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The starch-deficient plastidic PHOSPHOGLUCOMUTASE mutant of the constitutive crassulacean acid metabolism (CAM) species Kalanchoë fedtschenkoi impacts diel regulation and timing of stomatal CO2 responsiveness

Lookup NU author(s): Natalia Hurtado Castaño, Emeritus Professor Jerry Barnes, Emerita Professor Anne Borland

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© The Author(s) 2023.• Background and Aims Crassulacean acid metabolism (CAM) is a specialized type of photosynthesis characterized by a diel pattern of stomatal opening at night and closure during the day, which increases water-use efficiency. Starch degradation is a key regulator of CAM, providing phosphoenolpyruvate as a substrate in the mesophyll for nocturnal assimilation of CO2. Growing recognition of a key role for starch degradation in C3 photosynthesis guard cells for mediating daytime stomatal opening presents the possibility that starch degradation might also impact CAM by regulating the provision of energy and osmolytes to increase guard cell turgor and drive stomatal opening at night. In this study, we tested the hypothesis that the timing of diel starch turnover in CAM guard cells has been reprogrammed during evolution to enable nocturnal stomatal opening and daytime closure. • Methods Biochemical and genetic characterization of wild-type and starch-deficient RNAi lines of Kalanchoë fedtschenkoi with reduced activity of plastidic phosphoglucomutase (PGM) constituted a preliminary approach for the understanding of starch metabolism and its implications for stomatal regulation in CAM plants. • Key Results Starch deficiency reduced nocturnal net CO2 uptake but had negligible impact on nocturnal stomatal opening. In contrast, daytime stomatal closure was reduced in magnitude and duration in the starch-deficient rPGM RNAi lines, and their stomata were unable to remain closed in response to elevated concentrations of atmospheric CO2 administered during the day. Curtailed daytime stomatal closure was linked to higher soluble sugar contents in the epidermis and mesophyll. • Conclusions Nocturnal stomatal opening is not reliant upon starch degradation, but starch biosynthesis is an important sink for carbohydrates, ensuring daytime stomatal closure in this CAM species.


Publication metadata

Author(s): Hurtado-Castano N, Atkins E, Barnes J, Boxall SF, Dever LV, Knerova J, Hartwell J, Cushman JC, Borland AM

Publication type: Article

Publication status: Published

Journal: Annals of Botany

Year: 2023

Volume: 132

Issue: 4

Pages: 881-894

Print publication date: 20/09/2023

Online publication date: 20/01/2023

Acceptance date: 19/01/2023

Date deposited: 05/02/2024

ISSN (print): 0305-7364

ISSN (electronic): 1095-8290

Publisher: Oxford University Press

URL: https://doi.org/10.1093/aob/mcad017

DOI: 10.1093/aob/mcad017

PubMed id: 36661206


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Funding

Funder referenceFunder name
Biotechnology and Biological Sciences Research Council
BB/F009313/1
Colombian Ministry of Science, Technology and Innovation (Colciencias)
DE-SC0008834
U.S. Department of Energy Office of Science, Genomic Science Program

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