The variability in the xylem architecture of grapevine petiole and its contribution to hydraulic differences
Uri Hochberg A B , Asfaw Degu A B , Tanya Gendler B , Aaron Fait B and Shimon Rachmilevitch B CA Albert Katz International School, Beer-Sheva, Israel.
B The French Associates Institute for Agriculture and Biotechnology of Drylands (FAAB), the Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990 Sede Boqer, Israel.
C Corresponding author. Email: rshimon@bgu.ac.il
Functional Plant Biology 42(4) 357-365 https://doi.org/10.1071/FP14167
Submitted: 18 June 2014 Accepted: 9 November 2014 Published: 12 December 2014
Abstract
Grapevine cultivars possess large variability in their response to water availability, and are therefore considered as a good model to study plant hydraulic adjustments. The current research compared the petiole anatomy of two grapevine (Vitis vinifera L.) cultivars, Shiraz and Cabernet Sauvignon, in respect to hydraulic properties. Hydraulic differences between the cultivar petioles were tested over 3 years (2011–2013). Anatomical differences, hydraulic conductivity and embolism were tested under terminal drought conditions. Additionally, xylem differentiation under well watered (WW) and water deficit (WD) conditions was compared. Shiraz was shown to possess larger xylem vessels that resulted in a significantly higher theoretical specific hydraulic conductivity (Kts), leaf hydraulic conductivity (Kleaf) and maximal petiole hydraulic conductivity (Kpetiole). Under WD, smaller vessels were developed, more noticeably in Shiraz. Results confirmed a link between petiole hydraulic architecture and hydraulic behaviour, providing a simple mechanistic explanation for the higher transpiration rates commonly measured in Shiraz. Smaller xylem vessels in Cabernet Sauvignon could imply on its adaptation to WD, and explains its better performances under such conditions.
Additional keywords: anatomy, anisohydric, embolism, hydraulic conductance, isohydric, Vitis vinifera.
References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–42.Alsina M, De Herralde F, Aranda X, Save R, Biel C (2007) Water relations and vulnerability to embolism are not related: experiments with eight grapevine cultivars. Vitis 46, 1–6.
Bota J, Flexas J, Medrano H (2001) Genetic variability of photosynthesis and water use in Balearic grapevine cultivars. Annals of Applied Biology 138, 353–361.
| Genetic variability of photosynthesis and water use in Balearic grapevine cultivars.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, McAdam SA (2013) Abscisic acid mediates a divergence in the drought response of two conifers. Plant Physiology 162, 1370–1377.
| Abscisic acid mediates a divergence in the drought response of two conifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCmtLjF&md5=9c5f7844dca169d634e998e32c494317CAS | 23709665PubMed |
Chalmers YM (2007) Influence of sustained deficit irrigation on physiology and phenolic compounds in winegrapes and wine. PhD thesis. University of Adelaide.
Chaves MM, Zarrouk O, Francisco R, Costa JM, Santos T, Regalado AP, Rodrigues ML, Lopes CM (2010) Grapevine under deficit irrigation: hints from physiological and molecular data. Annals of Botany 105, 661–676.
| Grapevine under deficit irrigation: hints from physiological and molecular data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3ovFGnsg%3D%3D&md5=2029b649085860500462a15772fec919CAS | 20299345PubMed |
Choat B, Drayton W, Matthews M, Shackel K, Wada H, Mcelrone A (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. 33, 1502–1512.
Cochard H, Delzon S, Badel E (2014) X‐ray microtomography (micro‐CT): a reference technology for high‐resolution quantification of xylem embolism in trees. Plant, Cell & Environment
| X‐ray microtomography (micro‐CT): a reference technology for high‐resolution quantification of xylem embolism in trees.Crossref | GoogleScholarGoogle Scholar |
Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. American Journal of Botany 86, 1367–1372.
| The relationship between xylem conduit diameter and cavitation caused by freezing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngs1Gnug%3D%3D&md5=0be68732e2d401e00de1f49ec857346bCAS | 10523278PubMed |
Hochberg U, Degu A, Fait A, Rachmilevitch S (2013a) Near isohydric grapevine cultivar displays higher photosynthetic efficiency and photorespiration rates under drought stress as compared with near anisohydric grapevine cultivar. Physiologia Plantarum 147, 443–452.
