Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast

Villarejo, Arsenio; Burén, Stefan; Larsson, Susanne; Déjardin, Annabelle; Monné, Magnus; Rudhe, Charlotta; Karlsson, Jan; Jansson, Stefan; Lerouge, Patrice; Rolland, Norbert; Heijne, Gunnar von; Grebe, Markus; Bako, L.; Samuelsson, Göran

doi:10.1038/ncb1330

Cited by 314 publications

(264 citation statements)

References 36 publications

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“…These proteins appear to use a targeting mechanism that involves the ER/secretory pathway. Carbonic anhydrase 1 (CAH1) is one of the very few higher plant proteins also known to target chloroplast through the endomembrane system 49 . However, CAH1 localizes to the stroma indicating its targeting mechanism must be different from AZI1, at least in part.…”

Section: Resultsmentioning

confidence: 99%

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

et al. 2015

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Priming is a major mechanism behind the immunological 'memory' observed during two key plant systemic defences: systemic acquired resistance (SAR) and induced systemic resistance (ISR). Lipid-derived azelaic acid (AZA) is a mobile priming signal. Here, we show that the lipid transfer protein (LTP)-like AZI1 and its closest paralog EARLI1 are necessary for SAR, ISR and the systemic movement and uptake of AZA in Arabidopsis. Imaging and fractionation studies indicate that AZI1 and EARLI1 localize to expected places for lipid exchange/movement to occur. These are the ER/plasmodesmata, chloroplast outer envelopes and membrane contact sites between them. Furthermore, these LTP-like proteins form complexes and act at the site of SAR establishment. The plastid targeting of AZI1 and AZI1 paralogs occurs through a mechanism that may enable/facilitate their roles in signal mobilization.

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Section: Resultsmentioning

confidence: 99%

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

et al. 2015

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“…In addition, Hu et al (2010) presented evidence showing high expression of bCA2 and bCA4 in mesophyll cells, whereas bCA3 had very low expression in mesophyll cells, while Wang et al (2014) reported very low bCA3 expression in leaves with promoter::GUS studies. Since the other CAs that show significant expression are either in the chloroplast (Fett and Coleman, 1994;Villarejo et al, 2005;Fabre et al, 2007;Burén et al, 2011;Hu et al, 2015) or mitochondria (Fabre et al, 2007;Jiang et al, 2014), we conclude that bCA2 and bCA4 are the most abundant CA isoforms in the cytoplasm. This contention is supported by leaf RNAseq data (Table I), GUS staining (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…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 chloroplast in leaf tissue (Villarejo et al, 2005;Burén et al, 2011). The expression of aCA2 and aCA3 is quite low but higher than that of aCA4 to aCA8.…”

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confidence: 99%

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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“…Additionally, there is evidence that some proteins can also traffic to the chloroplast from the Golgi (Villarejo et al, 2005;Kitajima et al, 2009) or ER (J.K.C. Rose and S.-J.…”

Section: How Do Proteins Reach the Plant Cell Wall?mentioning

confidence: 99%

Straying off the Highway: Trafficking of Secreted Plant Proteins and Complexity in the Plant Cell Wall Proteome

2010

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From simply skimming through the abstract lists of more or less any collection of both basic and applied plant-related journals, it is immediately apparent that the plant cell wall represents a nexus of many fields of research: growth and development, plant-pathogen interactions, abiotic stress, self-and interorganismal recognition, signaling systems, numerous primary and specialized metabolic processes, biomaterials and bioproducts, and many others. That said, and to deal with an issue of semantics, while the term cell wall can refer specifically to the structural matrix that surrounds all plant cells, for the purposes of this Update it is used more broadly, also to include the apoplast, or extracellular environment. Given its multifunctional nature then, it is not surprising that the apoplast houses a dynamic and complex proteome, and the compendium of cell wall proteins continues to grow as researchers from disparate disciplines discover new roles for extracellular proteins. In addition, however, as cell wall proteomics projects develop and the subcellular localizations of an ever-growing list of plant proteins are determined, a number of surprises have been thrown up, both in terms of the identity of secreted proteins and the trafficking pathways that they follow. The purpose of this Update is to give some examples of previously unsuspected aspects of plant cell wall protein trafficking that are challenging longheld assumptions, rather than to provide an exhaustive review, and to highlight some questions that can be categorized into the "who, how, where, and when" of the cell wall proteome.

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Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast

Cited by 314 publications

References 36 publications

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

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

Straying off the Highway: Trafficking of Secreted Plant Proteins and Complexity in the Plant Cell Wall Proteome

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Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast

Cited by 314 publications

References 36 publications

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

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

Straying off the Highway: Trafficking of Secreted Plant Proteins and Complexity in the Plant Cell Wall Proteome

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