Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements

Hu, Honghong; Rappel, Wouter‐Jan; Occhipinti, Rossana; Ries, Amber; Böhmer, Maik; You, Lei; Xiao, Chuanlei; Engineer, Cawas; Boron, Walter F.; Schroeder, Julian I.

doi:10.1104/pp.15.00646

Cited by 90 publications

(79 citation statements)

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“…1). The longer leaf transcript, bCA4.1, encodes a protein that is targeted to the plasma membrane, as shown by our localization studies and the published work of Fabre et al (2007) and Hu et al, (2010Hu et al, ( , 2015. Here, we also determined that bCA4.2, the shorter transcript, encodes a cytoplasmic CA (Figs.…”

Section: Discussionsupporting

confidence: 49%

“…3; Fabre et al, 2007). bCA4.1-eGFP gave a plasma membrane signal as reported by Fabre et al (2007) and Hu et al (2010Hu et al ( , 2015, but bCA4.2-eGFP was localized to the cytoplasm (Fig. 3).…”

Section: Bca2 and Bca4 Are Expressed In Leavesmentioning

confidence: 54%

“…Previously, only bCA2 (Fett and Coleman, 1994;Fabre et al, 2007) and bCA3 (Fabre et al, 2007) were reported to be in the cytoplasm. The only reports for bCA4 localization indicated that the protein was associated with the plasma membrane (Fabre et al, 2007;Hu et al, 2010Hu et al, , 2015. In addition, we found the gene models presented in TAIR to be incomplete for bCA4 and inaccurate for bCA2.…”

Section: Discussionmentioning

confidence: 90%

“…The six bCA isoforms are found in a number of subcellular locations. bCA1 and bCA5 have been localized to the chloroplast (Fabre et al, 2007;Hu et al, 2015), while bCA2 and bCA3 are found in the cytosol (Fabre et al, 2007). The two other bCAs, bCA4 and bCA6, have been reported to be localized to the plasma membrane (Fabre et al, 2007;Hu et al, 2010Hu et al, , 2015 and the mitochondria (Fabre et al, 2007;Jiang et al, 2014), respectively.…”

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confidence: 97%

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confidence: 99%

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The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO₂

et al. 2016

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Carbonic anhydrases (CAs) are zinc metalloenzymes that interconvert CO 2 and HCO 3 2 . In plants, both a-and b-type CAs are present. We hypothesize that cytoplasmic bCAs are required to modulate inorganic carbon forms needed in leaf cells for carbonrequiring reactions such as photosynthesis and amino acid biosynthesis. In this report, we present evidence that bCA2 and bCA4 are the two most abundant cytoplasmic CAs in Arabidopsis (Arabidopsis thaliana) leaves. Previously, bCA4 was reported to be localized to the plasma membrane, but here, we show that two forms of bCA4 are expressed in a tissue-specific manner and that the two proteins encoded by bCA4 localize to two different regions of the cell. Comparing transfer DNA knockout lines with wild-type plants, there was no reduction in the growth rates of the single mutants, bca2 and bca4. However, the growth rate of the double mutant, bca2bca4, was reduced significantly when grown at 200 mL L 21 CO 2 . The reduction in growth of the double mutant was not linked to a reduction in photosynthetic rate. The amino acid content of leaves from the double mutant showed marked reduction in aspartate when compared with the wild type and the single mutants. This suggests the cytoplasmic CAs play an important but not previously appreciated role in amino acid biosynthesis.Carbonic anhydrases (CAs) are zinc metalloenzymes that catalyze the interconversion of CO 2 and HCO 3 2 . Flowering plants possess members of the aCA, bCA, and gCA families. While all three CA families contain zinc, they clearly have evolved independently (Hewett-Emmett and Tashian, 1996). Most aCAs are monomeric, although there are notable exceptions (Whittington et al., 2001;Hilvo et al., 2008;Suzuki et al., 2010Suzuki et al., , 2011Cuesta-Seijo et al., 2011). The aCA active site contains a single zinc molecule coordinated by three His residues and a water molecule (Liljas et al., 1972). bCAs also contain a zinc active site, although the coordinating molecules are two Cys residues, a His, and a water molecule (Bracey et al., 1994). The active unit of the bCA is a dimer where the active site is located at the interface of the two monomers (Kimber and Pai, 2000). In contrast, gCAs are trimers that have their active site zinc ion situated at the interface of two subunits coordinated by His residues from both subunits (Kisker et al., 1996;Iverson et al., 2000).In Arabidopsis (Arabidopsis thaliana), there are three gCA proteins and two g-like proteins that interact to form an extra structure of complex I of the mitochondrial electron transport chain (Perales et al., 2004;Sunderhaus et al., 2006). Although not active in vitro, gCA has been shown to bind inorganic carbon (Martin et al., 2009), affect complex I levels, plant growth, and gas-exchange rates when deleted (Perales et al., 2004;Soto et al., 2015), and cause plant sterility when ectopically overexpressed ). Arabidopsis has eight aCA genes, but only aCA1, aCA2, and aCA3 appear to be expressed in leaf tissue. aCA1 has been reported to be localized to the c...