| Near isohydric grapevine cultivar displays higher photosynthetic efficiency and photorespiration rates under drought stress as compared with near anisohydric grapevine cultivar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsFWgs7Y%3D&md5=f891ffdc20887b61d4103aaf373aa9aeCAS | 22901023PubMed |
Hochberg U, Degu A, Toubiana D, Gendler T, Nikoloski Z, Rachmilevitch S, Fait A (2013b) Metabolite profiling and network analysis reveal coordinated changes in grapevine water stress response. BMC Plant Biology 13, 184
| Metabolite profiling and network analysis reveal coordinated changes in grapevine water stress response.Crossref | GoogleScholarGoogle Scholar | 24256338PubMed |
Lovisolo C, Schubert A (1998) Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. Journal of Experimental Botany 49, 693–700.
Lovisolo C, Tramontini S (2010) ‘Methods for assessment of hydraulic conductance and embolism extent in grapevine organs. Methodologies and results in grapevine research.’ pp. 71–85. (Springer: New York)
Lovisolo C, Hartung W, Schubert A (2002) Whole-plant hydraulic conductance and root-to-shoot flow of abscisic acid are independently affected by water stress in grapevines. Functional Plant Biology 29, 1349–1356.
| Whole-plant hydraulic conductance and root-to-shoot flow of abscisic acid are independently affected by water stress in grapevines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1ygtLs%3D&md5=3f5aaf0088b8488dcd7bd8c73a37661fCAS |
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 Phytologist 180, 642–651.
| An abscisic acid-related reduced transpiration promotes gradual embolism repair when grapevines are rehydrated after drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKms7vM&md5=cfeacf1c306a527047c5f226a800ace5CAS |
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. Functional Plant Biology 37, 98–116.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlyhsrs%3D&md5=c5799bff3e8a9a6e08b22a493261ed27CAS |
Moshelion M, Halperin O, Wallach R, Oren R, Way DA (2014) The role of aquaporins in determining transpiration and photosynthesis in water‐stressed plants: crop water‐use efficiency, growth and yield. Plant, Cell & Environment
| The role of aquaporins in determining transpiration and photosynthesis in water‐stressed plants: crop water‐use efficiency, growth and yield.Crossref | GoogleScholarGoogle Scholar |
Netzer Y, Munitz S, Schwartz A (2013) Effects of RDI treatments on xylem characteristics, stem water potential, yield and wine quality. In ‘IX International symposium on grapevine physiology and biotechnology.’ (La Serena, Chile)
Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiology 149, 2000–2012.
| Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Wnsrg%3D&md5=fc9ff6952ded6a8aab67b0aace5ce24aCAS | 19211703PubMed |
Pou A, Flexas J, Alsina MM, Bota J, Carambula C, De Herralde F, Galmés J, Lovisolo C, Jiménez M, Ribas‐Carbó M (2008) Adjustments of water use efficiency by stomatal regulation during drought and recovery in the drought‐adapted Vitis hybrid Richter‐110 (V. berlandieri × V. rupestris). Physiologia Plantarum 134, 313–323.
| Adjustments of water use efficiency by stomatal regulation during drought and recovery in the drought‐adapted Vitis hybrid Richter‐110 (V. berlandieri × V. rupestris).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ektbbJ&md5=c99068d65f66527e4d6d970787b7bf93CAS | 18507813PubMed |
Pou A, Medrano H, Tomàs M, Martorell S, Ribas-Carbó M, Flexas J (2012) Anisohydric behaviour in grapevines results in better performance under moderate water stress and recovery than isohydric behaviour. Plant and Soil 359, 335–349.
| Anisohydric behaviour in grapevines results in better performance under moderate water stress and recovery than isohydric behaviour.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGmsrrP&md5=563e99e4b08158a92210d62d75a14885CAS |
Prado K, Maurel C (2013) Regulation of leaf hydraulics: from molecular to whole plant levels. Frontiers in Plant Science 4, 255
| Regulation of leaf hydraulics: from molecular to whole plant levels.Crossref | GoogleScholarGoogle Scholar | 23874349PubMed |
Rewald B, Raveh E, Gendler T, Ephrath JE, Rachmilevitch S (2012) Phenotypic plasticity and water flux rates of Citrus root orders under salinity. Journal of Experimental Botany 63, 2717–2727.
