Alarm Photosynthesis: Calcium Oxalate Crystals as an Internal CO2 Source in Plants.
Calcium oxalate crystals are widespread among animals and plants. In land plants, crystals often reach high amounts, up to 80% of dry biomass. They are formed within specific cells, and their accumulation constitutes a normal activity rather than a pathological symptom, as occurs in animals. Despite their ubiquity, our knowledge on the formation and the possible role(s) of these crystals remains limited. We show that the mesophyll crystals of pigweed (Amaranthus hybridus) exhibit diurnal volume changes with a gradual decrease during daytime and a total recovery during the night. Moreover, stable carbon isotope composition indicated that crystals are of nonatmospheric origin. Stomatal closure (under drought conditions or exogenous application of abscisic acid) was accompanied by crystal decomposition and by increased activity of oxalate oxidase that converts oxalate into CO2 Similar results were also observed under drought stress in Dianthus chinensis, Pelargonium peltatum, and Portulacaria afra Moreover, in A. hybridus, despite closed stomata, the leaf metabolic profiles combined with chlorophyll fluorescence measurements indicated active photosynthetic metabolism. In combination, calcium oxalate crystals in leaves can act as a biochemical reservoir that collects nonatmospheric carbon, mainly during the night. During the day, crystal degradation provides subsidiary carbon for photosynthetic assimilation, especially under drought conditions. This new photosynthetic path, with the suggested name "alarm photosynthesis," seems to provide a number of adaptive advantages, such as water economy, limitation of carbon losses to the atmosphere, and a lower risk of photoinhibition, roles that justify its vast presence in plants.
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Georgia
G
Tooulakou
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Andreas
A
Giannopoulos
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Dimosthenis
D
Nikolopoulos
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Panagiota
P
Bresta
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Elissavet
E
Dotsika
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Malvina G
MG
Orkoula
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Christos G
0000-0003-0452-1957
CG
Kontoyannis
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Costas
C
Fasseas
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Georgios
0000-0002-7511-0429
G
Liakopoulos
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.).
Maria I
0000-0002-2047-3185
MI
Klapa
Laboratory of Plant Physiology (G.T., A.G., D.N., P.B., G.L., G.K.) and Laboratory of Electron Microscopy (C.F.), Faculty of Crop Science, Agricultural University of Athens, GR-11855 Athens, Greece; Metabolic Engineering and Systems Biology Laboratory (G.T., M.I.K.), Institute of Chemical Engineering Sciences (C.G.K.), Foundation for Research and Technology-Hellas (FORTH/ICE-HT), GR-26504 Patras, Greece; Stable Isotope Unit, Institute of Material Science, National Centre for Scientific Research "Demokritos", GR-11510 Athens, Greece (E.D.); Department of Pharmacy, University of Patras, GR-26504 Patras, Greece (M.G.O., C.G.K.); and Departments of Chemical and Biomolecular Engineering and Bioengineering, University of Maryland, College Park, Maryland 20742 (M.I.K.) karab@aua.gr.
George
G
Karabourniotis
D000040:Abscisic Acid / Q000494:pharmacology; D002129:Calcium Oxalate / Q000378:metabolism*; D002245:Carbon Dioxide / Q000378:metabolism*; D002940:Circadian Rhythm / Q000187:drug effects; D003460:Crystallization; D055442:Metabolome / Q000187:drug effects; D055432:Metabolomics; D010788:Photosynthesis; D045332:Photosystem II Protein Complex / Q000378:metabolism; D018515:Plant Leaves / Q000187:drug effects / Q000378:metabolism; D054046:Plant Stomata / Q000187:drug effects / Q000502:physiology; D010944:Plants / Q000187:drug effects / Q000378:metabolism*; D013059:Spectrum Analysis, Raman; D014867:Water
D045332:Photosystem II Protein Complex; D014867:Water; D002245:Carbon Dioxide; D002129:Calcium Oxalate; D000040:Abscisic Acid