The Widened Pipe Model of plant hydraulic evolution.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
01 06 2021
Historique:
entrez: 27 5 2021
pubmed: 28 5 2021
medline: 15 12 2021
Statut: ppublish

Résumé

Shaping global water and carbon cycles, plants lift water from roots to leaves through xylem conduits. The importance of xylem water conduction makes it crucial to understand how natural selection deploys conduit diameters within and across plants. Wider conduits transport more water but are likely more vulnerable to conduction-blocking gas embolisms and cost more for a plant to build, a tension necessarily shaping xylem conduit diameters along plant stems. We build on this expectation to present the Widened Pipe Model (WPM) of plant hydraulic evolution, testing it against a global dataset. The WPM predicts that xylem conduits should be narrowest at the stem tips, widening quickly before plateauing toward the stem base. This universal profile emerges from Pareto modeling of a trade-off between just two competing vectors of natural selection: one favoring rapid widening of conduits tip to base, minimizing hydraulic resistance, and another favoring slow widening of conduits, minimizing carbon cost and embolism risk. Our data spanning terrestrial plant orders, life forms, habitats, and sizes conform closely to WPM predictions. The WPM highlights carbon economy as a powerful vector of natural selection shaping plant function. It further implies that factors that cause resistance in plant conductive systems, such as conduit pit membrane resistance, should scale in exact harmony with tip-to-base conduit widening. Furthermore, the WPM implies that alterations in the environments of individual plants should lead to changes in plant height, for example, shedding terminal branches and resprouting at lower height under drier climates, thus achieving narrower and potentially more embolism-resistant conduits.

Identifiants

pubmed: 34039710
pii: 2100314118
doi: 10.1073/pnas.2100314118
pmc: PMC8179198
pii:
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2021 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Loren Koçillari (L)

Dipartimento di Fisica e Astronomia G. Galilei, Istituto Nazionale di Fisica Nucleare, Università di Padova, 35131 Padova, Italy.
Laboratory of Neural Computation, Istituto Italiano di Tecnologia, 38068 Rovereto, Italy.

Mark E Olson (ME)

Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México 04510, Mexico; molson@ib.unam.mx andrea.rinaldo@epfl.ch banavar@uoregon.edu.

Samir Suweis (S)

Dipartimento di Fisica e Astronomia G. Galilei, Istituto Nazionale di Fisica Nucleare, Università di Padova, 35131 Padova, Italy.

Rodrigo P Rocha (RP)

Departamento de Física, Universidade Federal de Santa Catarina, Florianópolis-SC 88040-900, Brazil.

Alberto Lovison (A)

Dipartimento di Matematica Tullio Levi-Civita, Università di Padova, 35121 Padova, Italy.

Franco Cardin (F)

Dipartimento di Matematica Tullio Levi-Civita, Università di Padova, 35121 Padova, Italy.

Todd E Dawson (TE)

Department of Integrative Biology, University of California, Berkeley, CA 94720-3140.
Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3140.

Alberto Echeverría (A)

Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México 04510, Mexico.

Alex Fajardo (A)

Instituto de Investigación Interdisciplinario (I), Universidad de Talca, Campus Lircay, Talca 3460000, Chile.

Silvia Lechthaler (S)

Dipartimento Territorio e Sistemi Agro-Forestali, Università di Padova, Legnaro 35020, Italy.

Cecilia Martínez-Pérez (C)

Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México 04510, Mexico.
Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, 04510 Ciudad de México, Mexico.

Carmen Regina Marcati (CR)

Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, São Paulo 18603970, Brazil.

Kuo-Fang Chung (KF)

Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan.

Julieta A Rosell (JA)

Laboratorio Nacional de Ciencias de la Sostenibilidad, Instituto de Ecología, Universidad Nacional Autónoma de México, 04510 Ciudad de México, Mexico.

Alí Segovia-Rivas (A)

Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México 04510, Mexico.

Cameron B Williams (CB)

Department of Integrative Biology, University of California, Berkeley, CA 94720-3140.
Channel Islands National Park, Ventura, CA 93001-4354.
Santa Barbara Botanic Garden, Santa Barbara, CA 93105-2126.
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-7014.

Emilio Petrone-Mendoza (E)

Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México 04510, Mexico.

Andrea Rinaldo (A)

Laboratory of Ecohydrology, IIE/ENAC, Ecole Polytechinque Fédérale de Lausanne, 1015 Lausanne, Switzerland; molson@ib.unam.mx andrea.rinaldo@epfl.ch banavar@uoregon.edu.
Dipartimento Ingegneria Civile Edile e Ambientale, Università di Padova, 35131 Padova, Italy.

Tommaso Anfodillo (T)

Dipartimento Territorio e Sistemi Agro-Forestali, Università di Padova, Legnaro 35020, Italy.

Jayanth R Banavar (JR)

Department of Physics, University of Oregon, Eugene, OR 97403; molson@ib.unam.mx andrea.rinaldo@epfl.ch banavar@uoregon.edu.
Institute for Fundamental Science, University of Oregon, Eugene, OR 97403.

Amos Maritan (A)

Dipartimento di Fisica e Astronomia G. Galilei, Istituto Nazionale di Fisica Nucleare, Università di Padova, 35131 Padova, Italy.

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