Localized hypermutation and associated gene losses in legume chloroplast genomes

Magee, Alan M.; Aspinall, Sue; Rice, Danny W.; Cusack, Brian P.; Sémon, Marie; Perry, Antoinette S.; Stefanović, Saša; Milbourne, Dan; Barth, Susanne; Palmer, Jeffrey D.; Gray, John C.; Kavanagh, Tony A.; Wolfe, Kenneth H.

doi:10.1101/gr.111955.110

Cited by 217 publications

(362 citation statements)

References 94 publications

(134 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: 42%

“…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: 42%

Section: Discussionmentioning

confidence: 99%

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

et al. 2016

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“…It is noteworthy in this respect that the ycf4 gene, although otherwise well conserved in the green lineage, has been lost from the chloroplast genome in the legume species Lathyrus odoratus and separately in three other groups of legumes (Magee et al, 2010). A nuclear copy of ycf4 could not be identified in Lathyrus (Magee et al, 2010), making it unlikely that a functional gene copy was transferred to the nuclear genome. Although this conclusion still awaits ultimate confirmation from whole-genome sequencing, it lends support to the idea that Ycf4 function can be replaced by other factor(s) acting in PSI assembly.…”

Section: Discussionmentioning

confidence: 94%

The Plastid Genome-Encoded Ycf4 Protein Functions as a Nonessential Assembly Factor for Photosystem I in Higher Plants

et al. 2012

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Photosystem biogenesis in the thylakoid membrane is a highly complicated process that requires the coordinated assembly of nucleus-encoded and chloroplast-encoded protein subunits as well as the insertion of hundreds of cofactors, such as chromophores (chlorophylls, carotenoids) and iron-sulfur clusters. The molecular details of the assembly process and the identity and functions of the auxiliary factors involved in it are only poorly understood. In this work, we have characterized the chloroplast genome-encoded ycf4 (for hypothetical chloroplast reading frame no. 4) gene, previously shown to encode a protein involved in photosystem I (PSI) biogenesis in the unicellular green alga Chlamydomonas reinhardtii. Using stable transformation of the chloroplast genome, we have generated ycf4 knockout plants in the higher plant tobacco (Nicotiana tabacum). Although these mutants are severely affected in their photosynthetic performance, they are capable of photoautotrophic growth, demonstrating that, different from Chlamydomonas, the ycf4 gene product is not essential for photosynthesis. We further show that ycf4 knockout plants are specifically deficient in PSI accumulation. Unaltered expression of plastid-encoded PSI genes and biochemical analyses suggest a posttranslational action of the Ycf4 protein in the PSI assembly process. With increasing leaf age, the contents of Ycf4 and Y3IP1, another auxiliary factor involved in PSI assembly, decrease strongly, whereas PSI contents remain constant, suggesting that PSI is highly stable and that its biogenesis is restricted to young leaves.

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“…There still exist some chloroplast genes that can be functionally transferred to the nucleus. For example, chloroplast genes such as accD (Magee et al, 2010), infA (Millen et al, 2001), rpl22 (Gantt et al, 1991), and rpl32 (Cusack and Wolfe, 2007;Ueda et al, 2007) were recently functionally transferred from the chloroplast to the nucleus in some angiosperms (for review, see Rousseau-Gueutin et al, 2011). The number of genes that can be functionally transferred might be larger since analyses of the gene content of all plastomes sequenced so far showed that the ndh, psaI, rps16, rpl23, rpl33, or ycf4 genes were lost in some angiosperms (Magee et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Conservation of Plastid Sequences in the Plant Nuclear Genome for Millions of Years Facilitates Endosymbiotic Evolution

2011

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The nuclear genome of eukaryotes contains large amounts of cytoplasmic organelle DNA (nuclear integrants of organelle DNA [norgs]). The recent sequencing of many mitochondrial and chloroplast genomes has enabled investigation of the potential role of norgs in endosymbiotic evolution. In this article, we describe a new polymerase chain reaction-based method that allows the identification and evolutionary study of recent and older norgs in a range of eukaryotes. We tested this method in the genus Nicotiana and obtained sequences from seven nuclear integrants of plastid DNA (nupts) totaling 25 kb in length. These nupts were estimated to have been transferred 0.033 to 5.81 million years ago. The spectrum of mutations present in the potential protein-coding sequences compared with the noncoding sequences of each nupt revealed that nupts evolve in a nuclear-specific manner and are under neutral evolution. Indels were more frequent in noncoding regions than in potential coding sequences of former chloroplastic DNA, most probably due to the presence of a higher number of homopolymeric sequences. Unexpectedly, some potential protein-coding sequences within the nupts still contained intact open reading frames for up to 5.81 million years. These results suggest that chloroplast genes transferred to the nucleus have in some cases several millions of years to acquire nuclear regulatory elements and become functional. The different factors influencing this time frame and the potential role of nupts in endosymbiotic gene transfer are discussed.More than a billion years ago, the ancestors of mitochondria and plastids were free-living eubacteria that were sequentially engulfed by a precursor of the nucleated cell (Timmis et al., 2004). Since these two separate endosymbiotic events, organelle DNA has been continuously transferred and integrated into the nucleus. Insertions of organelle DNA are referred to as numts (nuclear integrants of mitochondrial DNA; Lopez et al., 1994) and nupts (nuclear integrants of plastid DNA; Timmis et al., 2004) or collectively as norgs (nuclear integrants of organelle DNA; Leister, 2005). Transfer of mitochondrial and plastid DNA to the nucleus has been shown to occur at a very high frequency ( Thorsness and Fox, 1990;Huang et al., 2003;Stegemann et al., 2003;Sheppard et al., 2008). Several molecular mechanisms involved in the integration of mitochondrial DNA into the nucleus have been suggested and are likely to be similar for nupts.These include the degradation and lysis of mitochondria, the encapsulation of mitochondrial DNA inside the nucleus, the direct physical association between the mitochondria and nucleus with membrane fusions, or the entry and incorporation of mitochondrial DNA into nuclear chromosomes (for review, see Hazkani-Covo et al., 2010). During evolution, this DNA transfer and integration into the nucleus have resulted in the functional relocation of many organelle genes in the nucleus, leading to a massive reduction in the size of organelle genomes compared with those of their fr...

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Localized hypermutation and associated gene losses in legume chloroplast genomes

Cited by 217 publications

References 94 publications

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

The Plastid Genome-Encoded Ycf4 Protein Functions as a Nonessential Assembly Factor for Photosystem I in Higher Plants

Conservation of Plastid Sequences in the Plant Nuclear Genome for Millions of Years Facilitates Endosymbiotic Evolution

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