| Phenotypic plasticity and water flux rates of Citrus root orders under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvF2qsr4%3D&md5=f0f833c5096a3fce95d52900a8396639CAS | 22268156PubMed |
Schultz H (2003) Differences in hydraulic architecture account for near-isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars during drought. Plant, Cell & Environment 26, 1393–1405.
| Differences in hydraulic architecture account for near-isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars during drought.Crossref | GoogleScholarGoogle Scholar |
Shatil‐Cohen A, Attia Z, Moshelion M (2011) Bundle‐sheath cell regulation of xylem‐mesophyll water transport via aquaporins under drought stress: a target of xylem‐borne ABA? The Plant Journal 67, 72–80.
| Bundle‐sheath cell regulation of xylem‐mesophyll water transport via aquaporins under drought stress: a target of xylem‐borne ABA?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsVyrtrg%3D&md5=58b9303bef4e24235fd3aef3a2146541CAS | 21401747PubMed |
Shelden MC (2008) A comparison of water stress-induced xylem embolism in two grapevine cultivars, Chardonnay and Grenache, and the role of aquaporins. PhD thesis. University of Adelaide.
Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. The Plant Cell 22, 3560–3573.
| ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVersg%3D%3D&md5=296560220e6233ddbb5dac519a533daeCAS | 21097710PubMed |
Soar C, Speirs J, Maffei S, Penrose A, McCarthy M, Loveys B (2006) Grape vine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue. Australian Journal of Grape and Wine Research 12, 2–12.
| Grape vine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFSlsLc%3D&md5=b7ec2f4497b8c80fe15b79ace3bf14f1CAS |
Sperry J, Pockman W (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant, Cell & Environment 16, 279–287.
| Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Holbrook NM, Zimmermann MH, Tyree MT (1987) Spring filling of xylem vessels in wild grapevine. Plant Physiology 83, 414–417.
| Spring filling of xylem vessels in wild grapevine.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhslChsQ%3D%3D&md5=5028b645dd7d697fca0b97164ea808e7CAS | 16665259PubMed |
Tramontini S, van Leeuwen C, Domec J, Destrac-Irvine A, Basteau C, Vitali M, Mosbach-Schulz O, Lovisolo C (2013) Impact of soil texture and water availability on the hydraulic control of plant and grape-berry development. Plant and Soil 368, 215–230.
| Impact of soil texture and water availability on the hydraulic control of plant and grape-berry development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Ghu70%3D&md5=0f51876313dd429217f596b78cf69173CAS |
Tramontini S, Döring J, Vitali M, Ferrandino A, Stoll M, Lovisolo C (2014) Soil water-holding capacity mediates hydraulic and hormonal signals of near-isohydric and near-anisohydric Vitis cultivars in potted grapevines. Functional Plant Biology
| Soil water-holding capacity mediates hydraulic and hormonal signals of near-isohydric and near-anisohydric Vitis cultivars in potted grapevines.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 |
Tuzet A, Perrier A, Leuning R (2003) A coupled model of stomatal conductance, photosynthesis and transpiration. Plant, Cell & Environment 26, 1097–1116.
| A coupled model of stomatal conductance, photosynthesis and transpiration.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Dixon MA (1986) Water stress induced cavitation and embolism in some woody plants. Physiologia Plantarum 66, 397–405.
| Water stress induced cavitation and embolism in some woody plants.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 M (2002) Hydraulic architecture of whole plants and plant performance. In ‘Xylem structure and the ascent of sap’. pp. 175–214. (Springer: Berlin)
Tyree MT, Davis SD, Cochard H (1994) Biophysical perspective of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerabilty to dysfunction? IAWA Journal 15, 335–360.
| Biophysical perspective of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerabilty to dysfunction?Crossref | GoogleScholarGoogle Scholar |
Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiology 149, 445–460.
| The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1WqtL8%3D&md5=f4b1ecd62035998641f1319dc84b91f7CAS | 18987216PubMed |
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter‐vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade‐off in xylem transport. Plant, Cell & Environment 28, 800–812.
| Inter‐vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade‐off in xylem transport.Crossref | GoogleScholarGoogle Scholar |
Wheeler JK, Huggett 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.
Zufferey V, Cochard H, Ameglio T, Spring JL, Viret O (2011) Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas). Journal of Experimental Botany 62, 3885–3894.
| Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFGjs74%3D&md5=a7457b76e2dcf711d1aed06788bc0a1bCAS | 21447755PubMed |