngvVWrsA%3D%3D&md5=b40e91eb292dbac7f923abeddc36d123CAS |
Sperry JS, Tyree MT (1990) Water-stress-induced xylem embolism in three species of conifers. Plant, Cell & Environment 13, 427–436.
| Water-stress-induced xylem embolism in three species of conifers.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Holbrook NM, Zimmermann MH, Tyree MT (1987) Spring refilling of xylem vessels in wild grapevine. Plant Physiology 83, 414–417.
| Spring refilling of xylem vessels in wild grapevine.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhslChsQ%3D%3D&md5=2030a5b32dc299f14d9aca3d2e8d0626CAS |
Sperry JS, Donnelly JR, Tyree MT (1988a) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11, 35–40.
| A method for measuring hydraulic conductivity and embolism in xylem.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Donnelly JR, Tyree MT (1988b) Seasonal occurence of xylem embolism in sugar maple (Acer saccharum). American Journal of Botany 75, 1212–1218.
| Seasonal occurence of xylem embolism in sugar maple (Acer saccharum).Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75, 1736–1752.
| Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska.Crossref | GoogleScholarGoogle Scholar |
Trifilò P, Raimondo F, Lo Gullo MA, Barbera PM, Salleo S, Nardini A (2014) Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values. Plant, Cell & Environment 37, 2491–2499.
| Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Cochard H (1996) Summer and winter embolism in oak: impact on water relations. Annales des Sciences Forestieres 53, 173–180.
| Summer and winter embolism in oak: impact on water relations.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytologist 119, 345–360.
| The hydraulic architecture of trees and other woody plants.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Zimmermann MH (2002) ‘Xylem structure and the ascent of sap.’ (Springer-Verlag: Berlin)
Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15, 335–360.
| Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction?Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R (1999) Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiology 120, 11–22.
| Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1Sru78%3D&md5=92d7a4efac17ff80b8db0ac013857789CAS |
Utsumi Y, Sano Y, Fujikawa S, Funada R, Ohtani J (1998) Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy. Plant Physiology 117, 1463–1471.
| Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFaqu7s%3D&md5=744534a981248f93c8d89e3b1da41f16CAS |
Wheeler JK, Hugett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell & Environment 36, 1938–1949.
Wiegand KM (1906) Pressure and flow of sap in the maple. American Naturalist 40, 409–453.
| Pressure and flow of sap in the maple.Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA, Holbrook NM (2009) Confronting Maxwell’s demon: biophysics of xylem embolism repair. Trends in Plant Science 14, 530–534.
| Confronting Maxwell’s demon: biophysics of xylem embolism repair.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Wqs7%2FF&md5=9cfa377c35e131ed0efddef7d74e6062CAS |
