Over-accumulation of abscisic acid in transgenic tomato plants increases the risk of hydraulic failure.
crop
drought
transgenic line
water deficit
xylem embolism
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
10
09
2019
revised:
11
11
2019
accepted:
03
12
2019
pubmed:
19
12
2019
medline:
31
12
2020
entrez:
19
12
2019
Statut:
ppublish
Résumé
Climate change threatens food security, and plant science researchers have investigated methods of sustaining crop yield under drought. One approach has been to overproduce abscisic acid (ABA) to enhance water use efficiency. However, the concomitant effects of ABA overproduction on plant vascular system functioning are critical as it influences vulnerability to xylem hydraulic failure. We investigated these effects by comparing physiological and hydraulic responses to water deficit between a tomato (Solanum lycopersicum) wild type control (WT) and a transgenic line overproducing ABA (sp12). Under well-watered conditions, the sp12 line displayed similar growth rate and greater water use efficiency by operating at lower maximum stomatal conductance. X-ray microtomography revealed that sp12 was significantly more vulnerable to xylem embolism, resulting in a reduced hydraulic safety margin. We also observed a significant ontogenic effect on vulnerability to xylem embolism for both WT and sp12. This study demonstrates that the greater water use efficiency in the tomato ABA overproducing line is associated with higher vulnerability of the vascular system to embolism and a higher risk of hydraulic failure. Integrating hydraulic traits into breeding programmes represents a critical step for effectively managing a crop's ability to maintain hydraulic conductivity and productivity under water deficit.
Substances chimiques
Gases
0
Water
059QF0KO0R
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
548-562Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L01954X/1
Pays : United Kingdom
Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Ahmad, H. B., Lens, F., Capdeville, G., Burlett, R., Lamarque, L. J., & Delzon, S. (2017). Intraspecific variation in embolism resistance and stem anatomy across four sunflowers. Physiologia Plantarum, 163, 59-72.
Ahmed, S., & Stepp, J. R. (2016). Beyond yields: Climate change effects on specialty crop quality and agroecological management. Elementa-Science of the Anthropocene, 4, 000092.
Aroca, R., Ferrante, A., Vernieri, P., & Chrispeels, M. J. (2006). Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Annals of Botany, 98, 1301-1310.
Bauer, H., Ache, P., Lautner, S., Fromm, J., Hartung, W., Al-Rasheid, K. A., et al. (2013). The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Current Biology, 23, 53-57.
Bauerle, W. L., Whitlow, T. H., Setter, T. L., & Vermeylen, F. M. (2004). Abscisic acid synthesis in Acer rubrum L. leaves: A vapor-pressure-deficit-mediated response. Journal of the American Society for Horticultural Science, 129, 182-187.
Blum, A. (2014). Genomics for drought resistance-Getting down to earth. Functional Plant Biology, 41, 1191-1198.
Blum, A. (2015). Towards a conceptual ABA ideotype in plant breeding for water limited environments. Functional Plant Biology, 42, 502-513.
Blum, A. (2017). Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant, Cell & Environment, 40, 4-10.
Blum, A., & Tuberosa, R. (2018). Dehydration survival of crop plants and its measurement. Journal of Experimental Botany, 69, 975-981.
Boursiac, Y., Chen, S., Luu, D. T., Sorieul, M., van den Dries, N., & Maurel, C. (2005). Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiology, 139, 790-805.
Brodribb, T. J., & Field, T. S. (2000). Stem hydraulic supply is linked to leaf photosynthetic capacity: Evidence from New Caledonian and Tasmanian rainforests. Plant, Cell & Environment, 23, 1381-1388.
Brodribb, T. J., Skelton, R. P., McAdam, S. A., Bienaime, D., Lucani, C. J., & Marmottant, P. (2016). Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist, 209, 1403-1409.
Cao, K. F., Yang, S. J., Zhang, Y. J., & Brodribb, T. J. (2012). The maximum height of grasses is determined by roots. Ecology Letters, 15, 666-672.
Cardoso, A. A., Brodribb, T. J., Lucani, C. J., DaMatta, F. M., & McAdam, S. A. M. (2018). Coordinated plasticity maintains hydraulic safety in sunflower leaves. Plant, Cell & Environment, 41, 2567-2576.
Cavender-Bares, J., & Bazzaz, F. A. (2000). Changes in drought response strategies with ontogeny in Quercus rubra: Implications for scaling from seedlings to mature trees. Oecologia, 1, 8-18.
