دورية أكاديمية

Gradients in embolism resistance within stems driven by secondary growth in herbs.

التفاصيل البيبلوغرافية
العنوان: Gradients in embolism resistance within stems driven by secondary growth in herbs.
المؤلفون: Haverroth EJ; Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA., Rimer IM; Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana, USA., Oliveira LA; Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA., de Lima LGA; Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil.; Synthetic and Systems Biology Center, InovaUSP, Avenida Professor Lucio Martins Rodrigues, São Paulo, Brazil., Cesarino I; Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil.; Synthetic and Systems Biology Center, InovaUSP, Avenida Professor Lucio Martins Rodrigues, São Paulo, Brazil., Martins SCV; Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Brazil., McAdam SAM; Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana, USA., Cardoso AA; Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina, USA.
المصدر: Plant, cell & environment [Plant Cell Environ] 2024 Aug; Vol. 47 (8), pp. 2986-2998. Date of Electronic Publication: 2024 Apr 21.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: John Wiley & Sons Ltd Country of Publication: United States NLM ID: 9309004 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-3040 (Electronic) Linking ISSN: 01407791 NLM ISO Abbreviation: Plant Cell Environ Subsets: MEDLINE
أسماء مطبوعة: Publication: Hoboken, NJ : John Wiley & Sons Ltd.
Original Publication: Oxford, UK : Blackwell Scientific Publications
مواضيع طبية MeSH: Plant Stems*/growth & development , Plant Stems*/physiology , Plant Leaves*/growth & development , Plant Leaves*/physiology, Xylem/physiology ; Xylem/growth & development ; Solanum lycopersicum/growth & development ; Solanum lycopersicum/physiology ; Lignin/metabolism ; Combretaceae/physiology ; Combretaceae/growth & development
مستخلص: The stems of some herbaceous species can undergo basal secondary growth, leading to a continuum in the degree of woodiness along the stem. Whether the formation of secondary growth in the stem base results in differences in embolism resistance between the base and the upper portions of stems is unknown. We assessed the embolism resistance of leaves and the basal and upper portions of stems simultaneously within the same individuals of two divergent herbaceous species that undergo secondary growth in the mature stem bases. The species were Solanum lycopersicum (tomato) and Senecio minimus (fireweed). Basal stem in mature plants of both species displayed advanced secondary growth and greater resistance to embolism than the upper stem. This also resulted in significant vulnerability segmentation between the basal stem and the leaves in both species. Greater embolism resistance in the woodier stem base was found alongside decreases in the pith-to-xylem ratio, increases in the proportion of secondary xylem, and increases in lignin content. We show that there can be considerable variation in embolism resistance across the stem in herbs and that this variation is linked to the degree of secondary growth present. A gradient in embolism resistance across the stem in herbaceous plants could be an adaptation to ensure reproduction or basal resprouting during episodes of drought late in the lifecycle.
(© 2024 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.)
References: Alder, N.N., Sperry, J.S. & Pockman, W.T. (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia, 105, 293–301.
Avila, R.T., Cardoso, A.A., Batz, T.A., Kane, C.N., DaMatta, F.M. & McAdam, S.A.M. (2021) Limited plasticity in embolism resistance in response to light in leaves and stems in species with considerable vulnerability segmentation. Physiologia Plantarum, 172, 2142–2152.
Avila, R.T., Guan, X., Kane, C.N., Cardoso, A.A., Batz, T.A., DaMatta, F.M. et al. (2022) Xylem embolism spread is largely prevented by interconduit pit membranes until the majority of conduits are gas‐filled. Plant, Cell & Environment, 45, 1204–1215.
Bouche, P.S., Delzon, S., Choat, B., Badel, E., Brodribb, T.J., Burlett, R. et al. (2016) Are needles of Pinus pinaster more vulnerable to xylem embolism than branches? New insights from X‐ray computed tomography. Plant, Cell & Environment, 39, 860–870.
Bourbia, I., Carins‐Murphy, M.R., Gracie, A. & Brodribb, T.J. (2020) Xylem cavitation isolates leaky flowers during water stress in pyrethrum. New Phytologist, 227, 146–155.
Brodersen, C.R., Mcelrone, A.J., Choat, B., Lee, E.F., Shackel, K.A. & Matthews, M.A. (2013) In vivo visualizations of drought‐induced embolism spread in vitis vinifera. Plant Physiology, 161, 1820–1829.
Brodribb, T., Brodersen, C.R., Carriqui, M., Tonet, V., Rodriguez Dominguez, C. & McAdam, S. (2021) Linking xylem network failure with leaf tissue death. New Phytologist, 232, 68–79.
