A comparison of stomatal conductance responses to blue and red light between C3 and C4 photosynthetic species in three phylogenetically-controlled experiments

Emmanuel L Bernardo; Cristina Rodrigues Gabriel Sales; Lucía Arce Cubas; Richard L Vath; Johannes Kromdijk

doi:10.3389/fpls.2023.1253976

A comparison of stomatal conductance responses to blue and red light between C3 and C4 photosynthetic species in three phylogenetically-controlled experiments

Front Plant Sci. 2023 Sep 27:14:1253976. doi: 10.3389/fpls.2023.1253976. eCollection 2023.

Authors

Emmanuel L Bernardo^{1

2}, Cristina Rodrigues Gabriel Sales¹, Lucía Arce Cubas¹, Richard L Vath¹, Johannes Kromdijk^{1

3}

Affiliations

¹ Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
² Institute of Crop Science, College of Agriculture and Food Science, University of the Philippines Los Baños, College, Los Baños, Laguna, Philippines.
³ Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, United States.

Abstract

Introduction: C₄ photosynthesis is an adaptation that has independently evolved at least 66 times in angiosperms. C₄ plants, unlike their C₃ ancestral, have a carbon concentrating mechanism which suppresses photorespiration, often resulting in faster photosynthetic rates, higher yields, and enhanced water use efficiency. Moreover, the presence of C₄ photosynthesis greatly alters the relation between CO₂ assimilation and stomatal conductance. Previous papers have suggested that the adjustment involves a decrease in stomatal density. Here, we tested if C₄ species also have differing stomatal responses to environmental cues, to accommodate the modified CO₂ assimilation patterns compared to C₃ species.

Methods: To test this hypothesis, stomatal responses to blue and red-light were analysed in three phylogenetically linked pairs of C3 and C4 species from the Cleomaceae (Gynandropsis and Tarenaya), Flaveria, and Alloteropsis, that use either C3 or C4 photosynthesis.

Results: The results showed strongly decreased stomatal sensitivity to blue light in C₄ dicots, compared to their C₃ counterparts, which exhibited significant blue light responses. In contrast, in C₃ and C₄ subspecies of the monocot A. semialata, the blue light response was observed regardless of photosynthetic type. Further, the quantitative red-light response varied across species, but the presence or absence of a significant stomatal red-light response was not directly associated with differences in photosynthetic pathway. Interestingly, stomatal density and morphology patterns observed across the three comparisons were also not consistent with patterns commonly asserted for C₃ and C₄ species.

Discussion: The strongly diminished blue-light sensitivity of stomatal responses in C₄ species across two of the comparisons suggests a common C₄ feature that may have functional implications. Altogether, the strong prevalence of species-specific effects clearly emphasizes the importance of phylogenetic controls in comparisons between C₃ and C₄ photosynthetic pathways.

Keywords: Alloteropsis; Cleomaceae; Flaveria; blue light; photosynthesis; red light; stomata; stomatal conductance.

Grants and funding

EB was funded by the Department of Science and Technology - Science Education Institute (DOST-SEI) under their Foreigh Graduate Scholarships in Specialized and Priority Fields in Science and Technology. EB also acknowledges further financial support from the University of the Philippines Los Baños, the Department of Plant Sciences, University of Cambridge, Emmanuel College, and the University of Cambridge.