Charrier, G., Burlett, R., Gambetta, G., Delzon, S., Domec, J.-C., & Beaujard, F. (2017). Monitoring xylem hydraulic pressure in woody plants. Bio-protocol, 7, e2580.
Charrier, G., Delzon, S., Domec, J-C., Zhang, L., Delmas, C. E. L., Merlin, I., Corso, D., King, A., Ojeda, H., Ollat, N., Prieto, J. A., Scholach, T., Skinner, P., van Leeuwen, C., & Gambetta, G. A. (2018). Drought will not leave your glass empty: Low risk of hydraulic failure revealed by long-term drought observations in world's top wine regions. Science Advances, 4, 1-9, eaao6969.
Charrier, G., Torres-Ruiz, J. M., Badel, E., Burlett, R., Choat, B., Cochard, H., … Delzon, S. (2016). Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiology, 172, 1657-1668.
Choat, B., Nolf, M., Lopez, R., Peters, J. M. R., Carins-Murphy, M. R., Creek, D., & Brodribb, T. J. (2019). Non-invasive imaging shows no evidence of embolism repair after drought in tree species of two genera. Tree Physiology, 39, 113-121.
Cochard, H. (2002a). Xylem embolism and drought-induced stomatal closure in maize. Planta, 215, 466-471.
Cochard, H. (2002b). A technique for measuring xylem hydraulic conductance under high negative pressures. Plant, Cell & Environment, 25, 815-819.
Cochard, H., Damour, G., Bodet, C., Tharwat, I., Poirier, M., & Améglio, T. (2005). Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiologia Plantarum, 124, 410-418.
Cochard, H., Delzon, S., & Badel, E. (2015). X-ray microtomography (micro-CT): A reference technology for high-resolution quantification of xylem embolism in trees. Plant, Cell & Environment, 38, 201-206.
Condon, A. G., Richards, R. A., Rebetzke, G. J., & Farquhar, G. D. (2002). Improving intrinsic water-use efficiency and crop yield. Crop Science, 42, 122-131.
Corcuera, L., Cochard, H., Gil-Pelegrin, E., & Notivol, E. (2011). Phenotypic plasticity in mesic populations of Pinus pinaster improves resistance to xylem embolism (P50) under severe drought. Trees, 25, 1033-1042.
Corso, D., Delzon, S., Lamarque, L. J., Cochard, H., Torres-Ruiz, J. M., King, A., & Brodribb, T. J. (in press). Neither xylem collapse, cavitation or leaf conductance drive stomatal closure in wheat. Plant, Cell & Environment.
Coupel-Ledru, A., Tyerman, S. D., Masclef, D., Lebon, E., Christophe, A., Edwards, E. J., & Simonneau, T. (2017). Abscisic acid down-regulates hydraulic conductance of grapevine leaves in isohydric genotypes only. Plant Physiology, 175, 1121-1134.
De Swaef, T., Hanssens, J., Cornelis, A., & Steppe, K. (2013). Non-destructive estimation of root pressure using sap flow, stem diameter measurements and mechanistic modelling. Annals of Botany, 111, 271-282.
Ewers, F. W., Cochard, H., & Tyree, M. T. (1997). A survey of root pressures in vines of a tropical lowland forest. Oecologia, 110, 191-196.
Gambetta, G. A., Knipfer, T., Fricke, W., & McElrone, A. J. (2017). Aquaporins and root water uptake. In F. Chaumont & S. Tyerman (Eds.), Plant aquaporins. Signaling and communication in plants (pp. 133-153). Cham: Springer.
Gambetta, G. A., Manuck, C. M., Drucker, S. T., Shaghasi, T., Fort, K., Matthews, M. A., … McElrone, A. J. (2012). The relationship between root hydraulics and scion vigour across Vitis rootstocks: What role do aquaporins play? Journal of Experimental Botany, 63, 6445-6455.
Gärtner, H., Lucchinetti, S., & Schweingruber, F. H. (2014). New perspectives for wood anatomical analysis in dendrosciences: The GSL1-microtome. Dendrochronologia, 32, 47-51.
Gleason, S. M., Westoby, M., Jansen, S., Choat, B., Hacke, U. G., Pratt, R. B., et al. (2016). Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. New Phytologist, 209, 123-136.
Gleason, S. M., Wiggans, D. R., Bliss, C. A., Young, J. S., Cooper, M., Willi, K. R., & Comas, L. H. (2017). Embolized stems recover overnight in Zea mays: The role of soil water, root pressure, and nighttime transpiration. Frontiers in Plant Science, 8, 662.
