Angiosperms follow a convex trade-off to optimize hydraulic safety and efficiency.

Luciano Pereira, Lucian Kaack, Xinyi Guan, Luciano de Melo Silva, Marcela T Miranda, Gabriel S Pires, Rafael V Ribeiro, H Jochen Schenk, Steven Jansen

Journal: The New phytologist 2023;240(5):1788-1801

PMID: 37691289

Abstract

Intervessel pits are considered to function as valves that avoid embolism spreading and optimize efficient transport of xylem sap across neighbouring vessels. Hydraulic transport between vessels would therefore follow a safety-efficiency trade-off, which is directly related to the total intervessel pit area (A ), inversely related to the pit membrane thickness (T ) and driven by a pressure difference. To test this hypothesis, we modelled the relative transport rate of gas (k ) and water (Q) at the intervessel pit level for 23 angiosperm species and correlated these parameters with the water potential at which 50% of embolism occurs (Ψ ). We also measured k for 10 species using pneumatic measurements. The pressure difference across adjacent vessels and estimated values of k and Q were related to Ψ , following a convex safety-efficiency trade-off based on modelled and experimental data. Minor changes in T and A exponentially affected the pressure difference and flow, respectively. Our results provide clear evidence that a xylem safety-efficiency trade-off is not linear, but convex due to flow across intervessel pit membranes, which represent mesoporous media within microporous conduits. Moreover, the convex nature of long-distance xylem transport may contribute to an adjustable fluid balance of plants, depending on environmental conditions.

© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.

Address: Institute of Botany, Ulm University, 89081, Ulm, Albert-Einstein-Allee 11, Germany.; Botanical Garden of Ulm University, 89081, Ulm, Hans-Krebs-Weg, Germany.; Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, 530004, Guangxi, Nanning, China.; Laboratory of Plant Physiology 'Coaracy M. Franco', Center R&D in Ecophysiology and Biophysics, Agronomic Institute (IAC), PO Box 28, Campinas, 13012-970, SP, Brazil.; Department of Plant Biology, Laboratory of Crop Physiology, Institute of Biology, University of Campinas (UNICAMP), 13083-970, SP, Campinas, PO Box 6109, Brazil.; Department of Biological Science, California State University Fullerton, 800 N. State College Blvd, Fullerton, 92831-3599, CA, USA.
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