Mesophyll airspace unsaturation drives C4 plant success under vapor pressure deficit stress

Journal Publication ResearchOnline@JCU
Márquez, Diego A.;Wong, Suan Chin;Stuart-Williams, Hilary;Cernusak, Lucas A.;Farquhar, Graham D.
Abstract

A fundamental assumption in plant science posits that leaf air spaces remain vapor saturated, leading to the predominant view that stomata alone control leaf water loss. This concept has been pivotal in photosynthesis and water-use efficiency research. However, recent evidence has refuted this longstanding assumption by providing evidence of unsaturation in the leaf air space of C3 plants under relatively mild vapor pressure deficit (VPD) stress. This phenomenon represents a nonstomatal mechanism restricting water loss from the mesophyll. The potential ubiquity and physiological implications of this phenomenon, its driving mechanisms in different plant species and habitats, and its interaction with other ecological adaptations remain to be fully explored. In this context, C4 plants spark particular interest for their importance as crops, bundle sheath cells’ unique anatomical characteristics and specialized functions, and notably higher water-use efficiency relative to C3 plants. Here, we confirm reduced relative humidities in the substomatal cavity of the C4 plants maize, sorghum, and proso millet down to 80% under mild VPD stress. We demonstrate the critical role of nonstomatal control in these plants, indicating that the role of the CO2 concentration mechanism in CO2 management at a high VPD may have been overestimated. Our findings offer a mechanistic reconciliation between discrepancies in CO2 and VPD responses reported in C4 species. They also reveal that nonstomatal control is integral to maintaining an advantageous microclimate of relatively higher CO2 concentrations in the mesophyll air space of C4 plants for carbon fixation, proving vital when these plants face VPD stress.

Journal

Proceedings of the National Academy of Sciences of the United States of America

Publication Name

Proceedings of the National Academy of Sciences of the United States of America

Volume

121

ISBN/ISSN

1091-6490

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Issue

39

Pages Count

9

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Publisher

National Academy of Sciences

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EISSN

N/A

DOI

10.1073/pnas.2402233121