Brodribb, T.J., Bienaimé, D. & Marmottant, P. (2016a) 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., Carriqui, M., Delzon, S. & Lucani, C. (2017) Optical measurement of stem xylem vulnerability. Plant Physiology, 174, 2054–2061.
Brodribb, T.J., Skelton, R.P., Mcadam, S.A.M., Bienaimé, D., Lucani, C.J. & Marmottant, P. (2016b) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist, 209, 1403–1409.
Cardoso, A.A. (2022) Linking leaf embolism resistance with pit membrane characteristics. Plant Physiology, 190, 185–187.
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., 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., Badel, E., Burlett, R., Delzon, S., Cochard, H. & Jansen, S. (2016) Noninvasive measurement of vulnerability to drought‐induced embolism by X‐Ray microtomography. Plant Physiology, 170, 273–282.
Choat, B., Brodersen, C.R. & McElrone, A.J. (2015) Synchrotron X‐ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytologist, 205, 1095–1105.
Choat, B., Cobb, A.R. & Jansen, S. (2008) Structure and function of bordered pits: new discoveries and impacts on whole‐plant hydraulic function. New Phytologist, 177, 608–626.
Choat, B., Drayton, W.M., Brodersen, C., Matthews, M.A., Shackel, K.A., Wada, H.I.R. et al. (2010) Measurement of vulnerability to water stress‐induced cavitation in grapevine: a comparison of four techniques applied to a long‐vesseled species. Plant, Cell and Environment, 33, 1502–1512.
Choat, B., Jansen, S., Zwieniecki, M.A., Smets, E. & Holbrook, N.M. (2004) Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. Journal of Experimental Botany, 55, 1569–1575.
Choat, B., Lahr, E.C., Melcher, P.J., Zwieniecki, M.A. & Holbrook, N.M. (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant, Cell & Environment, 28, 1082–1089.
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.
Cremer, K. & Mount.A.B, A.B. (1965) Early stages of plant succession following the complete felling and burning of Eucalyptus regnans forest in the Florentine Valley, Tasmania. Australian Journal of Botany, 13, 303.
Dixon, H.H. & Joly, J. (1895) XII. On the ascent of sap. Philosophical Transactions of the Royal Society of London. (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., del 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.
Esau, K. (1977) Anatomy of seed plants, 2nd ed. New York: John Wiley & Sons Ltd.
Fromm, J., Rockel, B., Lautner, S., Windeisen, E. & Wanner, G. (2003) Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques. Journal of Structural Biology, 143, 77–84.
Fukushima, R.S. & Kerley, M.S. (2011) Use of lignin extracted from different plant sources as standards in the spectrophotometric acetyl bromide lignin method. Journal of Agricultural and Food Chemistry, 59, 3505–3509.
Hacke, U.G., Sperry, J.S., Pockman, W.T., Davis, S.D. & McCulloh, K.A. (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia, 126, 457–461.
Hammond, W.M., Yu, K., Wilson, L.A., Will, R.E., Anderegg, W.R.L. & Adams, H.D. (2019) Dead or dying? Quantifying the point of no return from hydraulic failure in drought‐induced tree mortality. New Phytologist, 223, 1834–1843.
Hao, G.‐Y., Wheeler, J.K., Holbrook, N.M. & 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.
Harrison Day, B.L. & Brodribb, T.J. (2023) Resistant xylem from roots to peduncles sustains reproductive water supply after drought‐induced cavitation of wheat leaves. Annals of Botany, 131, 839–850.
Harrison Day, B.L., Carins‐Murphy, M.R. & Brodribb, T.J. (2022) Reproductive water supply is prioritized during drought in tomato. Plant, Cell & Environment, 45, 69–79.
Harrison Day, B.L., Johnson, K.M., Tonet, V., Bourbia, I., Blackman, C. & Brodribb, T.J. (2023) The root of the problem: diverse vulnerability to xylem cavitation found within the root system of wheat plants. New Phytologist, 239, 1239–1252.
Haverroth, E.J., Oliveira, L.A., Andrade, M.T., Taggart, M., McAdam, S.A.M., Zsögön, A. et al. (2023) Abscisic acid acts essentially on stomata, not on the xylem, to improve drought resistance in tomato. Plant, Cell & Environment, 46, 3229–3241.
Herbette, S., Bouchet, B., Brunel, N., Bonnin, E., Cochard, H. & Guillon, F. (2015) Immunolabelling of intervessel pits for polysaccharides and lignin helps in understanding their hydraulic properties in Populus tremula × alba. Annals of Botany, 115, 187–199.
Holbrook, N.M., Ahrens, E.T., Burns, M.J. & Zwieniecki, M.A. (2001) In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiology, 126, 27–31.
Johansen, D.A. (1940) Plant microtechnique. New York: McGraw‐Hill.
