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Title: 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

Abstract

Abstract 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 andmore » 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.« less

Authors:
; ; ; ; ; ; ; ;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
2282173
Alternate Identifier(s):
OSTI ID: 1958637
Grant/Contract Number:  
SC0008834
Resource Type:
Published Article
Journal Name:
Annals of Botany
Additional Journal Information:
Journal Name: Annals of Botany Journal Volume: 132 Journal Issue: 4; Journal ID: ISSN 0305-7364
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Hurtado-Castano, Natalia, Atkins, Elliott, Barnes, Jerry, Boxall, Susanna F., Dever, Louisa V., Kneřová, Jana, Hartwell, James, Cushman, John C., and Borland, Anne M. 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. United Kingdom: N. p., 2023. Web. doi:10.1093/aob/mcad017.
Hurtado-Castano, Natalia, Atkins, Elliott, Barnes, Jerry, Boxall, Susanna F., Dever, Louisa V., Kneřová, Jana, Hartwell, James, Cushman, John C., & Borland, Anne M. 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. United Kingdom. https://doi.org/10.1093/aob/mcad017
Hurtado-Castano, Natalia, Atkins, Elliott, Barnes, Jerry, Boxall, Susanna F., Dever, Louisa V., Kneřová, Jana, Hartwell, James, Cushman, John C., and Borland, Anne M. Fri . "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". United Kingdom. https://doi.org/10.1093/aob/mcad017.
@article{osti_2282173,
title = {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},
author = {Hurtado-Castano, Natalia and Atkins, Elliott and Barnes, Jerry and Boxall, Susanna F. and Dever, Louisa V. and Kneřová, Jana and Hartwell, James and Cushman, John C. and Borland, Anne M.},
abstractNote = {Abstract 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.},
doi = {10.1093/aob/mcad017},
journal = {Annals of Botany},
number = 4,
volume = 132,
place = {United Kingdom},
year = {Fri Jan 20 00:00:00 EST 2023},
month = {Fri Jan 20 00:00:00 EST 2023}
}

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

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