Modified Clp Protease Complex in the ClpP3 Null Mutant and Consequences for Chloroplast Development and Function in Arabidopsis

Kim, Ji-Tae; Olinares, Paul Dominic B.; Oh, Soo-hyun; Ghisaura, Stefania; Poliakov, Anton; Ponnala, Lalit; Wijk, Klaas J. van

doi:10.1104/pp.113.215699

Cited by 55 publications

(86 citation statements)

References 87 publications

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“…Moreover, chloroplast-encoded proteins were clearly not affected in the same manner (e.g., ribosomal proteins levels are barely changed while thylakoid proteins are strongly downregulated), suggesting that despite the strong increase in protein translation factors and tRNA synthases, plastid gene expression was not systematically affected. Direct comparison of the significantly changed plastid proteins with significantly changed chloroplast proteins in CLPPR core and CLPC1 mutants Kim et al, 2009Kim et al, , 2013Zybailov et al, 2009;Nishimura et al, 2013) showed great consistency as is illustrated in Table 1. This suggests that the clpt1-2 clpt2-1 molecular phenotype results mainly from reduced Clp protease capacity (see Discussion).…”

Section: No Differential Effect On Chloroplast-encoded Compared With mentioning

confidence: 81%

Structures, Functions, and Interactions of ClpT1 and ClpT2 in the Clp Protease System of Arabidopsis Chloroplasts

et al. 2015

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Section: No Differential Effect On Chloroplast-encoded Compared With mentioning

confidence: 81%

Structures, Functions, and Interactions of ClpT1 and ClpT2 in the Clp Protease System of Arabidopsis Chloroplasts

et al. 2015

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“…These accessions can therefore be utilized as conditional triple knockouts to study the functions of three intriguing chloroplast proteins and their associated complexes. Based on the known lethality of Arabidopsis mutants defective in ClpP subunits (Kim et al, 2013), the presumed lethality of tobacco (Nicotiana tabacum) cells harboring plastid clpP1 gene disruptions (Kuroda and Maliga, 2003), and the viability of white leaf sectors in the maize (Zea mays) iojap mutant, which lack ClpP1 because they are devoid of chloroplast ribosomes (Walbot and Coe, 1979), we postulate that ClpP1 functions primarily to modulate chloroplast translation. This model predicts that in our system, where chloroplast translation is blocked through exposure to spectinomycin or mutations that disrupt chloroplast ribosomes, loss of ClpP1 activity should not further limit the growth of cells already defective in chloroplast translation.…”

Section: Loss Of Tic20-iv-mediated Chloroplast Protein Import Resultsmentioning

confidence: 99%

Analysis of Arabidopsis Accessions Hypersensitive to a Loss of Chloroplast Translation

2016

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Natural accessions of Arabidopsis (Arabidopsis thaliana) differ in their ability to tolerate a loss of chloroplast translation. These differences can be attributed in part to variation in a duplicated nuclear gene (ACC2) that targets homomeric acetyl-coenzyme A carboxylase (ACCase) to plastids. This functional redundancy allows limited fatty acid biosynthesis to occur in the absence of heteromeric ACCase, which is encoded in part by the plastid genome. In the presence of functional ACC2, tolerant alleles of several nuclear genes, not yet identified, enhance the growth of seedlings and embryos disrupted in chloroplast translation. ACC2 knockout mutants, by contrast, are hypersensitive. Here we describe an expanded search for hypersensitive accessions of Arabidopsis, evaluate whether all of these accessions are defective in ACC2, and characterize genotype-to-phenotype relationships for homomeric ACCase variants identified among 855 accessions with sequenced genomes. Null alleles with ACC2 nonsense mutations, frameshift mutations, small deletions, genomic rearrangements, and defects in RNA splicing are included among the most sensitive accessions examined. By contrast, most missense mutations affecting highly conserved residues failed to eliminate ACC2 function. Several accessions were identified where sensitivity could not be attributed to a defect in either ACC2 or Tic20-IV, the chloroplast membrane channel required for ACC2 uptake. Overall, these results underscore the central role of ACC2 in mediating Arabidopsis response to a loss of chloroplast translation, highlight future applications of this system to analyzing chloroplast protein import, and provide valuable insights into the mutational landscape of an important metabolic enzyme that is highly conserved throughout eukaryotes.

