Closing Plant Stomata Requires a Homolog of an Aluminum-Activated Malate Transporter

Plant stomata limit both carbon dioxide uptake and water loss; hence, stomatal aperture is carefully set as the environment fluctuates. Aperture area is known to be regulated in part by ion transport, but few of the transporters have been characterized. Here we report that AtALMT12 (At4g17970), a homolog of the aluminum-activated malate transporter (ALMT) of wheat, is expressed in guard cells of Arabidopsis thaliana. Loss-of-function mutations in AtALMT12 impair stomatal closure induced by ABA, calcium and darkness, but do not abolish either the rapidly activated or the slowly activated anion currents previously identified as being important for stomatal closure. Expressed in Xenopus oocytes, AtALMT12 facilitates chloride and nitrate currents, but not those of organic solutes. Therefore, we conclude that AtALMT12 is a novel class of anion transporter involved in stomatal closure.

• Publication year

  2010

• Venue

  Plant and Cell Physiology

• Publication date

  2010-02-11

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1093/pcp/pcq016PMID 20154005PMCID 2835873
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2009influential reference
• Novel Properties of the Wheat Aluminum Tolerance Organic Acid Transporter (TaALMT1) Revealed by Electrophysiological Characterization in Xenopus Oocytes: Functional and Structural Implications1[OA]

  2008cited by this paper
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  2008influential reference
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  2007cited by this paper
• Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation.

  2007cited by this paper
• The roles of organic anion permeases in aluminium resistance and mineral nutrition

  2007cited by this paper
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• Elaboration of a novel technique for purification of plasma membranes from Xenopus laevis oocytes.

  2007cited by this paper
• Abscisic acid triggers the endocytosis of the arabidopsis KAT1 K+ channel and its recycling to the plasma membrane.

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  2007cited by this paper
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  2007cited by this paper
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  2007cited by this paper
• Alternative splicing of pre-messenger RNAs in plants in the genomic era.

  2007cited by this paper
• Protein Aggregates are Transported to Vacuoles by Macroautophagic Mechanism in Nutrient-Starved Plant Cells

  2006cited by this paper
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  2006cited by this paper
• CDPKs CPK6 and CPK3 Function in ABA Regulation of Guard Cell S-Type Anion- and Ca2+- Permeable Channels and Stomatal Closure

  2006influential reference
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  2006cited by this paper
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  2006cited by this paper
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  2005cited by this paper
• Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability.

  2005cited by this paper
• A wheat gene encoding an aluminum-activated malate transporter.

  2004influential reference
• How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency.

  2004cited by this paper
• The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration

  2003cited by this paper
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  2003cited by this paper
• Arabidopsis : a laboratory manual

  2002cited by this paper
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  2001cited by this paper
• Aluminium tolerance in plants and the complexing role of organic acids.

  2001cited by this paper
• The sfr6 Mutation in Arabidopsis Suppresses Low-Temperature Induction of Genes Dependent on the CRT/DRE Sequence Motif

  1999influential reference
• Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.

  1998cited by this paper
• Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants.

  1997influential reference
• Engineered GFP as a vital reporter in plants.

  1996cited by this paper
• Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events.

  1995cited by this paper
• Calculation and control of free divalent cations in solutions used for membrane fusion studies.

  1993cited by this paper
• Two types of anion channel currents in guard cells with distinct voltage regulation.

  1992cited by this paper
• Appearance of Water Channels in Xenopus Oocytes Expressing Red Cell CHIP28 Protein

  1992cited by this paper
• Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells.

  1990cited by this paper
• Construction and Expression in Tobacco of a β-Glucuronidase (GUS) Reporter Gene Containing an Intron Within the Coding Sequence

  1990cited by this paper
• Voltage-dependent anion channels in the plasma membrane of guard cells

  1989cited by this paper
• The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA

  1986cited by this paper
• High efficiency transformation of cultured tobacco cells.

  1985cited by this paper

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  2025cites this paper
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  2018cites this paper
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  2017cites this paper
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  2017cites this paper
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