Helander, J. D. M., Vaidya, A. S., & Cutler, S. R. (2016). Chemical manipulation of plant water use. Bioorganic & Medicinal Chemistry, 24, 493-500.
Henson, I. E., Jensen, C. R., & Turner, N. C. (1989). Leaf gas exchange and water relations of lupins and wheat. III. Abscisic acid and drought-induced stomatal closure. Australian Journal of Plant Physiology, 16, 429-442.
Hochberg, U., Windt, C. W., Ponomarenko, A., Zhang, Y. J., Gersony, J., Rockwell, F. E., & Holbrook, N. M. (2017). Stomatal closure, basal leaf embolism, and shedding protect the hydraulic integrity of grape stem. Plant Physiology, 174, 764-775.
Hu, H., & Xiong, L. (2014). Genetic engineering and breeding of drought-resistant crops. Annual Review of Plant Biology, 65, 715-741.
Johnson, K. M., Jordan, G. J., & Brodribb, T. J. (2018). Wheat leaves embolized by water stress do not recover function upon rewatering. Plant, Cell & Environment, 41, 2704-2714.
Kell, D. B. (2011). Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Annals of Botany, 108, 407-411.
King, A., Guignot, N., Zerbino, P., Boulard, E., Desjardins, K., Bordessoule, M., … Itié, J.-P. (2016). Tomography and imaging at the PSICHE beam line of the SOLEIL Synchrotron. Review of Scientific Instruments, 87, 093704.
Knipfer, T., Cuneo, I. F., Earles, J. M., Reyes, C., Brodersen, C. R., & McElrone, A. J. (2017). Storage compartments for capillary water rarely refill in an intact woody plant. Plant Physiology, 175, 1649-1660.
Knipfer, T., Eustis, A. J., Brodersen, C. R., Walker, M. A., & McElrone, A. J. (2015). Grapevine species from varied native habitats exhibit differences in embolism formation/repair associated with leaf gas exchange and root pressure. Plant, Cell & Environment, 38, 1503-1513.
Knipfer, T., & Fricke, W. (2010). Root pressure and a solute reflection coefficient close to unity exclude a purely apoplastic pathway of radial water transport in barley (Hordeum vulgare). New Phytologist, 187, 159-170.
Knox, J., Hess, T., Daccache, A., & Wheeler, T. (2012). Climate change impacts on crop productivity in Africa and South Asia. Environmental Research Letters, 7, 034032.
Kotowska, M. M., Hertel, D., Rajab, Y. A., Barus, H., & Schuldt, B. (2015). Patterns in hydraulic architecture from roots to branches in six tropical tree species from cacao agroforestry and their relation to wood density and stem growth. Frontiers in Plant Science, 6, 191.
Lamarque, L. J., Corso, D., Torres-Ruiz, J. M., Badel, E., Brodribb, T. J., Burlett, R., … Delzon, S. (2018). An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L. Annals of Forest Science, 75, 88.
Lens, F., Picon-Cochard, C., Delmas, C. E., Signarbieux, C., Buttler, A., Cochard, H., … Delzon, S. (2016). Herbaceous angiosperms are not more vulnerable to drought-induced embolism than angiosperm trees. Plant Physiology, 172, 661-667.
Lesk, C., Rowhani, P., & Ramankutty, N. (2016). Influence of extreme weather disasters on global crop production. Nature, 529, 84-87.
Li, S., Klepsch, M., Jansen, S., Schmitt, M., Lens, F., Karimi, Z., … Schenk, H. J. (2016). Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA Journal, 37, 152-171.
Li, Y., Sperry, J. S., & Shao, M. (2009). Hydraulic conductance and vulnerability to cavitation in corn (Zea mays L.) hybrids of differing drought resistance. Environmental and Experimental Botany, 66, 341-346.
Li-Marchetti, C., Le Bras, C., Relion, D., Citerne, S., Huché-Thélier, L., Sakr, S., … Crespel, L. (2015). Genotypic differences in architectural and physiological responses to water restriction in rose bush. Frontiers in Plant Science, 6, 355.
Lobell, D. B., & Field, C. B. (2007). Global scale climate-crop yield relationships and the impacts of recent warming. Environmental Research Letters, 2, 014002.