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“…The first approach identified four candidate genes that seemed to explain the importance of chloroplast translation: accD (Kode et al, 2005); ycf1 (Drescher et al, 2000), which functions in protein import (Kikuchi et al, 2013); ycf2 (Drescher et al, 2000), whose function remains unknown; and clpP1 (Kuroda and Maliga, 2003), which encodes part of the ClpP protease that regulates protein degradation (Kim et al, 2013). All four genes are retained in the plastids of most flowering plants, consistent with their proposed essential functions.…”

Section: Comparative Genomics and The Loss Of Essential Chloroplast Gmentioning

confidence: 94%

Natural Variation in Sensitivity to a Loss of Chloroplast Translation in Arabidopsis

2014

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Mutations that eliminate chloroplast translation in Arabidopsis (Arabidopsis thaliana) result in embryo lethality. The stage of embryo arrest, however, can be influenced by genetic background. To identify genes responsible for improved growth in the absence of chloroplast translation, we examined seedling responses of different Arabidopsis accessions on spectinomycin, an inhibitor of chloroplast translation, and crossed the most tolerant accessions with embryo-defective mutants disrupted in chloroplast ribosomal proteins generated in a sensitive background. The results indicate that tolerance is mediated by ACC2, a duplicated nuclear gene that targets homomeric acetyl-coenzyme A carboxylase to plastids, where the multidomain protein can participate in fatty acid biosynthesis. In the presence of functional ACC2, tolerance is enhanced by a second locus that maps to chromosome 5 and heightened by additional genetic modifiers present in the most tolerant accessions. Notably, some of the most sensitive accessions contain nonsense mutations in ACC2, including the "Nossen" line used to generate several of the mutants studied here. Functional ACC2 protein is therefore not required for survival in natural environments, where heteromeric acetyl-coenzyme A carboxylase encoded in part by the chloroplast genome can function instead. This work highlights an interesting example of a tandem gene duplication in Arabidopsis, helps to explain the range of embryo phenotypes found in Arabidopsis mutants disrupted in essential chloroplast functions, addresses the nature of essential proteins encoded by the chloroplast genome, and underscores the value of using natural variation to study the relationship between chloroplast translation, plant metabolism, protein import, and plant development.Embryo development in Arabidopsis (Arabidopsis thaliana) requires the coordinated expression of a large number of essential genes (Muralla et al., 2011). Recessive mutations that disrupt these nuclear genes result in an embryodefective (emb) mutant phenotype (Meinke, 2013). Many EMB genes of Arabidopsis encode chloroplast-localized proteins involved in basic metabolism, protein import, and chloroplast gene expression (Hsu et al., 2010;Bryant et al., 2011;Savage et al., 2013). Functional plastids are therefore required for embryo development in Arabidopsis. Mutations that disrupt photosynthesis alone interfere with embryo and seedling pigmentation, not embryo development. Multiple examples of EMB genes that encode chloroplast-localized aminoacyl-tRNA synthetases, RNA-binding proteins, translation factors, and ribosomal proteins have been described in the literature (Berg et al., 2005;Bryant et al., 2011;Muralla et al., 2011;Romani et al., 2012;Tiller and Bock, 2014). Translation of some chloroplast-encoded mRNAs is therefore essential for seed development. This raises a basic question: which chloroplast genes are required? In this report, we used natural variation and genetic analysis to evaluate the model (Bryant et al., 2011) that a single chloro...

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Modified Clp Protease Complex in the ClpP3 Null Mutant and Consequences for Chloroplast Development and Function in Arabidopsis

Cited by 55 publications

References 87 publications

Structures, Functions, and Interactions of ClpT1 and ClpT2 in the Clp Protease System of Arabidopsis Chloroplasts

Structures, Functions, and Interactions of ClpT1 and ClpT2 in the Clp Protease System of Arabidopsis Chloroplasts

Analysis of Arabidopsis Accessions Hypersensitive to a Loss of Chloroplast Translation

Natural Variation in Sensitivity to a Loss of Chloroplast Translation in Arabidopsis

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