Cargando…
The Widened Pipe Model of plant hydraulic evolution
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...
Autores principales: | , , , , , , , , , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8179198/ https://www.ncbi.nlm.nih.gov/pubmed/34039710 http://dx.doi.org/10.1073/pnas.2100314118 |
_version_ | 1783703729841635328 |
---|---|
author | Koçillari, Loren Olson, Mark E. Suweis, Samir Rocha, Rodrigo P. Lovison, Alberto Cardin, Franco Dawson, Todd E. Echeverría, Alberto Fajardo, Alex Lechthaler, Silvia Martínez-Pérez, Cecilia Marcati, Carmen Regina Chung, Kuo-Fang Rosell, Julieta A. Segovia-Rivas, Alí Williams, Cameron B. Petrone-Mendoza, Emilio Rinaldo, Andrea Anfodillo, Tommaso Banavar, Jayanth R. Maritan, Amos |
author_facet | Koçillari, Loren Olson, Mark E. Suweis, Samir Rocha, Rodrigo P. Lovison, Alberto Cardin, Franco Dawson, Todd E. Echeverría, Alberto Fajardo, Alex Lechthaler, Silvia Martínez-Pérez, Cecilia Marcati, Carmen Regina Chung, Kuo-Fang Rosell, Julieta A. Segovia-Rivas, Alí Williams, Cameron B. Petrone-Mendoza, Emilio Rinaldo, Andrea Anfodillo, Tommaso Banavar, Jayanth R. Maritan, Amos |
author_sort | Koçillari, Loren |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-8179198 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-81791982021-06-16 The Widened Pipe Model of plant hydraulic evolution Koçillari, Loren Olson, Mark E. Suweis, Samir Rocha, Rodrigo P. Lovison, Alberto Cardin, Franco Dawson, Todd E. Echeverría, Alberto Fajardo, Alex Lechthaler, Silvia Martínez-Pérez, Cecilia Marcati, Carmen Regina Chung, Kuo-Fang Rosell, Julieta A. Segovia-Rivas, Alí Williams, Cameron B. Petrone-Mendoza, Emilio Rinaldo, Andrea Anfodillo, Tommaso Banavar, Jayanth R. Maritan, Amos Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2021-06-01 2021-05-26 /pmc/articles/PMC8179198/ /pubmed/34039710 http://dx.doi.org/10.1073/pnas.2100314118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Biological Sciences Koçillari, Loren Olson, Mark E. Suweis, Samir Rocha, Rodrigo P. Lovison, Alberto Cardin, Franco Dawson, Todd E. Echeverría, Alberto Fajardo, Alex Lechthaler, Silvia Martínez-Pérez, Cecilia Marcati, Carmen Regina Chung, Kuo-Fang Rosell, Julieta A. Segovia-Rivas, Alí Williams, Cameron B. Petrone-Mendoza, Emilio Rinaldo, Andrea Anfodillo, Tommaso Banavar, Jayanth R. Maritan, Amos The Widened Pipe Model of plant hydraulic evolution |
title | The Widened Pipe Model of plant hydraulic evolution |
title_full | The Widened Pipe Model of plant hydraulic evolution |
title_fullStr | The Widened Pipe Model of plant hydraulic evolution |
title_full_unstemmed | The Widened Pipe Model of plant hydraulic evolution |
title_short | The Widened Pipe Model of plant hydraulic evolution |
title_sort | widened pipe model of plant hydraulic evolution |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8179198/ https://www.ncbi.nlm.nih.gov/pubmed/34039710 http://dx.doi.org/10.1073/pnas.2100314118 |
work_keys_str_mv | AT kocillariloren thewidenedpipemodelofplanthydraulicevolution AT olsonmarke thewidenedpipemodelofplanthydraulicevolution AT suweissamir thewidenedpipemodelofplanthydraulicevolution AT rocharodrigop thewidenedpipemodelofplanthydraulicevolution AT lovisonalberto thewidenedpipemodelofplanthydraulicevolution AT cardinfranco thewidenedpipemodelofplanthydraulicevolution AT dawsontodde thewidenedpipemodelofplanthydraulicevolution AT echeverriaalberto thewidenedpipemodelofplanthydraulicevolution AT fajardoalex thewidenedpipemodelofplanthydraulicevolution AT lechthalersilvia thewidenedpipemodelofplanthydraulicevolution AT martinezperezcecilia thewidenedpipemodelofplanthydraulicevolution AT marcaticarmenregina thewidenedpipemodelofplanthydraulicevolution AT chungkuofang thewidenedpipemodelofplanthydraulicevolution AT roselljulietaa thewidenedpipemodelofplanthydraulicevolution AT segoviarivasali thewidenedpipemodelofplanthydraulicevolution AT williamscameronb thewidenedpipemodelofplanthydraulicevolution AT petronemendozaemilio thewidenedpipemodelofplanthydraulicevolution AT rinaldoandrea thewidenedpipemodelofplanthydraulicevolution AT anfodillotommaso thewidenedpipemodelofplanthydraulicevolution AT banavarjayanthr thewidenedpipemodelofplanthydraulicevolution AT maritanamos thewidenedpipemodelofplanthydraulicevolution AT kocillariloren widenedpipemodelofplanthydraulicevolution AT olsonmarke widenedpipemodelofplanthydraulicevolution AT suweissamir widenedpipemodelofplanthydraulicevolution AT rocharodrigop widenedpipemodelofplanthydraulicevolution AT lovisonalberto widenedpipemodelofplanthydraulicevolution AT cardinfranco widenedpipemodelofplanthydraulicevolution AT dawsontodde widenedpipemodelofplanthydraulicevolution AT echeverriaalberto widenedpipemodelofplanthydraulicevolution AT fajardoalex widenedpipemodelofplanthydraulicevolution AT lechthalersilvia widenedpipemodelofplanthydraulicevolution AT martinezperezcecilia widenedpipemodelofplanthydraulicevolution AT marcaticarmenregina widenedpipemodelofplanthydraulicevolution AT chungkuofang widenedpipemodelofplanthydraulicevolution AT roselljulietaa widenedpipemodelofplanthydraulicevolution AT segoviarivasali widenedpipemodelofplanthydraulicevolution AT williamscameronb widenedpipemodelofplanthydraulicevolution AT petronemendozaemilio widenedpipemodelofplanthydraulicevolution AT rinaldoandrea widenedpipemodelofplanthydraulicevolution AT anfodillotommaso widenedpipemodelofplanthydraulicevolution AT banavarjayanthr widenedpipemodelofplanthydraulicevolution AT maritanamos widenedpipemodelofplanthydraulicevolution |