Lopes, M. S., Araus, J. L., van Heerden, P. D. R., & Foyer, C. H. (2011). Enhancing drought tolerance in C4 crops. Journal of Experimental Botany, 62, 3135-3153.
Lucani, C. J., Brodribb, T. J., Jordan, G. J., & Mitchell, P. J. (2019). Junevile and adult leaves of heteroblastic Eucalyptus globulus vary in xylem vulnerability. Trees, 33, 1167-1178.
Mahdieh, M., & Mostajeran, A. (2009). Abscisic acid regulates root hydraulic conductance via aquaporin expression modulation in Nicotiana tabacum. Journal of Plant Physiology, 166, 1993-2003.
Martínez-Vilalta, J., Cochard, H., Mencuccini, M., Sterck, F., Herrero, A., Korhonen, J. F. J., … Ripullone, F. (2009). Hydraulic adjustment of Scots pine across Europe. New Phytologist, 184, 353-364.
Martin-StPaul, N., Delzon, S., & Cochard, H. (2017). Plant resistance to drought depends on timely stomatal closure. Ecology Letters, 20, 1437-1447.
Matiu, M., Ankerst, D. P., & Menzel, A. (2017). Interactions between temperature and drought in global and regional crop yield variability during 1961-2014. PLoS One, 12, e0178339.
McAdam, S. A. M., & Brodribb, T. J. (2015). The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiology, 167, 833-843.
Mega, R., Abe, F., Kim, J. S., Tsuboi, Y., Tanaka, K., Kobayashi, H., … Okamoto, M. (2019). Tuning water-use efficiency and drought tolerance in wheat using abscisic acid receptors. Nature Plants, 5, 153-159.
Meinzer, F. C., Grantz, D. A., & Smit, B. (1991). Root signals mediate coordination of stomatal and root hydraulic conductance in growing sugarcane. Australian Journal of Plant Physiology, 18, 329-338.
Mirone, A., Brun, E., Gouillart, E., Tafforeau, P., & Kieffer, J. (2014). The PyHST2 hybrid distributed code for high speed tomographic reconstruction with interaction reconstruction and a priori knowledge capabilities. Nuclear Instruments and Methods in Physics Research, 324, 41-48.
Mittelheuser, C. J., & van Steveninck, R. F. M. (1969). Stomatal closure and inhibition of transpiration induced by (RS)-abscisic acid. Nature, 221, 281-282.
Neufeld, H. S., Grantz, D. A., Meinzer, F. C., Goldstein, G., Crisosto, G. M., & Crisosto, C. (1992). Genotypic variability in vulnerability of leaf xylem to cavitation in water-stressed and well-irrigated sugarcane. Plant Physiology, 100, 1020-1028.
Nobel, P. S. (1991). Physicochemical and environmental plant physiology. UK: Academic Press.
Nuccio, M. L., Paul, M., Bate, N. J., Cohn, J., & Cutler, S. R. (2018). Where are the drought tolerant crops? An assessment of more than two decades of plant biotechnology effort in crop improvement. Plant Science, 273, 110-119.
Paganin, D., Mayon, S. C., Gureyev, T. E., Miller, P. R., & Wilkins, S. W. (2002). Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. Journal of Microscopy, 206, 33-40.
Pammenter, N. W., & Van der Willigen, C. (1998). A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiology, 18, 589-593.
Pantin, F., Monnet, F., Jannaud, D., Costa, J. M., Renaud, J., Muller, B., … Genty, B. (2013). The dual effect of abscisic acid on stomata. New Phytologist, 193, 65-72.
Papacek, M., Christmann, A., & Grill, E. (2019). Increased water use efficiency and water productivity of arabidopsis by abscisic acid receptors from Populus canescens. Annals of Botany, 225, 1-9.
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.
Passioura, J. (2006). Increasing crop productivity when water is scarce-From breeding to field management. Agricultural Water Management, 80, 176-196.
Passioura, J., & Angus, J. F. (2010). Increasing productivity of crops in water-limited environments. Advances in Agronomy, 106, 37-75.
Porter, J. R., Xie, L., Challinor, A. J., Cochrane, K., Howden, S. M., Iqbal, M. M., … Travasso, M. I. (2014). Food security and food production systems. In C. B. Field, V. R. Barros, D. J. Dokken, K. J. Mach, M. D. Mastrandrea, T. E. Bilir, et al. (Eds.), Climate change 2014: Impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. Contribution of working group II to the fifth assessment report of the intergouvernmental panel on climate change (pp. 485-533). Cambridge: Cambridge University Press.