Johnson, D.M., McCulloh, K.A., Woodruff, D.R. & Meinzer, F.C. (2012) Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Science, 195, 48–53.
Johnson, D.M., Wortemann, R., McCulloh, K.A., Jordan‐Meille, L., Ward, E., Warren, J.M. et al. (2016) A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. Tree Physiology, 36, 983–993.
Johnson, K.M. & Brodribb, T.J. (2023) Evidence for a trade‐off between growth rate and xylem cavitation resistance in Callitris rhomboidea. Tree Physiology, 43, 1055–1065.
Johnson, K.M. & Fletcher, L.R. (2023) A herbaceous species provides insights into drought‐driven plant adaptation. Journal of Experimental Botany, 74, 680–683.
Kaack, L., Weber, M., Isasa, E., Karimi, Z., Li, S., Pereira, L. et al. (2021) Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms. New Phytologist, 230, 1829–1843.
Kidner, C., Groover, A., Thomas, D.C., Emelianova, K., Soliz‐Gamboa, C. & Lens, F. (2015) First steps in studying the origins of secondary woodiness inBegonia(Begoniaceae): combining anatomy, phylogenetics, and stem transcriptomics: secondary woodiness in Begonia. Biological Journal of the Linnean Society, 117, 121–138.
Klepsch, M., Zhang, Y., Kotowska, M.M., Lamarque, L.J., Nolf, M., Schuldt, B. et al. (2018) Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy. Journal of Experimental Botany, 69, 5611–5623.
Kolb & Sperry. (1999) Transport constraints on water use by the Great Basin shrub, Artemisia tridentata. Plant, Cell & Environment, 22, 925–935.
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.
Lens, F., Gleason, S.M., Bortolami, G., Brodersen, C., Delzon, S. & Jansen, S. (2022) Functional xylem characteristics associated with drought‐induced embolism in angiosperms. New Phytologist, 236, 2019–2036.
Lens, F., Picon‐Cochard, C., Delmas, C.E., Signarbieux, C., Buttler, A., Cochard, H. et al. (2016) Herbaceous angiosperms are not more vulnerable to drought‐induced embolism than angiosperm trees. Plant Physiology, 172, pp. 00829.2016.
Levionnois, S., Jansen, S., Wandji, R.T., Beauchêne, J., Ziegler, C., Coste, S. et al. (2021) Linking drought‐induced xylem embolism resistance to wood anatomical traits in neotropical trees. New Phytologist, 229, 1453–1466.
Levionnois, S., Kaack, L., Heuret, P., Abel, N., Ziegler, C., Coste, S. et al. (2022) Pit characters determine drought‐induced embolism resistance of leaf xylem across 18 neotropical tree species. Plant Physiology, 190, 371–386.
Li, S., Lens, F., Espino, S., Karimi, Z., Klepsch, M., Schenk, H.J. et al. (2016) Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA Journal, 37, 152–171.
Li, X., Delzon, S., Torres‐Ruiz, J., Badel, E., Burlett, R., Cochard, H. et al. (2020) Lack of vulnerability segmentation in four angiosperm tree species: evidence from direct X‐ray microtomography observation. Annals of Forest Science, 77, 37.
McAdam, S.A.M., Brodribb, T.J., Ross, J.J. & Jordan, G.J. (2011) Augmentation of abscisic acid (ABA) levels by drought does not induce short‐term stomatal sensitivity to CO2 in two divergent conifer species. Journal of Experimental Botany, 62, 195–203.
McAdam, S.A.M. & Cardoso, A.A. (2019) The recurrent evolution of extremely resistant xylem. Annals of Forest Science, 76, 2–5.
McCulloh, K., Sperry, J.S., Lachenbruch, B., Meinzer, F.C., Reich, P.B. & Voelker, S. (2010) Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring‐porous, and diffuse‐porous saplings from temperate and tropical forests. New Phytologist, 186, 439–450.
Mencuccini, M. & Comstock, J. (1997) Vulnerability to cavitation in populations of two desert species, Hymenoclea salsola and Ambrosia dumosa, from different climatic regions. Journal of Experimental Botany, 48, 1323–1334.
Miller, M.L. & Johnson, D.M. (2017) Vascular development in very young conifer seedlings: theoretical hydraulic capacities and potential resistance to embolism. American Journal of Botany, 104, 979–992.
Pereira, L., Domingues‐Junior, A.P., Jansen, S., Choat, B. & Mazzafera, P. (2018) Is embolism resistance in plant xylem associated with quantity and characteristics of lignin? Trees, 32, 349–358.
Posit Team (2023) RStudio: Integrated Development Environment for R.
