Negative allometry of leaf xylem conduit diameter and double-wall thickness: implications for implosion safety.

drought implosion safety leaf anatomy plant allometry plant hydraulics xylem collapse xylem conduit

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
19 Apr 2024
Historique:
received: 11 12 2023
accepted: 25 03 2024
medline: 20 4 2024
pubmed: 20 4 2024
entrez: 19 4 2024
Statut: aheadofprint

Résumé

Xylem conduits have lignified walls to resist crushing pressures. The thicker the double-wall (T) relative to its diameter (D), the greater the implosion safety. Having safer conduits may incur higher costs and reduced flow, while having less resistant xylem may lead to catastrophic collapse under drought. Although recent studies have shown that conduit implosion commonly occurs in leaves, little is known about how leaf xylem scales T vs D to trade off safety, flow efficiency, mechanical support, and cost. We measured T and D in > 7000 conduits of 122 species to investigate how T vs D scaling varies across clades, habitats, growth forms, leaf, and vein sizes. As conduits become wider, their double-cell walls become proportionally thinner, resulting in a negative allometry between T and D. That is, narrower conduits, which are usually subjected to more negative pressures, are proportionally safer than wider ones. Higher implosion safety (i.e. higher T/D ratios) was found in asterids, arid habitats, shrubs, small leaves, and minor veins. Despite the strong allometry, implosion safety does not clearly trade off with other measured leaf functions, suggesting that implosion safety at whole-leaf level cannot be easily predicted solely by individual conduits' anatomy.

Identifiants

pubmed: 38641796
doi: 10.1111/nph.19771
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Directorate for Biological Sciences
ID : DEB-2025282

Informations de copyright

© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.

