Evidence map›Paper›PMID 27261065›Full record

ArticlePlant physiology2016

Alarm Photosynthesis: Calcium Oxalate Crystals as an Internal CO2 Source in Plants.

Georgia Tooulakou, Andreas Giannopoulos, Dimosthenis Nikolopoulos, Panagiota Bresta, Elissavet Dotsika, Malvina G Orkoula, Christos G Kontoyannis, Costas Fasseas, Georgios Liakopoulos, Maria I Klapa and 1 more

Open access · bronzeAbstract read
In one paragraph

Article in Plant physiology, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 34 papers.

0numbers the graph read from it
0cells of the map it votes in
34citing papers in PubMed
21.9field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

34 citing papers in PubMed, 129 citations in OpenAlex.

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  14. Acclimation of the GrapevinePlants (Basel, Switzerland) · 2023
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  16. The CAM lineages of planet Earth.Annals of botany · 2023
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  17. Review
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4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

11 authors at 4 institutions in 2 countries.

Georgia TooulakouLaboratory 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 GiannopoulosLaboratory 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 NikolopoulosLaboratory 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 BrestaLaboratory 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 DotsikaLaboratory 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 OrkoulaLaboratory 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 KontoyannisLaboratory 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.).ORCID 0000-0003-0452-1957
Costas FasseasLaboratory 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 LiakopoulosLaboratory 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.).ORCID 0000-0002-7511-0429
Maria I KlapaLaboratory 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.).ORCID 0000-0002-2047-3185
George KarabourniotisLaboratory 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.
Agricultural University of Athens · GRUniversity of Patras · GRNational Centre of Scientific Research "Demokritos" · GRUniversity of Maryland, College Park · US

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

Abstract

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.

Indexed as

PhotosynthesisAbscisic AcidCalcium OxalateCarbon DioxideCircadian RhythmCrystallizationMetabolomeMetabolomicsPhotosystem II Protein ComplexPlant LeavesPlantsPlant StomataSpectrum Analysis, RamanWaterAbscisic AcidCalcium OxalateCarbon DioxidePhotosystem II Protein ComplexWater

Identifiers

PMID27261065
PMCPMC4972262
OpenAlexW2417097384

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