Postaire, O., Tournaire-Roux, C., Grondin, A., Boursiac, Y., Morillon, R., Schaffner, A. R., & Maurel, C. (2010). A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiology, 152, 1418-1430.
Pouzoulet, J., Scudiero, E., Schiavon, M., & Rolshausen, P. E. (2017). Xylem vessel diameter affects the compartmentalization of the vascular pathogen Phaeomoniella chlamydospora in grapevine. Frontiers in Plant Science, 8, 1442.
Ray, D. K., Gerber, J. S., MacDonald, G. K., & West, P. C. (2015). Climate variation explains a third of global crop yield variability. Nature Communications, 6, 5989.
Ruzin, S. E. (1999). Plant microtechnique and microscopy (Vol. 198). UK: Oxford University Press.
Ryu, J., Hwang, B. G., Kim, Y. X., & Lee, S. J. (2016). Direct observation of local xylem embolisms induced by soil drying in intact Zea mays leaves. Journal of Experimental Botany, 67, 2617-2626.
Saradadevi, R., Bramley, H., Siddique, K. H. M., Edwards, E., & Palta, J. A. (2014). Contrasting stomatal regulation and leaf ABA concentrations in wheat genotypes when split root systems were exposed to terminal drought. Field Crops Research, 162, 77-86.
Saradadevi, R., Palta, J. A., & Siddique, K. H. M. (2017). ABA-Mediated stomatal response in regulating water use during the development of terminal drought in wheat. Frontiers in Plant Science, 8, 1251.
Schauberger, B., Archontoulis, S., Arneth, A., Balkovic, J., Ciais, P., Deryng, D., … Frieler, K. (2017). Consistent negative response of US crops to high temperatures in observations and crop models. Nature Communications, 8, 13931.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
Schuldt, B., Knutzen, F., Delzon, S., Jansen, S., Müller-Haubold, H., Burlett, R., … Leuschner, C. (2016). How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytologist, 210, 443-458.
Sharipova, G., Veselov, D., Kudoyarova, G., Fricke, W., Dodd, I. C., Katsuhara, M., … Veselov, S. (2016). Exogenous application of abscisic acid (ABA) increases root and cell hydraulic conductivity and abundance of some aquaporin isoforms in the ABA-deficient barley mutant Az34. Annals of Botany, 118, 777-785.
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-born ABA? The Plant Journal, 67, 72-80.
Skelton, R. P., Brodribb, T. J., & Choat, B. (2017). Casting light on xylem vulnerability in an herbaceous species reveal a lack of segmentation. New Phytologist, 214, 561-569.
Smeeton, R. C. (2010). An evaluation of the effects of over-production of ABA on whole plant water use, growth and productivity. PhD thesis, 250 pp. University of Warwick and University of Nottingham.
Sperry, J. (2013). Cutting-edge research or cutting-edge artefact? An overdue control experiment complicates the xylem refilling story. Plant, Cell & Environment, 36, 1916-1918.
Sperry, J. S., Donnelly, J. R., & Tyree, M. T. (1988). A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment, 11, 35-40.
Steudle, E. (2001). The cohesion-tension mechanism and the acquisition of water by plant roots. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 487-875.
Stiller, V., Lafitte, H. R., & Sperry, J. S. (2003). Hydraulic properties of rice and the response of gas exchange to water stress. Plant Physiology, 132, 1698-1706.
Stiller, V., & Sperry, J. S. (2002). Cavitation fatigue and its reversal in sunflower (Helianthus annuus L.). Journal of Experimental Botany, 53, 1155-1161.
Stiller, V., Sperry, J. S., & Lafitte, R. (2005). Embolized conduits of rice (Oryza sativa, Poaceae) refill despite negative xylem pressure. American Journal of Botany, 92, 1970-1974.
Tardieu, F., Lafarge, T., & Simonneau, T. (1996). Stomatal control by fed or endogenous xylem ABA in sunflower: Interpretation of correlations between leaf water potential and stomatal conductance in anisohydric species. Plant, Cell & Environment, 19, 75-84.
Tardieu, F., & Parent, B. (2017). Predictable ‘meta-mechanisms' emerge from feedbacks between transpiration and plant growth and cannot be simply deduced from short-term mechanisms. Plant, Cell & Environment, 40, 846-857.
Tardieu, F., Parent, B., Caldeira, C. F., & Welcker, C. (2014). Genetic and physiological controls of growth under water deficit. Plant Physiology, 164, 1628-1635.
