The Widened Pipe Model of plant hydraulic evolution

Detalhes bibliográficos
Autor(a) principal: Kocillari, Loren
Data de Publicação: 2021
Outros Autores: Olson, Mark E., Suweis, Samir, Rocha, Rodrigo P., Lovison, Alberto, Cardin, Franco, Dawson, Todd E., Echeverria, Alberto, Fajardo, Alex, Lechthaler, Silvia, Martinez-Perez, Cecilia, Marcati, Carmen Regina [UNESP], Chung, Kuo-Fang, Rosell, Julieta A., Segovia-Rivas, Ali, Williams, Cameron B., Petrone-Mendoza, Emilio, Rinaldo, Andrea, Anfodillo, Tommaso, Banavar, Jayanth R., Maritan, Amos
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1073/pnas.2100314118|1of8
http://hdl.handle.net/11449/210811
Resumo: 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 tradeoff 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.
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spelling The Widened Pipe Model of plant hydraulic evolutionplant hydraulicsxylemPareto optimalityallometryadaptationShaping 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 tradeoff 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.Cariparo FoundationSwiss National Science FoundationPhysics and Astronomy Department of the University of PadovaIstituto Nazionale di Fisica Nucleare, Padova sectionUniversity of PadovaFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Direccion General de Asuntos del Personal Academico, Universidad Nacional Autonoma de MexicoNSF Integrative Graduate Education and Research Traineeship awardConsejo Nacional de Ciencia y TecnologiaPrograma de Apoyo a Proyectos de Investigacion e Innovacion Tecnologica, Universidad Nacional Autonoma de MexicoUniversity of California Institute for Mexico and the United StatesFondecytNSFAcademia SinicaKnight Chair from the University of OregonUniv Padua, Ist Nazl Fis Nucl, Dipartimento Fis & Astron G Galilei, I-35131 Padua, ItalyIst Italiano Tecnol, Lab Neural Computat, I-38068 Rovereto, ItalyUniv Nacl Autonoma Mexico, Inst Biol, Ciudad De Mexico 04510, MexicoUniv Fed Santa Catarina, Dept Fis, BR-88040900 Florianopolis, SC, BrazilUniv Padua, Dipartimento Matemat Tullio Levi Civita, I-35121 Padua, ItalyUniv Calif Berkeley, Dept Integrat Biol, Berkeley, CA 94720 USAUniv Calif Berkeley, Dept Environm Sci Policy & Management, Berkeley, CA 94720 USAUniv Talca, Lnstituto Invest Interdisciplinario 13, Campus Lircay, Talca 3460000, ChileUniv Padua, Dipartimento Terr & Sistemi Agroforestali, I-35020 Legnaro, ItalyUniv Nacl Autonoma Mexico, Inst Ecol, Dept Ecol Evolut, Ciudad De Mexico 04510, MexicoUniv Estadual Paulista, Fac Ciencias Agronom, BR-18603970 Sao Paulo, BrazilAcad Sinica, Biodivers Res Ctr, Taipei 11529, TaiwanUniv Nacl Autonoma Mexico, Inst Ecol, Lab Nacl Ciencias Sostenibilidad, Ciudad De Mexico 04510, MexicoChannel Isl Natl Pk, Ventura, CA 93001 USASanta Barbara Bot Garden, Santa Barbara, CA 93105 USANo Arizona Univ, Dept Biol Sci, Flagstaff, AZ 86011 USAEcole Polytechinque Fed Lausanne, Lab Ecohydrol, IIE ENAC, CH-1015 Lausanne, SwitzerlandUniv Padua, Dipartimento Ingn Civile Edile & Ambientale, I-35131 Padua, ItalyUniv Oregon, Dept Phys, Eugene, OR 97403 USAUniv Oregon, Inst Fundamental Sci, Eugene, OR 97403 USAUniv Estadual Paulista, Fac Ciencias Agronom, BR-18603970 Sao Paulo, BrazilSwiss National Science Foundation: CRSII5_186422Physics and Astronomy Department of the University of Padova: SUWE\BIRD2020\01FAPESP: 2018/086098FAPESP: 2014/14778-6FAPESP: 2015/14954-1NSF Integrative Graduate Education and Research Traineeship award: 0549505Consejo Nacional de Ciencia y Tecnologia: A1-S-26934Consejo Nacional de Ciencia y Tecnologia: 237061Programa de Apoyo a Proyectos de Investigacion e Innovacion Tecnologica, Universidad Nacional Autonoma de Mexico: IN210719Programa de Apoyo a Proyectos de Investigacion e Innovacion Tecnologica, Universidad Nacional Autonoma de Mexico: IN210220University of California Institute for Mexico and the United States: CN-15-1428Fondecyt: 1160329Fondecyt: 1190900NSF: IOS-1010769Natl Acad SciencesUniv PaduaIst Italiano TecnolUniv Nacl Autonoma MexicoUniversidade Federal de Santa Catarina (UFSC)Univ Calif BerkeleyUniv TalcaUniversidade Estadual Paulista (Unesp)Acad SinicaChannel Isl Natl PkSanta Barbara Bot GardenNo Arizona UnivEcole Polytechinque Fed LausanneUniv OregonKocillari, LorenOlson, Mark E.Suweis, SamirRocha, Rodrigo P.Lovison, AlbertoCardin, FrancoDawson, Todd