Pit characters determine drought-induced embolism resistance of leaf xylem across 18 Neotropical tree species

Author:

Levionnois Sébastien12ORCID,Kaack Lucian3ORCID,Heuret Patrick2ORCID,Abel Nina3,Ziegler Camille14ORCID,Coste Sabrina1ORCID,Stahl Clément1ORCID,Jansen Steven3ORCID

Affiliation:

1. UMR EcoFoG, AgroParisTech, CIRAD, CNRS, INRAE, Université des Antilles, Université de Guyane , Kourou 97310, France

2. UMR AMAP, Univ. Montpellier, CIRAD, CNRS, INRAE, IRD , Montpellier 34000, France

3. Institute of Systematic Botany and Ecology, Ulm University , Ulm D-89081, Germany

4. Université de Lorraine, AgroParisTech, INRAE, UMR SILVA , Nancy 54000, France

Abstract

Abstract Embolism spreading in xylem is an important component of plant drought resistance. Since embolism resistance has been shown to be mechanistically linked to pit membrane characters in stem xylem, we speculate that similar mechanisms account for leaf xylem. We conducted transmission electron microscopy to investigate pit membrane characters in leaf xylem across 18 Neotropical tree species. We also conducted gold perfusion and polar lipid detection experiments on three species covering the full range of leaf embolism resistance. We then related these observations to previously published data on embolism resistance of leaf xylem. We also incorporated previously published data on stem embolism resistance and stem xylem pit membranes to investigate the link between vulnerability segmentation (i.e. difference in embolism resistance) and leaf–stem anatomical variation. Maximum pit membrane thickness (Tpm,max) and the pit membrane thickness-to-diameter ratio (Tpm,max/Dpm) were predictive of leaf embolism resistance, especially when vestured pits were taken into account. Variation in Tpm,max/Dpm was the only trait predictive of vulnerability segmentation between leaves and stems. Gold particles of 5- and 10-nm infiltrated pit membranes in three species, while the entry of 50-nm particles was blocked. Moreover, polar lipids were associated with inner conduit walls and pits. Our results suggest that mechanisms related to embolism spreading are determined by Tpm, pore constrictions (i.e. the narrowest bottlenecks along pore pathways), and lipid surfactants, which are largely similar between leaf and stem xylem and between temperate and tropical trees. However, our mechanistic understanding of embolism propagation and the functional relevance of Tpm,max/Dpm remains elusive.

Funder

GFclim project (FEDER

Investissement d’Avenir” grant managed by Agence Nationale de la Recherche (CEBA

CEBA

Deutsche Forschungsgemeinschaft (DFG

German Research Foundation

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Genetics,Physiology

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