Abscisic acid acts essentially on stomata, not on the xylem, to improve drought resistance in tomato.

Solanum lycopersicum embolism resistance hydraulic vulnerability minimum leaf conductance water deficit water loss

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 15 07 2023
received: 10 05 2023
accepted: 22 07 2023
pubmed: 1 8 2023
medline: 1 8 2023
entrez: 1 8 2023
Statut: ppublish

Résumé

Drought resistance is essential for plant production under water-limiting environments. Abscisic acid (ABA) plays a critical role in stomata but its impact on hydraulic function beyond the stomata is far less studied. We selected genotypes differing in their ability to accumulate ABA to investigate its role in drought-induced dysfunction. All genotypes exhibited similar leaf and stem embolism resistance regardless of differences in ABA levels. Their leaf hydraulic resistance was also similar. Differences were only observed between the two extreme genotypes: sitiens (sit; a strong ABA-deficient mutant) and sp12 (a transgenic line that constitutively overaccumulates ABA), where the water potential inducing 50% embolism was 0.25 MPa lower in sp12 than in sit. Maximum stomatal and minimum leaf conductances were considerably lower in plants with higher ABA (wild type [WT] and sp12) than in ABA-deficient mutants. Variations in gas exchange across genotypes were associated with ABA levels and differences in stomatal density and size. The lower water loss in plants with higher ABA meant that lethal water potentials associated with embolism occurred later during drought in sp12 plants, followed by WT, and then by the ABA-deficient mutants. Therefore, the primary pathway by which ABA enhances drought resistance is via declines in water loss, which delays dehydration and hydraulic dysfunction.

Identifiants

pubmed: 37526514
doi: 10.1111/pce.14676
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3229-3241

Subventions

Organisme : U.S. Department of Agriculture
Organisme : National Science Foundation
ID : IOS-2140119

Informations de copyright

© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.