Roddy, A.B., Guilliams, C.M., Fine, P.V.A., Mambelli, S., Dawson, T.E. & Simonin, K.A. (2023) Flowers are leakier than leaves but cheaper to build. New Phytologist, 239, 2076–2082.
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.
Schmitz, N., Koch, G., Schmitt, U., Beeckman, H. & Koedam, N. (2008) Intervessel pit structure and histochemistry of two mangrove species as revealed by cellular UV microspectrophotometry and electron microscopy: intraspecific variation and functional significance. Microscopy and Microanalysis, 14, 387–397.
Scholz, A., Klepsch, M., Karimi, Z. & Jansen, S. (2013) How to quantify conduits in wood? Frontiers in Plant Science, 4, 4.
Skelton, R.P., Anderegg, L.D.L., Papper, P., Reich, E., Dawson, T.E., Kling, M. et al. (2019) No local adaptation in leaf or stem xylem vulnerability to embolism, but consistent vulnerability segmentation in a North American oak. New Phytologist, 223, 1296–1306.
Skelton, R.P., Brodribb, T.J. & Choat, B. (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytologist, 214, 561–569.
Smith‐Martin, C.M., Skelton, R.P., Johnson, K.M., Lucani, C. & Brodribb, T.J. (2020) Lack of vulnerability segmentation among woody species in a diverse dry sclerophyll woodland community. Functional Ecology, 34, 777–787.
Sperry, J.S. & Ikeda, T. (1997) Xylem cavitation in roots and stems of Douglas‐fir and White fir. Tree Physiology, 17, 275–280.
Strock, C.F. & Lynch, J.P. (2020) Root secondary growth: an unexplored component of soil resource acquisition. Annals of Botany, 126, 205–218.
Thompson, N.P. & Heimsch, C. (1964) Stem anatomy and aspects of development in tomato. American Journal of Botany, 51, 7–19.
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.
Tixier, A., Cochard, H., Badel, E., Dusotoit‐Coucaud, A., Jansen, S. & Herbette, S. (2013) Arabidopsis thaliana as a model species for xylem hydraulics: does size matter? Journal of Experimental Botany, 64, 2295–2305.
Tixier, A., Herbette, S., Jansen, S., Capron, M., Tordjeman, P., Cochard, H. et al. (2014) Modelling the mechanical behaviour of pit membranes in bordered pits with respect to cavitation resistance in angiosperms. Annals of Botany, 114, 325–334.
Tonet, V., Carins‐Murphy, M., Deans, R. & Brodribb, T.J. (2023) Deadly acceleration in dehydration of Eucalyptus viminalis leaves coincides with high‐order vein cavitation. Plant Physiology, 191, 1648–1661.
Tyree, M.T. & Ewers, F.W. (1991) The hydraulic architecture of trees and other woody plants. New Phytologist, 119, 345–360.
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.
Urli, M., Porte, A.J., Cochard, H., Guengant, Y., Burlett, R. & Delzon, S. (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology, 33, 672–683.
Venturas, M.D., Pratt, R.B., Jacobsen, A.L., Castro, V., Fickle, J.C. & Hacke, U.G. (2019) Direct comparison of four methods to construct xylem vulnerability curves: differences among techniques are linked to vessel network characteristics. Plant, Cell & Environment, 42, 2422–2436.
Wapstra, M., Thompson, I. & Buchanan, A. (2008) An illustrated and annotated key to the Tasmanian species of Senecio (Asteraceae). Kanunnah, 3, 49–93.
Wilkening, J.V., Skelton, R.P., Feng, X., Dawson, T.E. & Thompson, S.E. (2023) Exploring within‐plant hydraulic trait variation: a test of the vulnerability segmentation hypothesis. Plant, Cell & Environment, 46, 2726–2746.
Wolfe, B.T., Sperry, J.S. & Kursar, T.A. (2016) Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis. New Phytologist, 212, 1007–1018.
Zhang, F.P. & Brodribb, T.J. (2017) Are flowers vulnerable to xylem cavitation during drought? Proceedings of the Royal Society B: Biological Sciences, 284, 20162642.
معلومات مُعتمدة: IOS-2140119 National Institute of Food and Agriculture; Hatch Project 7003279 National Science Foundation
فهرسة مساهمة: Keywords: cavitation; drought resistance; lignin; secondary xylem; vulnerability segmentation; woodiness
المشرفين على المادة: 9005-53-2 (Lignin)
تواريخ الأحداث: Date Created: 20240422 Date Completed: 20240711 Latest Revision: 20240711
رمز التحديث: 20240711
DOI: 10.1111/pce.14921
PMID: 38644584
قاعدة البيانات: MEDLINE
الوصف
تدمد:1365-3040
DOI:10.1111/pce.14921