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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
Hurtado-Castano, Natalia; Atkins, Elliott; Barnes, Jerry; Boxall, Susanna F; Dever, Louisa V; Kneřová, Jana; Hartwell, James; Cushman, John C; Borland, Anne M
2023 Annals of Botany
doi: 10.1093/aob/mcad017pmid: 36661206
Abstract Background and Aims Crassulacean acid metabolism (CAM) is a specialised type of photosynthesis characterised 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 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 day-time 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. This study tested the hypothesis that the timing of diel starch turnover in CAM guard cells has been re-programmed during evolution to enable nocturnal stomatal opening and day-time closure. Methods Biochemical and genetic characterisation 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, day-time 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 day-time 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 day-time stomatal closure in this CAM species. Crassulacean acid metabolism, Kalanchoë fedtschenkoi, CO2 uptake, stomatal conductance, starch, phosphoglucomutase Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. PDF This content is only available as a PDF. © The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.