Références

Amthor JS. 2003. Efficiency of lignin biosynthesis: a quantitative analysis. Annals of Botany 91: 673–695.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57: 289–300.
Blackman CJ, Brodribb TJ, Jordan GJ. 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 CJ, Gleason SM, Cook AM, Chang Y, Laws CA, Westoby M. 2018. The links between leaf hydraulic vulnerability to drought and key aspects of leaf venation and xylem anatomy among 26 Australian woody angiosperms from contrasting climates. Annals of Botany 122: 59–67.
Blomberg SP, Garland T Jr, Ives AR. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745.
Blonder B, Both S, Jodra M, Xu H, Fricker M, Matos IS, Majalap N, Burslem DFRP, Teh YA, Malhi Y. 2020. Linking functional traits to multiscale statistics of leaf venation networks. New Phytologist 228: 1796–1810.
Bouche PS, Larter M, Domec J‐C, Burlett R, Gasson P, Jansen S, Delzon S. 2014. A broad survey of hydraulic and mechanical safety in the xylem of conifers. Journal of Experimental Botany 65: 4419–4431.
Brodribb TJ, Bienaimé D, Marmottant P. 2016. Revealing catastrophic failure of leaf networks under stress. Proceedings of the National Academy of Sciences, USA 113: 4865–4869.
Brodribb TJ, Holbrook NM. 2005. Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiology 137: 1139–1146.
Carlquist S. 2012. Monocot xylem revisited: new information, new paradigms. The Botanical Review 78: 87–153.
Chin ARO, Guzmán‐Delgado P, Sillett SC, Kerhoulas LP, Ambrose AR, McElrone AR, Zwieniecki MA. 2022. Tracheid buckling buys time, foliar water uptake pays it back: coordination of leaf structure and function in tall redwood trees. Plant, Cell & Environment 45: 2607–2616.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752–755.
Cochard H, Froux F, Mayr S, Coutand C. 2004. Xylem wall collapse in water‐stressed pine needles. Plant Physiology 134: 401–408.
Coomes DA, Heathcote S, Godfrey ER, Shepherd JJ, Sack L. 2008. Scaling of xylem vessels and veins within the leaves of oak species. Biology Letters 23: 302–306.
Ding Y, Zhang Y, Zheng Q‐S, Tyree MT. 2014. Pressure–volume curves: revisiting the impact of negative turgor during cell collapse by literature review and simulations of cell micromechanics. New Phytologist 203: 378–387.
Echeverría A, Petrone‐Mendoza E, Segovia‐Rivas A, Figueroa‐Abundiz VA, Olson ME. 2022. The vessel wall thickness–vessel diameter relationship across woody angiosperms. American Journal of Botany 109: 856–873.
Feild TS, Brodribb TJ. 2013. Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytologist 199: 720–726.
Fontes CG, Pinto‐Ledezma J, Jacobsen AL, Pratt RB, Cavender‐Bares J. 2022. Adaptive variation among oaks in wood anatomical properties is shaped by climate of origin and shows limited plasticity across environments. Functional Ecology 36: 326–340.
Fonti P, Jansen S. 2012. Xylem plasticity in response to climate. New Phytologist 195: 734–736.
Gričar J, Prislan P, De Luis M, Gryc V, Hacurová J, Vavrčík H, Čufar K. 2015. Plasticity in variation of xylem and phloem cell characteristics of Norway spruce under different local conditions. Frontiers in Plant Science 6: 730.
Hacke UG, Sperry JS, Pittermann J. 2004. Analysis of circular bordered pit function II. Gymnosperm tracheids with torus‐margo pit membranes. American Journal of Botany 91: 386–400.
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126: 457–461.
Ikeda CM, Wilkerling J, Duncan JH. 2013. The implosion of cylindrical shell structures in a high‐pressure water environment. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences 469: 20130443.
Jackson DA. 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74: 2204–2214.
Jin Y, Qian H. 2022. v.phylomaker2: an updated and enlarged R package that can generate very large phylogenies for vascular plants. Plant Diversity 44: 335–339.
Johansen DA. 1940. Plant microtechnique. London, UK: McGraw‐Hill Book, 530.
Karam GN. 2005. Biomechanical model of the xylem vessels in vascular plants. Annals of Botany 95: 1179–1186.
Kawai K, Okada N. 2016. How are leaf mechanical properties and water‐use traits coordinated by vein traits? A case study in Fagaceae. Functional Ecology 30: 527–536.
Maitner BS, Boyle B, Casler N, Condit R, Donoghue J, Durán SM, Guaderrama D, Hinchliff CE, Jørgensen PM, Kraft NJB et al. 2018. The bien R package: a tool to access the Botanical Information and Ecology Network (BIEN) database. Methods in Ecology and Evolution 9: 373–379.
McDonald PG, Fonseca CR, Overton JM, Westoby M. 2003. Leaf‐size divergence along rainfall and soil‐nutrient gradients: is the method of size reduction common among clades? Functional Ecology 17: 50–57.
Melcher PJ, Michele Holbrook N, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L. 2012. Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods in Ecology and Evolution 3: 685–694.
Nardini A. 2022. Hard and tough: the coordination between leaf mechanical resistance and drought tolerance. Flora 288: 152023.
Ohtsuka A, Sack L, Taneda H. 2018. Bundle sheath lignification mediates the linkage of leaf hydraulics and venation. Plant, Cell & Environment 41: 342–353.
Pérez‐Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret‐Harte MS, Cornwell WK, Craine JM, Gurvich DE et al. 2016. Corrigendum to: New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 64: 715.
Pittermann J, Limm E, Rico C, Christman MA. 2011. Structure‐function constraints of tracheid‐based xylem: a comparison of conifers and ferns. New Phytologist 192: 449–461.
Pittermann J, Sperry JS, Wheeler JK, Hacke UG, Sikkema EH. 2006. Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant, Cell & Environment 29: 1618–1628.
Pratt RB, Jacobsen AL. 2017. Conflicting demands on angiosperm xylem: tradeoffs among storage, transport and biomechanics. Plant, Cell & Environment 40: 897–913.
R Core Team. 2023. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R‐project.org/ [accessed 10 December 2023].
Read J, Sanson GD, Lamont BB. 2005. Leaf mechanical properties in sclerophyll woodland and shrubland on contrasting soils. Plant and Soil 276: 95–113.
Růžička K, Ursache R, Hejátko J, Helariutta Y. 2015. Xylem development – from the cradle to the grave. New Phytologist 207: 519–535.
Sack L, Scoffoni C. 2012. Measurement of leaf hydraulic conductance and stomatal conductance and their responses to irradiance and dehydration using the evaporative flux method (EFM). Journal of Visualized Experiments 70: 4179.
Shipley B, De Bello F, Cornelissen JHC, Laliberté E, Laughlin DC, Reich PB. 2016. Reinforcing loose foundation stones in trait‐based plant ecology. Oecologia 180: 923–993.
Soltis DE, Bell CD, Kim S, Soltis PS. 2008. Origin and early evolution of angiosperms. Annals of the New York Academy of Sciences 1133: 3–25.
Sperry JS. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164: S115–S127.
Sperry JS, Hacke UG. 2004. Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. American Journal of Botany 91: 369–385.
Sperry JS, Hacke UG, Pittermann J. 2006. Size and function in conifer tracheids and angiosperm vessels. American Journal of Botany 93: 1490–1500.
Timoshenko S. 1930. Strength of materials. London, UK: MacMillan.
Tucker SC. 1964. The terminal idioblasts in magnoliaceous leaves. American Journal of Botany 51: 1051–1062.
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.
Warton DI, Duursma RA, Falster DS, Taskinen S. 2012. smatr 3 – an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3: 257–259.
Webb LJ. 1959. A physiognomic classification of Australian rain forests. Journal of Ecology 47: 551–570.
Xu H, Blonder B, Jodra M, Malhi Y, Fricker M. 2021. Automated and accurate segmentation of leaf venation networks via deep learning. New Phytologist 229: 631–648.
Young WC. 1989. Roark's formulas for stress and strain. New York, NY, USA: McGraw‐Hill.
Zhang Y, Hochberg U, Rockwell FE, Ponomarenko A, Chen Y, Manandhar A, Graham AC, Holbrook NM. 2023. Xylem conduit deformation across vascular plants: an evolutionary spandrel or protective valve? New Phytologist 237: 1242–1255.
Zhang Y‐J, Rockwell FE, Graham AC, Alexander T, Holbrook NM. 2016. Reversible leaf xylem collapse: a potential “circuit breaker” against cavitation. Plant Physiology 172: 2261–2274.
Zhang Y‐J, Rockwell FE, Wheeler JK, Holbrook NM. 2014. Reversible deformation of transfusion tracheids in Taxus baccata is associated with a reversible decrease in leaf hydraulic conductance. Plant Physiology 165: 1557–1565.
Zhong R, Cui D, Ye Z‐H. 2019. Secondary cell wall biosynthesis. New Phytologist 221: 1703–1723.
Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM. 2002. Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25: 1445–1450.

Auteurs

Ilaine Silveira Matos (IS)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.
School of Biological Sciences, The University of Adelaide, Adelaide, SA, 5005, Australia.

Samantha McDonough (S)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Breanna Carrillo Johnson (BC)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Diana Kalantar (D)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

James Rohde (J)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Roshni Sahu (R)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Joyce Wang (J)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Adrian Fontao (A)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Jason To (J)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Sonoma Carlos (S)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Lisa Garcia (L)

Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA.

Mickey Boakye (M)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Holly Forbes (H)

University of California Botanical Garden, Berkeley, CA, 94720, USA.

Benjamin Wong Blonder (BW)

Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, 94720, USA.

Classifications MeSH