Tardieu, F., Zhang, J., Katerji, N., Bethenod, O., Palmer, S., & Davies, W. J. (1992). Xylem ABA controls the stomatal conductance of field-grown maize subjected to soil compaction or soil drying. Plant, Cell & Environment, 15, 193-197.
Thompson, A. J., Andrews, J., Mulholland, B. J., McKee, J. M. T., Hilton, H. W., Horridge, J. S., … Taylor, I. B. (2007). Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiology, 143, 1905-1917.
Thompson, A. J., Jackson, A. C., Symonds, R. C., Mulholland, B. J., Dadswell, A. R., Blake, P. S., … Taylor, I. B. (2000). Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. The Plant Journal, 23, 363-374.
Thompson, A. J., Mulholland, B. J., Jackson, A. C., McKee, J. M. T., Hilton, H. W., Symonds, R. C., … Taylor, I. B. (2007). Regulation and manipulation of ABA biosynthesis in roots. Plant, Cell & Environment, 30, 67-78.
Tonetto de Freitas, S., Shackel, K. A., & Mitcham, E. J. (2011). Abscisic acid triggers whole-plant and fruit-specific mechanisms to increase fruit calcium uptake and prevent blossom end rot development in tomato fruit. Journal of Experimental Botany, 62, 2645-2656.
Torres-Ruiz, J. M., Cochard, H., Choat, B., Jansen, S., Lopez, R., Tomaskova, I., … Delzon, S. (2017). Xylem resistance to embolism: Presenting a simple diagnostic test for the open vessel artefact. New Phytologist, 215, 489-499.
Torres-Ruiz, J. M., Jansen, S., Choat, B., McElrone, A. J., Cochard, H., Brodribb, T. J., … Delzon, S. (2015). Direct x-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiology, 167, 40-43.
Torres-Ruiz, J. M., Sperry, J. S., & Fernandez, J. E. (2012). Improving xylem hydraulic conductivity measurements by correcting the error caused by passive water uptake. Physiologia Plantarum, 146, 129-135.
Tyree, M. T., & Ewers, F. W. (1991). The hydraulic architecture of trees and other woody plants. New Phytologist, 119, 345-360.
Tyree, M. T., Fiscus, E. L., Wullschleger, S. D., & Dixon, M. A. (1986). Detection of xylem cavitation in corn under field conditions. Plant Physiology, 82, 597-599.
Vadez, V., Kholova, J., Medina, S., Kakkera, A., & Anderberg, H. (2014). Transpiration efficiency: New insights into an old story. Journal of Experimental Botany, 65, 6141-6153.
Vandeleur, R. K., Mayo, G., Shelden, M. C., Gilliham, M., Kaiser, B. N., & Tyerman, D. S. (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.
Vandeleur, R. K., Sullivan, W., Athman, A., Jordans, C., Gilliham, M., Kaiser, B. N., & Tyerman, S. D. (2014). Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant, Cell & Environment, 37, 520-538.
Vu, N. T., Kang, H. M., Kim, Y. S., Choi, K. Y., & Kim, I. S. (2015). Growth, physiology, and abiotic stress response to abscisic acid in tomato seedlings. Horticulture, Environment, and Biotechnology, 56, 294-304.
Wheeler, J. K., Sperry, J. S., Hacke, U. G., & Hoang, N. (2005). Inter-vessel pitting and cavitation in woody Rosaceae and other vessel led plants: A basis for a safety versus efficiency trade-off in xylem transport. Plant, Cell & Environment, 28, 800-812.
Yang, Z., Liu, J., Poree, F., Schaeufele, R., Helmke, H., Frackenpohl, J., … Grill, E. (2019). Abscisic acid receptors and coreceptors modulate plant water use efficiency and water productivity. Plant Physiology, 180, 1066-1080. https://doi.org/10.1104/pp.18.01238
Yang, Z., Liu, J., Tischer, S. V., Christmann, A., Windisch, W., Schnyder, H., & Grill, E. (2016). Leveraging abscisic acid receptors for efficient water use in Arabidopsis. Proceedings of the National Academy of Sciences, 113, 6791-6796.
Zhang, J., & Davies, W. J. (1989). Sequential response of whole plant water relations to prolonged soil drying and the involvement of xylem sap ABA in the regulation of stomatal behaviour of sunflower plants. New Phytologist, 113, 167-174.