E.Echeverria, AlbertoFajardo, AlexLechthaler, SilviaMartinez-Perez, CeciliaMarcati, Carmen Regina [UNESP]Chung, Kuo-FangRosell, Julieta A.Segovia-Rivas, AliWilliams, Cameron B.Petrone-Mendoza, EmilioRinaldo, AndreaAnfodillo, TommasoBanavar, Jayanth R.Maritan, Amos2021-06-26T08:03:36Z2021-06-26T08:03:36Z2021-06-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article8http://dx.doi.org/10.1073/pnas.2100314118|1of8Proceedings Of The National Academy Of Sciences Of The United States Of America. Washington: Natl Acad Sciences, v. 118, n. 22, 8 p., 2021.0027-8424http://hdl.handle.net/11449/21081110.1073/pnas.2100314118|1of8WOS:000659434200001Web of Sciencereponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengProceedings Of The National Academy Of Sciences Of The United States Of Americainfo:eu-repo/semantics/openAccess2024-04-30T13:11:27Zoai:repositorio.unesp.br:11449/210811Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T23:18:37.473551Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv The Widened Pipe Model of plant hydraulic evolution
title The Widened Pipe Model of plant hydraulic evolution
spellingShingle The Widened Pipe Model of plant hydraulic evolution
Kocillari, Loren
plant hydraulics
xylem
Pareto optimality
allometry
adaptation
title_short 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_sort The Widened Pipe Model of plant hydraulic evolution
author Kocillari, Loren
author_facet Kocillari, Loren
Olson, Mark E.
Suweis, Samir
Rocha, Rodrigo P.
Lovison, Alberto
Cardin, Franco
Dawson, Todd E.
Echeverria, Alberto
Fajardo, Alex
Lechthaler, Silvia
Martinez-Perez, Cecilia
Marcati, Carmen Regina [UNESP]
Chung, Kuo-Fang
Rosell, Julieta A.
Segovia-Rivas, Ali
Williams, Cameron B.
Petrone-Mendoza, Emilio
Rinaldo, Andrea
Anfodillo, Tommaso
Banavar, Jayanth R.
Maritan, Amos
author_role author
author2 Olson, Mark E.
Suweis, Samir
Rocha, Rodrigo P.
Lovison, Alberto
Cardin, Franco
Dawson, Todd E.
Echeverria, Alberto
Fajardo, Alex
Lechthaler, Silvia
Martinez-Perez, Cecilia
Marcati, Carmen Regina [UNESP]
Chung, Kuo-Fang
Rosell, Julieta A.
Segovia-Rivas, Ali
Williams, Cameron B.
Petrone-Mendoza, Emilio
Rinaldo, Andrea
Anfodillo, Tommaso
Banavar, Jayanth R.
Maritan, Amos
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Univ Padua
Ist Italiano Tecnol
Univ Nacl Autonoma Mexico
Universidade Federal de Santa Catarina (UFSC)
Univ Calif Berkeley
Univ Talca
Universidade Estadual Paulista (Unesp)
Acad Sinica
Channel Isl Natl Pk
Santa Barbara Bot Garden
No Arizona Univ
Ecole Polytechinque Fed Lausanne
Univ Oregon
dc.contributor.author.fl_str_mv Kocillari, Loren
Olson, Mark E.
Suweis, Samir
Rocha, Rodrigo P.
Lovison, Alberto
Cardin, Franco
Dawson, Todd E.
Echeverria, Alberto
Fajardo, Alex
Lechthaler, Silvia
Martinez-Perez, Cecilia
Marcati, Carmen Regina [UNESP]
Chung, Kuo-Fang
Rosell, Julieta A.
Segovia-Rivas, Ali
Williams, Cameron B.
Petrone-Mendoza, Emilio
Rinaldo, Andrea
Anfodillo, Tommaso
Banavar, Jayanth R.
Maritan, Amos
dc.subject.por.fl_str_mv plant hydraulics
xylem
Pareto optimality
allometry
adaptation
topic plant hydraulics
xylem
Pareto optimality
allometry
adaptation
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 tradeoff 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.
publishDate 2021
dc.date.none.fl_str_mv 2021-06-26T08:03:36Z
2021-06-26T08:03:36Z
2021-06-01
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1073/pnas.2100314118|1of8
Proceedings Of The National Academy Of Sciences Of The United States Of America. Washington: Natl Acad Sciences, v. 118, n. 22, 8 p., 2021.
0027-8424
http://hdl.handle.net/11449/210811
10.1073/pnas.2100314118|1of8
WOS:000659434200001
url http://dx.doi.org/10.1073/pnas.2100314118|1of8
http://hdl.handle.net/11449/210811
identifier_str_mv Proceedings Of The National Academy Of Sciences Of The United States Of America. Washington: Natl Acad Sciences, v. 118, n. 22, 8 p., 2021.
0027-8424
10.1073/pnas.2100314118|1of8
WOS:000659434200001
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Proceedings Of The National Academy Of Sciences Of The United States Of America
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 8
dc.publisher.none.fl_str_mv Natl Acad Sciences
publisher.none.fl_str_mv Natl Acad Sciences
dc.source.none.fl_str_mv Web of Science
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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