Rampant Gene Loss in the Underground Orchid Rhizanthella gardneri Highlights Evolutionary Constraints on Plastid Genomes

Delannoy, Étienne; Fujii, Sota; Francs‐Small, Catherine Colas des; Brundrett, Mark; Small, Ian

doi:10.1093/molbev/msr028

Cited by 236 publications

(273 citation statements)

References 70 publications

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“…The prokaryote-type ACCase is composed of four subunits (Gornicki et al, 1997): the a-carboxyltransferase subunit (accA), the biotin carboxyl carrier (accB), and the biotin carboxylase (accC), which are all nucleus encoded, and the b-carboxyltransferase subunit (accD) that is encoded in the plastome (even in the reduced plastomes of parasitic and nonphotosynthetic plants; Wolfe et al, 1992;Bungard, 2004;Delannoy et al, 2011). From a study of 28 plant families, it was observed that, apart from Poaceae, all flowering plants (including Campanulaceae) contain prokaryotic-like ACCase proteins in their chloroplasts (Konishi and Sasaki, 1994;Konishi et al, 1996;Gornicki et al, 1997).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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(M.A.) Eukaryotic cells originated when an ancestor of the nucleated cell engulfed bacterial endosymbionts that gradually evolved into the mitochondrion and the chloroplast. Soon after these endosymbiotic events, thousands of ancestral prokaryotic genes were functionally transferred from the endosymbionts to the nucleus. This process of functional gene relocation, now rare in eukaryotes, continues in angiosperms. In this article, we show that the chloroplastic acetyl-CoA carboxylase subunit (accD) gene that is present in the plastome of most angiosperms has been functionally relocated to the nucleus in the Campanulaceae. Surprisingly, the nucleus-encoded accD transcript is considerably smaller than the plastidic version, consisting of little more than the carboxylase domain of the plastidic accD gene fused to a coding region encoding a plastid targeting peptide. We verified experimentally the presence of a chloroplastic transit peptide by showing that the product of the nuclear accD fused to green fluorescent protein was imported in the chloroplasts. The nuclear gene regulatory elements that enabled the erstwhile plastidic gene to become functional in the nuclear genome were identified, and the evolution of the intronic and exonic sequences in the nucleus is described. Relocation and truncation of the accD gene is a remarkable example of the processes underpinning endosymbiotic evolution.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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“…In the absence of a plastid genome and plastid trnE in Polytomella spp., the heme pathway could likely only be completed through the import of a nuclear tRNA for Glu into the plastid from the cytosol, because the Polytomella mitochondrial genome encodes only a single tRNA (an elongator tRNA for Met; Smith et al, 2010). Although plastid tRNA import has yet to be documented, it is thought to occur in various parasitic species (Wolfe et al, 1992;Alkatib et al, 2012a), such as the underground orchid Rhizanthella gardneri (Delannoy et al, 2011). Import of cytosolic tRNAs into mitochondria, however, is well-documented (Duchêne et al, 2009) and, in fact, must occur in the mitochondria of Polytomella spp.…”

Section: The Possibility Of Plastid Genome Lossmentioning

confidence: 99%

A Plastid without a Genome: Evidence from the Nonphotosynthetic Green Algal Genus Polytomella

2014

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ORCID ID: 0000-0001-9560-5210 (D.R.S.).Polytomella spp. are free-living, nonphotosynthetic green algae closely related to the model organism Chlamydomonas reinhardtii. Although colorless, Polytomella spp. have a plastid, but it is still unknown whether they harbor a plastid genome. We took a next generation sequencing approach, along with transcriptome sequencing, to search for a plastid genome and an associated gene expression system in Polytomella spp. Illumina sequencing of total DNA from four Polytomella spp. did not produce any recognizable plastid-derived reads but did generate a large number of mitochondrial DNA sequences. Transcriptomic analysis of Polytomella parva uncovered hundreds of putative nuclear-encoded, plastid-targeted proteins, which support the presence of plastid-based metabolic functions, similar to those observed in the plastids of other nonphotosynthetic algae. Conspicuously absent, however, were any plastid-targeted proteins involved in the expression, replication, or repair of plastid DNA. Based on these findings and earlier findings, we argue that the Polytomella genus represents the first wellsupported example, to our knowledge, of a primary plastid-bearing lineage without a plastid genome.

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“…These examples seem to indicate that ycf1, ycf2, and clpP1 are dispensable. However, their retention in the reduced plastid genomes of parasitic plants (dePamphilis and Palmer, 1990;Funk et al, 2007;McNeal et al, 2007;Delannoy et al, 2011;Logacheva et al, 2011) argues that they are indeed essential, with functions not limited to photosynthesis. This appears to conflict with the model (Bryant et al, 2011) that accD alone is required for embryo development in Arabidopsis.…”

Section: Comparative Genomics and The Loss Of Essential Chloroplast Gmentioning

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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Rampant Gene Loss in the Underground Orchid Rhizanthella gardneri Highlights Evolutionary Constraints on Plastid Genomes

Cited by 236 publications

References 70 publications

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

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

A Plastid without a Genome: Evidence from the Nonphotosynthetic Green Algal Genus Polytomella

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

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