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Section: Discussionsupporting

confidence: 49%

Section: Bca2 and Bca4 Are Expressed In Leavesmentioning

confidence: 54%

Section: Discussionmentioning

confidence: 90%

mentioning

confidence: 97%

mentioning

confidence: 99%

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The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO₂

et al. 2016

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Oxygenic Photosynthesis – a Major Driver of Climate Change and Stress Tolerance

Tripathy

2023

Global Climate Change and Plant Stress Management

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GhMPK9‐GhRAF39_1‐GhWRKY40a Regulates the GhERF1b‐ and GhABF2‐Mediated Pathways to Increase Cotton Disease Resistance

Mi,

Li,

Chen

et al. 2024

Advanced Science

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Mitogen‐activated protein kinase (MAPK) cascade is the center of plant signal transduction system that amplify immune signals into cellular responses by phosphorylating diverse substrates. The MAPK cascade consisting of MAPK kinase kinases (MAPKKKs), MAPK kinases (MAPKKs), and MAPKs is well characterized in plants, in which Raf‐like kinases are generally regarded as MAPKKKs. However, it is rarely reported that Raf‐like MAPKKKs function as middle regulators to link MAPK and its downstream transcription factors in plant immunity. Verticillium wilt, caused by the soil‐borne vascular fungus Verticillium dahliae, is a serious disease in many plants, including cotton. The previous studies showed that GhMPK9 (a MAPK) is involved in the response to Verticillium wilt. Here, the Raf‐like kinase GhRAF39_1 is reported as helper regulates the phosphorylation of WRKY transcription factor GhWRKY40a by GhMPK9. The phosphorylated GhWRKY40a can further activate the transcription of GhERF1b to up‐regulate defense‐related genes while inhibit the transcription of GhABF2 to regulate the stomatal opening, thus improving the resistance to Verticillium wilt in cotton. This study reveals a new signaling module of GhMPK9‐GhRAF39_1‐GhWRKY40a to regulate GhERF1b‐ and GhABF2‐mediated defense responses, which triggers plant defense against Verticillium wilt.

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Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements

Cited by 90 publications

References 50 publications

The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO₂

The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO₂

Oxygenic Photosynthesis – a Major Driver of Climate Change and Stress Tolerance

GhMPK9‐GhRAF39_1‐GhWRKY40a Regulates the GhERF1b‐ and GhABF2‐Mediated Pathways to Increase Cotton Disease Resistance

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Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements

Cited by 90 publications

References 50 publications

The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO2

The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO2

Oxygenic Photosynthesis – a Major Driver of Climate Change and Stress Tolerance

GhMPK9‐GhRAF39_1‐GhWRKY40a Regulates the GhERF1b‐ and GhABF2‐Mediated Pathways to Increase Cotton Disease Resistance

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The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO₂

The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO₂