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 »
- 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}
}
https://doi.org/10.1093/aob/mcad017
Works referenced in this record:
A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity
journal, January 2012
- Haider, M. S.; Barnes, J. D.; Cushman, J. C.
- Journal of Experimental Botany, Vol. 63, Issue 5
Rethinking Guard Cell Metabolism
journal, September 2016
- Santelia, Diana; Lawson, Tracy
- Plant Physiology, Vol. 172, Issue 3
Isolation and Characterization of Mutants of Common Ice Plant Deficient in Crassulacean Acid Metabolism
journal, March 2008
- Cushman, John C.; Agarie, Sakae; Albion, Rebecca L.
- Plant Physiology, Vol. 147, Issue 1
Malate. Jack of all trades or master of a few?
journal, May 2009
- Fernie, Alisdair R.; Martinoia, Enrico
- Phytochemistry, Vol. 70, Issue 7
Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO 2 - and ABA-induced stomatal closing
journal, July 2015
- Azoulay-Shemer, Tamar; Palomares, Axxell; Bagheri, Andisheh
- The Plant Journal, Vol. 83, Issue 4
Orchestration of carbohydrate processing for crassulacean acid metabolism
journal, June 2016
- Borland, Anne M.; Guo, Hao-Bo; Yang, Xiaohan
- Current Opinion in Plant Biology, Vol. 31
Stomatal Responses to Light, CO2, and Mesophyll Tissue in Vicia faba and Kalanchoë fedtschenkoi
journal, October 2021
- Santos, Mauro G.; Davey, Phillip A.; Hofmann, Tanja A.
- Frontiers in Plant Science, Vol. 12
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants
journal, September 2019
- Liu, Degao; Chen, Mei; Mendoza, Brian
- Journal of Experimental Botany, Vol. 70, Issue 22
Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour
journal, July 2014
- Lawson, Tracy; Simkin, Andrew J.; Kelly, Gilor
- New Phytologist, Vol. 203, Issue 4
Stomatal Biology of CAM Plants
journal, February 2017
- Males, Jamie; Griffiths, Howard
- Plant Physiology, Vol. 174, Issue 2
Diurnal and Light-Regulated Expression of AtSTP1 in Guard Cells of Arabidopsis
journal, October 2003
- Stadler, Ruth; Büttner, Michael; Ache, Peter
- Plant Physiology, Vol. 133, Issue 2
Emerging model systems for functional genomics analysis of Crassulacean acid metabolism
journal, June 2016
- Hartwell, James; Dever, Louisa V.; Boxall, Susanna F.
- Current Opinion in Plant Biology, Vol. 31
The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2
journal, September 2008
- Lee, Miyoung; Choi, Yongwook; Burla, Bo
- Nature Cell Biology, Vol. 10, Issue 10
Transitory Starch Metabolism in Guard Cells: Unique Features for a Unique Function
journal, March 2017
- Santelia, Diana; Lunn, John E.
- Plant Physiology, Vol. 174, Issue 2
Low-level CAM photosynthesis in a succulent-leaved member of the Urticaceae,
journal, December 2020
- Winter, Klaus; Garcia, Milton; Virgo, Aurelio
- Functional Plant Biology, Vol. 48, Issue 7
Phosphorylation of Phospho enol pyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO 2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi
journal, September 2017
- Boxall, Susanna F.; Dever, Louisa V.; Kneřová, Jana
- The Plant Cell, Vol. 29, Issue 10
Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening
journal, February 2016
- Horrer, Daniel; Flütsch, Sabrina; Pazmino, Diana
- Current Biology, Vol. 26, Issue 3
Peeling back the layers of crassulacean acid metabolism: functional differentiation between Kalanchoë fedtschenkoi epidermis and mesophyll proteomes
journal, April 2020
- Abraham, Paul E.; Hurtado Castano, Natalia; Cowan‐Turner, Daniel
- The Plant Journal, Vol. 103, Issue 2
Kalanchoë PPC1 Is Essential for Crassulacean Acid Metabolism and the Regulation of Core Circadian Clock and Guard Cell Signaling Genes
journal, February 2020
- Boxall, Susanna F.; Kadu, Nirja; Dever, Louisa V.
- The Plant Cell, Vol. 32, Issue 4
GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002
- Karimi, Mansour; Inzé, Dirk; Depicker, Ann
- Trends in Plant Science, Vol. 7, Issue 5, p. 193-195
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth
journal, November 2014
- Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana
- Plant Physiology, Vol. 167, Issue 1
Stomatal responses to CO 2 during a diel Crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata
journal, May 2009
- Von Caemmerer, Susanne; Griffiths, Howard
- Plant, Cell & Environment, Vol. 32, Issue 5
Crassulacean acid metabolism guard cell anion channel activity follows transcript abundance and is suppressed by apoplastic malate
journal, June 2020
- Lefoulon, Cécile; Boxall, Susanna F.; Hartwell, James
- New Phytologist, Vol. 227, Issue 6
Colorimetric Method for Determination of Sugars and Related Substances
journal, March 1956
- DuBois, Michel.; Gilles, K. A.; Hamilton, J. K.
- Analytical Chemistry, Vol. 28, Issue 3, p. 350-356
A Starchless Mutant of Nicotiana sylvestris Containing a Modified Plastid Phosphoglucomutase
journal, November 1988
- Hanson, Kenneth R.; McHale, Neil A.
- Plant Physiology, Vol. 88, Issue 3
The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017
- Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu
- Nature Communications, Vol. 8, Issue 1
Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and Crassulacean acid metabolism (CAM)
journal, March 2008
- Cushman, John C.; Tillett, Richard L.; Wood, Joshua A.
- Journal of Experimental Botany, Vol. 59, Issue 7
Engineering crassulacean acid metabolism to improve water-use efficiency
journal, May 2014
- Borland, Anne M.; Hartwell, James; Weston, David J.
- Trends in Plant Science, Vol. 19, Issue 5
Stomatal Opening Mechanism of CAM Plants
journal, February 2010
- Lee, Joon Sang
- Journal of Plant Biology, Vol. 53, Issue 1
An Endogenous Rhythm in the Rate of Carbon Dioxide Output of Bryophyllum: I. SOME PRELIMINARY EXPERIMENTS
journal, January 1959
- Wilkins, M. B.
- Journal of Experimental Botany, Vol. 10, Issue 3
Starch Metabolism in Arabidopsis
journal, January 2012
- Streb, Sebastian; Zeeman, Samuel C.
- The Arabidopsis Book, Vol. 10
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Understanding trait diversity associated with crassulacean acid metabolism (CAM)
journal, June 2019
- Niechayev, Nicholas A.; Pereira, Paula N.; Cushman, John C.
- Current Opinion in Plant Biology, Vol. 49
Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity
journal, September 1985
- Caspar, Timothy; Huber, Steven C.; Somerville, Chris
- Plant Physiology, Vol. 79, Issue 1
Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis
journal, February 2019
- Lim, Sung Don; Lee, Sojeong; Choi, Won-Gyu
- Frontiers in Plant Science, Vol. 10
Phosphorolytic degradation of leaf starch via plastidic α-glucan phosphorylase leads to optimized plant growth and water use efficiency over the diel phases of Crassulacean acid metabolism
journal, March 2021
- Ceusters, Nathalie; Ceusters, Johan; Hurtado-Castano, Natalia
- Journal of Experimental Botany, Vol. 72, Issue 12