Potential Functional Replacement of the Plastidic Acetyl-CoA Carboxylase Subunit (<i>accD</i>) Gene by Recent Transfers to the Nucleus in Some Angiosperm Lineages

Rousseau‐Gueutin, Mathieu; Huang, Xun; Higginson, Emily; Ayliffe, Michael; Day, Anil; Timmis, Jeremy N.

doi:10.1104/pp.113.214528

Cited by 88 publications

(93 citation statements)

References 84 publications

(114 reference statements)

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“…These questions extend to the entire ACCase complex, as we found evidence of gene loss/decay in nuclearencoded S. paradoxa ACCase genes (i.e., the apparent loss of ACCB1 and pseudogenization of ACCA). In at least two angiosperm lineages, the plastid accD gene has been transferred to the nucleus (Magee et al 2010;Rousseau-Gueutin et al 2013). However, we found no evidence of a functional nuclear copy of accD in any Silene species examined.…”

Section: Loss Of Plastid Heteromeric Accasecontrasting

confidence: 55%

“…Furthermore, even in species with typical, slow-evolving plastomes, it is primarily the catalytic C-terminal domain of AccD that is highly conserved, whereas the N-terminal domain, which is plant-specific and has an unknown function, accumulates substantial structural divergence (Greiner et al 2008a). The evolution of accD is further complicated in some angiosperm lineages by functional transfer to the nucleus (Magee et al 2010;Rousseau-Gueutin et al 2013) or by functional replacement with a duplicated and retargeted copy of the homomeric ACCase (Konishi and Sasaki 1994). In contrast, there is no evidence (to our knowledge) of functional transfer of clpP1 to the nucleus in green plants.…”

Section: Discussionmentioning

confidence: 99%

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Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

et al. 2016

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Rates of sequence evolution in plastid genomes are generally low, but numerous angiosperm lineages exhibit accelerated evolutionary rates in similar subsets of plastid genes. These genes include clpP1 and accD, which encode components of the caseinolytic protease (CLP) and acetyl-coA carboxylase (ACCase) complexes, respectively. Whether these extreme and repeated accelerations in rates of plastid genome evolution result from adaptive change in proteins (i.e., positive selection) or simply a loss of functional constraint (i.e., relaxed purifying selection) is a source of ongoing controversy. To address this, we have taken advantage of the multiple independent accelerations that have occurred within the genus Silene (Caryophyllaceae) by examining phylogenetic and population genetic variation in the nuclear genes that encode subunits of the CLP and ACCase complexes. We found that, in species with accelerated plastid genome evolution, the nuclear-encoded subunits in the CLP and ACCase complexes are also evolving rapidly, especially those involved in direct physical interactions with plastid-encoded proteins. A massive excess of nonsynonymous substitutions between species relative to levels of intraspecific polymorphism indicated a history of strong positive selection (particularly in CLP genes). Interestingly, however, some species are likely undergoing loss of the native (heteromeric) plastid ACCase and putative functional replacement by a duplicated cytosolic (homomeric) ACCase. Overall, the patterns of molecular evolution in these plastidnuclear complexes are unusual for anciently conserved enzymes. They instead resemble cases of antagonistic coevolution between pathogens and host immune genes. We discuss a possible role of plastid-nuclear conflict as a novel cause of accelerated evolution.

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Section: Loss Of Plastid Heteromeric Accasecontrasting

confidence: 55%

Section: Discussionmentioning

confidence: 99%

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

et al. 2016

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“…1480 bp for taxa in this study) that has been lost from plastid genomes of some angiosperm families (Rousseau-Gueutin et al 2013) including the two species representing Alismatales (Spirodela polyrhiza and Colocasia esculenta) and the three species included in this study from Liliales (Smilax china, Veratrum patulum, and Fritillaria taipaiensis). In some cases accD and infA have been reported as transferred to the nuclear genome (Millen et al 2001;Rousseau-Gueutin et al 2013). Other coding regions missing from the plastid genome of comparator species included psaJ and ycf1 (Smilax china), rps12, rpl20, and trnH-GUG tRNA (Spirodela polyrhiza), and rps16 (Veratrum patulum and Dioscorea elephantipes).…”

Section: Comparisons Among the Plastid Genomes Of Iris Gatesii And Otmentioning

confidence: 96%

The Complete Plastid Genome Sequence of Iris gatesii (Section Oncocyclus), a Bearded Species from Southeastern Turkey

Wilson¹

2014

aliso

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“…Comparative genomics have shown that all four genes are retained in the plastid genomes of most angiosperms, including chlorophyll-deficient, parasitic species (dePamphilis and Palmer, 1990;Funk et al, 2007;Jansen et al, 2007). Several examples of essential chloroplast genes that relocated to the nucleus have also been described (Magee et al, 2010;Rousseau-Gueutin et al, 2013). The absence of ycf1 and ycf2 in grasses (Jansen et al, 2007) and the replacement of accD with a nuclear gene that targets functional protein back to the chloroplast (Konishi and Sasaki, 1994;Chalupska et al, 2008) remain to be explained.…”

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confidence: 99%

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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Potential Functional Replacement of the Plastidic Acetyl-CoA Carboxylase Subunit (accD) Gene by Recent Transfers to the Nucleus in Some Angiosperm Lineages

Cited by 88 publications

References 84 publications

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

The Complete Plastid Genome Sequence of Iris gatesii (Section Oncocyclus), a Bearded Species from Southeastern Turkey

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

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