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.

doi:10.1093/aob/mcad017

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

Journal Article · Fri Jan 20 00:00:00 EST 2023 · Annals of Botany

DOI:https://doi.org/10.1093/aob/mcad017· OSTI ID:2282173

Hurtado-Castano, Natalia; Atkins, Elliott; Barnes, Jerry; Boxall, Susanna F.; Dever, Louisa V.; Kneřová, Jana; Hartwell, James; Cushman, John C.; Borland, Anne M.

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.

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Research Organization:: University of Nevada, Reno, NV (United States)

Sponsoring Organization:: Biotechnology and Biological Sciences Research Council (BBSRC); USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0008834

OSTI ID:: 2282173

Alternate ID(s):: OSTI ID: 2471985
OSTI ID: 1958637

Journal Information:: Annals of Botany, Journal Name: Annals of Botany Journal Issue: 4 Vol. 132; ISSN 0305-7364

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (37)

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Coordination Between Photosynthesis and Stomatal Behavior Lawson, Tracy; Terashima, Ichiro; Fujita, Takashi The Leaf: A Platform for Performing Photosynthesis https://doi.org/10.1007/978-3-319-93594-2_6	book	January 2018
Stomatal Opening Mechanism of CAM Plants Lee, Joon Sang Journal of Plant Biology, Vol. 53, Issue 1 https://doi.org/10.1007/s12374-010-9097-8	journal	February 2010
GATEWAY™ vectors for Agrobacterium-mediated plant transformation Karimi, Mansour; Inzé, Dirk; Depicker, Ann Trends in Plant Science, Vol. 7, Issue 5, p. 193-195 https://doi.org/10.1016/S1360-1385(02)02251-3	journal	May 2002
Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening Horrer, Daniel; Flütsch, Sabrina; Pazmino, Diana Current Biology, Vol. 26, Issue 3 https://doi.org/10.1016/j.cub.2015.12.036	journal	February 2016
Emerging model systems for functional genomics analysis of Crassulacean acid metabolism Hartwell, James; Dever, Louisa V.; Boxall, Susanna F. Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.03.019	journal	June 2016
Orchestration of carbohydrate processing for crassulacean acid metabolism Borland, Anne M.; Guo, Hao-Bo; Yang, Xiaohan Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.04.001	journal	June 2016
Understanding trait diversity associated with crassulacean acid metabolism (CAM) Niechayev, Nicholas A.; Pereira, Paula N.; Cushman, John C. Current Opinion in Plant Biology, Vol. 49 https://doi.org/10.1016/j.pbi.2019.06.004	journal	June 2019
Malate. Jack of all trades or master of a few? Fernie, Alisdair R.; Martinoia, Enrico Phytochemistry, Vol. 70, Issue 7 https://doi.org/10.1016/j.phytochem.2009.04.023	journal	May 2009
Engineering crassulacean acid metabolism to improve water-use efficiency Borland, Anne M.; Hartwell, James; Weston, David J. Trends in Plant Science, Vol. 19, Issue 5 https://doi.org/10.1016/j.tplants.2014.01.006	journal	May 2014
Colorimetric Method for Determination of Sugars and Related Substances DuBois, Michel.; Gilles, K. A.; Hamilton, J. K. Analytical Chemistry, Vol. 28, Issue 3, p. 350-356 https://doi.org/10.1021/ac60111a017	journal	March 1956
The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2 Lee, Miyoung; Choi, Yongwook; Burla, Bo Nature Cell Biology, Vol. 10, Issue 10 https://doi.org/10.1038/ncb1782	journal	September 2008
The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01491-7	journal	December 2017
Low-level CAM photosynthesis in a succulent-leaved member of the Urticaceae, Winter, Klaus; Garcia, Milton; Virgo, Aurelio Functional Plant Biology, Vol. 48, Issue 7 https://doi.org/10.1071/FP20151	journal	December 2020
An Endogenous Rhythm in the Rate of Carbon Dioxide Output of Bryophyllum: I. SOME PRELIMINARY EXPERIMENTS Wilkins, M. B. Journal of Experimental Botany, Vol. 10, Issue 3 https://doi.org/10.1093/jxb/10.3.377	journal	January 1959
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 Ceusters, Nathalie; Ceusters, Johan; Hurtado-Castano, Natalia Journal of Experimental Botany, Vol. 72, Issue 12 https://doi.org/10.1093/jxb/erab132	journal	March 2021
Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and Crassulacean acid metabolism (CAM) Cushman, John C.; Tillett, Richard L.; Wood, Joshua A. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/ern008	journal	March 2008
A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity Haider, M. S.; Barnes, J. D.; Cushman, J. C. Journal of Experimental Botany, Vol. 63, Issue 5 https://doi.org/10.1093/jxb/err412	journal	January 2012
