4.8 Article

The Widened Pipe Model of plant hydraulic evolution

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2100314118

Keywords

plant hydraulics; xylem; Pareto optimality; allometry; adaptation

Funding

  1. Cariparo Foundation
  2. Swiss National Science Foundation [CRSII5_186422]
  3. Physics and Astronomy Department of the University of Padova [SUWE\BIRD2020\01]
  4. Istituto Nazionale di Fisica Nucleare, Padova section
  5. University of Padova
  6. Sao Paulo Research Foundation [2018/086098, 2014/14778-6, 2015/14954-1]
  7. Direccion General de Asuntos del Personal Academico, Universidad Nacional Autonoma de Mexico
  8. NSF Integrative Graduate Education and Research Traineeship award [0549505]
  9. Consejo Nacional de Ciencia y Tecnologia [A1-S-26934, 237061]
  10. Programa de Apoyo a Proyectos de Investigacion e Innovacion Tecnologica, Universidad Nacional Autonoma de Mexico [IN210719, IN210220]
  11. University of California Institute for Mexico and the United States [CN-15-1428]
  12. Fondecyt [1160329, 1190900]
  13. NSF [IOS-1010769]
  14. Academia Sinica
  15. Knight Chair from the University of Oregon

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Plants play a crucial role in shaping global water and carbon cycles through the transportation of water via xylem conduits. The Widened Pipe Model (WPM) proposes that xylem conduits should have a specific profile along plant stems, balancing between hydraulic efficiency and carbon cost. The data analysis supports the WPM predictions, highlighting the influence of natural selection on 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 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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