Références

Avila, R.T., Kane, C.N., Batz, T.A., Trabi, C., Damatta, F.M., Jansen, S. et al. (2023) The relative area of vessels in xylem correlates with stem embolism resistance within and between genera. Tree Physiology, 43, 75-87.
Blackman, C.J. & Brodribb, T.J. (2011) Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Functional Plant Biology, 38, 118.
Blackman, C.J., Brodribb, T.J. & Jordan, G.J. (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytologist, 188, 1113-1123.
Blackman, C.J., Li, X., Choat, B., Rymer, P.D., de Kauwe, M.G., Duursma, R.A. et al. (2019) Desiccation time during drought is highly predictable across species of Eucalyptus from contrasting climates. New Phytologist, 224, 632-643.
Brodribb, T.J., Bienaimé, D. & Marmottant, P. (2016) Revealing catastrophic failure of leaf networks under stress. Proceedings of the National Academy of Sciences of the United States of America, 113, 4865-4869.
Brodribb, T.J. & Cochard, H. (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology, 149, 575-584.
Brodribb, T.J. & Holbrook, N.M. (2006) Declining hydraulic efficiency as transpiring leaves desiccate: two types of response. Plant, Cell and Environment, 29, 2205-2215.
Burbidge, A., Grieve, T.M., Jackson, A., Thompson, a, McCarty, D.R. & Taylor, I.B. (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. The Plant Journal, 17, 427-431.
Cardoso, A.A., Batz, T.A. & McAdam, S.A.M. (2020) Xylem embolism resistance determines leaf mortality during drought in Persea americana. Plant Physiology, 182, 547-554.
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.
Cardoso, A.A., Kane, C.N., Rimer, I.M. & McAdam, S.A.M. (2022) Seeing is believing: what visualising bubbles in the xylem has revealed about plant hydraulic function. Functional Plant Biology, 49, 759-772.
Choat, B., Jansen, S., Brodribb, T.J., Cochard, H., Delzon, S., Bhaskar, R. et al. (2012) Global convergence in the vulnerability of forests to drought. Nature, 491, 752-755.
Creek, D., Lamarque, L.J., Torres-Ruiz, J.M., Parise, C., Burlett, R., Tissue, D.T. et al. (2020) Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualization technique. Journal of Experimental Botany, 71, 1151-1159.
Creelman, R.A. & Zeevaart, J.A.D. (1985) Abscisic acid accumulation in spinach leaf slices in the presence of penetrating and nonpenetrating solutes. Plant Physiology, 77, 25-28.
Dai, A. (2013) Increasing drought under global warming in observations and models. Nature Climate Change, 3, 52-58.
Da-li, G., Lei, L., Yu-sen, Y., Feng-wang, M. & Qing-mei, G. (2022) Factors affecting hydraulic conductivity and methods to measure in plants. Journal of Integrative Agriculture, 21, 310-315.
Daszkowska-Golec, A. & Szarejko, I. (2013) Open or close the gate - stomata action under the control of phytohormones in drought stress conditions. Frontiers in Plant Science, 4, 1-16.
Ding, Q., Zeng, J., & He, X.Q. (2016) MiR169 and its target PagHAP2-6 regulated by ABA are involved in poplar cambium dormancy. Journal of Plant Physiology, 198, 1-9.
Dixon, H.H. & Joly, J. (1895) XII. On the ascent of sap. Philosophical Transactions of the Royal Society B, 186, 563-576.
Dória, L.C., Meijs, C., Podadera, D.S., del Arco, M., Smets, E., Delzon, S. et al. (2019) Embolism resistance in stems of herbaceous Brassicaceae and Asteraceae is linked to differences in woodiness and precipitation. Annals of Botany, 124, 1-14.
Dória, L.C., Podadera, D.S., Arco, M., Chauvin, T., Smets, E., Delzon, S. et al. (2018) Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to drought-induced hydraulic failure than their herbaceous relatives. Functional Ecology, 32, 1467-1478.
Duursma, R.A., Blackman, C.J., Lopéz, R., Martin-StPaul, N.K., Cochard, H. & Medlyn, B.E. (2019) On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. New Phytologist, 221, 693-705.
Fromm J. (1997) Hormonal physiology of wood growth in willow (Salix viminalis L.): Effects of spermine and abscisic acid. Wood Science and Technology, 31, 119-130.
Gleason, S.M., Blackman, C.J., Cook, A.M., Laws, C.A. & Westoby, M. (2014) Whole-plant capacitance, embolism resistance and slow transpiration rates all contribute to longer desiccation times in woody angiosperms from arid and wet habitats. Tree Physiology, 34, 275-284.
Harrison, E., Burbidge, A., Okyere, J.P., Thompson, A.J. & Taylor, I.B. (2011) Identification of the tomato ABA-deficient mutant sitiens as a member of the ABA-aldehyde oxidase gene family using genetic and genomic analysis. Plant Growth Regulation, 64, 301-309.
Helander, J.D.M., Vaidya, A.S. & Cutler, S.R. (2016) Chemical manipulation of plant water use. Bioorganic & Medicinal Chemistry, 24, 493-500.
Hou, H.-W., Zhou, Y.-T., Mwange, K.-N., Li, W.-F., He, X.-Q., & Cui, K.-M. (2006) ABP1 expression regulated by IAA and ABA is associated with the cambium periodicity in Eucommia ulmoides Oliv. Journal of Experimental Botany, 57, 3857-3867.
Isasa, E., Link, R.M., Jansen, S., Tezeh, F.R., Kaack, L., Sarmento Cabral, J. et al. (2023) Addressing controversies in the xylem embolism resistance-vessel diameter relationship. New Phytologist, 238, 283-296.
Johnson, K.M., Lucani, C. & Brodribb, T.J. (2022) In vivo monitoring of drought-induced embolism in Callitris rhomboidea trees reveals wide variation in branchlet vulnerability and high resistance to tissue death. New Phytologist, 233, 207-218.
Lamarque, L.J., Delzon, S., Toups, H., Gravel, A.I., Corso, D., Badel, E. et al. (2020) Over-accumulation of abscisic acid in transgenic tomato plants increases the risk of hydraulic failure. Plant, Cell & Environment, 43, 548-562.
Lesk, C., Rowhani, P. & Ramankutty, N. (2016) Influence of extreme weather disasters on global crop production. Nature, 529, 84-87.
Lobell, D.B. & Field, C.B. (2007) Global scale climate-crop yield relationships and the impacts of recent warming. Environmental Research Letters, 2, 014002.
Loepfe, L., Martinez-Vilalta, J., Piñol, J. & Mencuccini, M. (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. Journal of Theoretical Biology, 247, 788-803.