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants Liu, Degao; Chen, Mei; Mendoza, Brian Journal of Experimental Botany, Vol. 70, Issue 22 https://doi.org/10.1093/jxb/erz415	journal	September 2019
Diurnal and Light-Regulated Expression of AtSTP1 in Guard Cells of Arabidopsis Stadler, Ruth; Büttner, Michael; Ache, Peter Plant Physiology, Vol. 133, Issue 2 https://doi.org/10.1104/pp.103.024240	journal	October 2003
Isolation and Characterization of Mutants of Common Ice Plant Deficient in Crassulacean Acid Metabolism Cushman, John C.; Agarie, Sakae; Albion, Rebecca L. Plant Physiology, Vol. 147, Issue 1 https://doi.org/10.1104/pp.108.116889	journal	March 2008
Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana Plant Physiology, Vol. 167, Issue 1 https://doi.org/10.1104/pp.114.251827	journal	November 2014
Rethinking Guard Cell Metabolism Santelia, Diana; Lawson, Tracy Plant Physiology, Vol. 172, Issue 3 https://doi.org/10.1104/pp.16.00767	journal	September 2016
Stomatal Biology of CAM Plants Males, Jamie; Griffiths, Howard Plant Physiology, Vol. 174, Issue 2 https://doi.org/10.1104/pp.17.00114	journal	February 2017
Transitory Starch Metabolism in Guard Cells: Unique Features for a Unique Function Santelia, Diana; Lunn, John E. Plant Physiology, Vol. 174, Issue 2 https://doi.org/10.1104/pp.17.00211	journal	March 2017
Alterations in Growth, Photosynthesis, and Respiration in a Starchless Mutant of Arabidopsis thaliana (L.) Deficient in Chloroplast Phosphoglucomutase Activity Caspar, Timothy; Huber, Steven C.; Somerville, Chris Plant Physiology, Vol. 79, Issue 1 https://doi.org/10.1104/pp.79.1.11	journal	September 1985
A Starchless Mutant of Nicotiana sylvestris Containing a Modified Plastid Phosphoglucomutase Hanson, Kenneth R.; McHale, Neil A. Plant Physiology, Vol. 88, Issue 3 https://doi.org/10.1104/pp.88.3.838	journal	November 1988
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 Boxall, Susanna F.; Dever, Louisa V.; Kneřová, Jana The Plant Cell, Vol. 29, Issue 10 https://doi.org/10.1105/tpc.17.00301	journal	September 2017
Kalanchoë PPC1 Is Essential for Crassulacean Acid Metabolism and the Regulation of Core Circadian Clock and Guard Cell Signaling Genes Boxall, Susanna F.; Kadu, Nirja; Dever, Louisa V. The Plant Cell, Vol. 32, Issue 4 https://doi.org/10.1105/tpc.19.00481	journal	February 2020
Stomatal responses to CO ₂ during a diel Crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata Von Caemmerer, Susanne; Griffiths, Howard Plant, Cell & Environment, Vol. 32, Issue 5 https://doi.org/10.1111/j.1365-3040.2009.01951.x	journal	May 2009
Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour Lawson, Tracy; Simkin, Andrew J.; Kelly, Gilor New Phytologist, Vol. 203, Issue 4 https://doi.org/10.1111/nph.12945	journal	July 2014
Crassulacean acid metabolism guard cell anion channel activity follows transcript abundance and is suppressed by apoplastic malate Lefoulon, Cécile; Boxall, Susanna F.; Hartwell, James New Phytologist, Vol. 227, Issue 6 https://doi.org/10.1111/nph.16640	journal	June 2020
Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO ₂ - and ABA-induced stomatal closing Azoulay-Shemer, Tamar; Palomares, Axxell; Bagheri, Andisheh The Plant Journal, Vol. 83, Issue 4 https://doi.org/10.1111/tpj.12916	journal	July 2015
Peeling back the layers of crassulacean acid metabolism: functional differentiation between Kalanchoë fedtschenkoi epidermis and mesophyll proteomes Abraham, Paul E.; Hurtado Castano, Natalia; Cowan‐Turner, Daniel The Plant Journal, Vol. 103, Issue 2 https://doi.org/10.1111/tpj.14757	journal	April 2020
Starch Metabolism in Arabidopsis Streb, Sebastian; Zeeman, Samuel C. The Arabidopsis Book, Vol. 10 https://doi.org/10.1199/tab.0160	journal	January 2012
Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis Lim, Sung Don; Lee, Sojeong; Choi, Won-Gyu Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00101	journal	February 2019
Stomatal Responses to Light, CO2, and Mesophyll Tissue in Vicia faba and Kalanchoë fedtschenkoi Santos, Mauro G.; Davey, Phillip A.; Hofmann, Tanja A. Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.740534	journal	October 2021

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59 BASIC BIOLOGICAL SCIENCES
CO2 uptake
Crassulacean acid metabolism
Kalanchoë fedtschenkoi
Plant Sciences
phosphoglucomutase
starch
stomatal conductance

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

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