title: Enhanced Photosynthesis and Growth in atquac1 Knockout Mutants Are Due to Altered Organic Acid Accumulation and an Increase in Both Stomatal and Mesophyll Conductance.
abstract: Stomata control the exchange of CO2 and water vapor in land plants. Thus, whereas a constant supply of CO2 is required to maintain adequate rates of photosynthesis, the accompanying water losses must be tightly regulated to prevent dehydration and undesired metabolic changes. Accordingly, the uptake or release of ions and metabolites from guard cells is necessary to achieve normal stomatal function. The AtQUAC1, an R-type anion channel responsible for the release of malate from guard cells, is essential for efficient stomatal closure. Here, we demonstrate that mutant plants lacking AtQUAC1 accumulated higher levels of malate and fumarate. These mutant plants not only display slower stomatal closure in response to increased CO2 concentration and dark but are also characterized by improved mesophyll conductance. These responses were accompanied by increases in both photosynthesis and respiration rates, without affecting the activity of photosynthetic and respiratory enzymes and the expression of other transporter genes in guard cells, which ultimately led to improved growth. Collectively, our results highlight that the transport of organic acids plays a key role in plant cell metabolism and demonstrate that AtQUAC1 reduce diffusive limitations to photosynthesis, which, at least partially, explain the observed increments in growth under well-watered conditions.
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: David B
authors.identifier: http://orcid.org/0000-0001-9086-730X
authors.initials: DB
authors.lastname: Medeiros
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: Samuel C V
authors.initials: SC
authors.lastname: Martins
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: João Henrique F
authors.identifier: http://orcid.org/0000-0002-1136-6564
authors.initials: JH
authors.lastname: Cavalcanti
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: Danilo M
authors.initials: DM
authors.lastname: Daloso
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: Enrico
authors.initials: E
authors.lastname: Martinoia
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: Adriano
authors.initials: A
authors.lastname: Nunes-Nesi
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: Fábio M
authors.initials: FM
authors.lastname: DaMatta
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.).
authors.forename: Alisdair R
authors.initials: AR
authors.lastname: Fernie
authors.affiliation: Departamento de Biologia Vegetal (D.B.M., S.C.V.M, J.H.F.C., A.N.-N., F.M.D., W.L.A.) and Max-Planck Partner Group at the Departamento de Biologia Vegetal (D.B.M., J.H.F.C., A.N.-N., W.L.A.), Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil;Central Metabolism Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (D.M.D., A.R.F.); andInstitute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland (E.M.) wlaraujo@ufv.br.
authors.forename: Wagner L
authors.initials: WL
authors.lastname: Araújo
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002244:Carbon / Q000378:metabolism; D002245:Carbon Dioxide / Q000378:metabolism; D055864:Droughts; D004798:Enzymes / Q000235:genetics / Q000378:metabolism; D005650:Fumarates / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D055786:Gene Knockout Techniques; D008293:Malates / Q000378:metabolism; D058503:Mesophyll Cells / Q000502:physiology*; D009154:Mutation; D027361:Organic Anion Transporters / Q000235:genetics / Q000378:metabolism*; D010788:Photosynthesis / Q000502:physiology*; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development; D054046:Plant Stomata / Q000235:genetics / Q000502:physiology*
chemical_list: D029681:Arabidopsis Proteins; D004798:Enzymes; D005650:Fumarates; D008293:Malates; D027361:Organic Anion Transporters; C587314:QUAC1 protein, Arabidopsis; D002245:Carbon Dioxide; D002244:Carbon; C030298:malic acid