Machado, R., Loram-Lourenço, L., Farnese, F.S., Alves, R.D.F.B., de Sousa, L.F., Silva, F.G. et al. (2021) Where do leaf water leaks come from? Trade-offs underlying the variability in minimum conductance across tropical savanna species with contrasting growth strategies. New Phytologist, 229, 1415-1430.
McAdam, S. (2015) Physicochemical quantification of abscisic acid levels in plant tissues with an added internal standard by ultra-performance liquid chromatography. Bio-Protocol, 5, e1599-e1612.
McAdam, S.A.M. & Brodribb, T.J. (2016) Linking turgor with ABA biosynthesis: implications for stomatal responses to vapor pressure deficit across land plants. Plant Physiology, 171, 2008-2016.
McAdam, S.A.M. & Brodribb, T.J. (2018) Mesophyll cells are the main site of abscisic acid biosynthesis in water-stressed leaves. Plant Physiology, 177, 911-917.
McAdam, S.A.M. & Cardoso, A.A. (2019) The recurrent evolution of extremely resistant xylem. Annals of Forest Science, 76, 2.
Mega, R., Abe, F., Kim, J.S., Tsuboi, Y., Tanaka, K., Kobayashi, H. et al. (2019) Tuning water-use efficiency and drought tolerance in wheat using abscisic acid receptors. Nature Plants, 5, 153-159.
Miyamoto, N., Steudle, E., Hirasawa, T. & Lafitte, R. (2001) Hydraulic conductivity of rice roots. Journal of Experimental Botany, 52, 1835-1846.
Mrad, A., Johnson, D.M., Love, D.M. & Domec, J.C. (2021) The roles of conduit redundancy and connectivity in xylem hydraulic functions. New Phytologist, 231, 996-1007.
Muchow, R.C. & Sinclair, T.R. (1989) Epidermal conductance, stomatal density and stomatal size among genotypes of Sorghum bicolor (L.) Moench. Plant, Cell and Environment, 12, 425-431.
Mwange, K.N.K., Hou, H.W., Wang, Y.Q., He, X.Q., & Cui, K.M. (2005) Opposite patterns in the annual distribution and time-course of endogenous abscisic acid and indole-3-acetic acid in relation to the periodicity of cambial activity in Eucommia ulmoides Oliv. Journal of Experimental Botany, 56, 1017-1028.
Pierce, M. & Raschke, K. (1980) Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta, 148, 174-182.
Posit Team. (2023). RStudio: Integrated development environment for R.
Rodriguez-Dominguez, C.M., Carins Murphy, M.R., Lucani, C. & Brodribb, T.J. (2018) Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytologist, 218, 1025-1035.
Scoffoni, C., Albuquerque, C., Brodersen, C.R., Townes, S.V., John, G.P., Bartlett, M.K. et al. (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiology, 173, 1197-1210.
Sperry, J.S., Donnelly, J.R. & Tyree, M.T. (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell and Environment, 11, 35-40.
Stubbe, H. (1957) Mutanten der Kulturtomate Lycopersicon esculentum Miller I. Die Kulturpflanze, 5, 190-220.
Stubbe, H. (1958) Mutanten der Kulturtomate Lycopersicon esculentum Miller Il. Die Kulturpflanze, 6, 89-115.
Tal, M. & Nevo, Y. (1973) Abnormal stomatal behavior and root resistance, and hormonal imbalance in three wilty mutants of tomato. Biochemical Genetics, 8, 291-300.
Tanaka, Y., Nose, T., Jikumaru, Y. & Kamiya, Y. (2013) ABA inhibits entry into stomatal-lineage development in Arabidopsis leaves. The Plant Journal, 74, 448-457.
Thompson, A.J., Andrews, J., Mulholland, B.J., McKee, J.M.T., Hilton, H.W., Horridge, J.S. et al. (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiology, 143, 1905-1917.
Thompson, N.P. & Heimsch, C. (1964) Stem anatomy and aspects of development in tomato. American Journal of Botany, 51, 7-19.
Thompson, A.J., Jackson, A.C., Symonds, R.C., Mulholland, B.J., Dadswell, A.R., Blake, P.S. et al. (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. et al. (2007) Regulation and manipulation of ABA biosynthesis in roots. Plant, Cell and Environment, 30, 67-78.
Thonglim, A., Bortolami, G., Delzon, S., Larter, M., Offringa, R., Keurentjes, J.J.B. et al. (2023) Drought response in Arabidopsis displays synergistic coordination between stems and leaves. Journal of Experimental Botany, 74, 1004-1021.
Thonglim, A., Delzon, S., Larter, M., Karami, O., Rahimi, A., Offringa, R. et al. (2021) Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions. Annals of Botany, 128, 171-182.
Trueba, S., Pan, R., Scoffoni, C., John, G.P., Davis, S.D. & Sack, L. (2019) Thresholds for leaf damage due to dehydration: declines of hydraulic function, stomatal conductance and cellular integrity precede those for photochemistry. New Phytologist, 223, 134-149.
Tyree, M.T. & Hammel, H.T. (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany, 23, 267-282.
Tyree, M.T. & Sperry, J.S. (1989) Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 19-36.
Venturas, M.D., Sperry, J.S. & Hacke, U.G. (2017) Plant xylem hydraulics: what we understand, current research, and future challenges. Journal of Integrative Plant Biology, 59, 356-389.
Xie, X., Wang, Y., Williamson, L., Holroyd, G.H., Tagliavia, C., Murchie, E. et al. (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Current Biology, 16, 882-887.
Zhang, F.-P., Sussmilch, F., Nichols, D.S., Cardoso, A.A., Brodribb, T.J. & McAdam, S.A.M. (2018) Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms. Journal of Experimental Botany, 69, 1261-1267.

Auteurs

Eduardo J Haverroth (EJ)

Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA.
Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

Leonardo A Oliveira (LA)

Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA.
Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

Moab T Andrade (MT)

Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

Matthew Taggart (M)

Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA.

Scott A M McAdam (SAM)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana, USA.

Agustin Zsögön (A)

Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

Andrew J Thompson (AJ)

Centre for Soil, Agrifood and Biosciences, Cranfield University, Bedfordshire, UK.

Samuel C V Martins (SCV)

Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

Amanda A Cardoso (AA)

Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA.

Classifications MeSH