Nuclear-Cytoplasmic Conflict in Pea (Pisum sativum L.) Is Associated with Nuclear and Plastidic Candidate Genes Encoding Acetyl-CoA Carboxylase Subunits

Богданова, В. С.; Zaytseva, Olga O.; Mglinets, A. V.; Shatskaya, Natalia V.; Kosterin, Oleg E.; Vasiliev, Gennady V.

doi:10.1371/journal.pone.0119835

Cited by 42 publications

(45 citation statements)

References 52 publications

(81 reference statements)

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“…Recent studies have provided support for the possibility of selfish plastid-nuclear interactions within complexes such as the heteromeric ACCase and the CLP complex. In particular, reproductive incompatibilities (including male sterility) between wild and domesticated lines of peas were recently attributed to variation in nuclear-and plastid-encoded components of the heteromeric ACCase (Bogdanova et al 2015). Plastid-nuclear incompatibilities have also been implicated in male sterility in Oenothera (Stubbe and Steiner 1999).…”

Section: Antagonistic Coevolution and Plastid-nuclear Conflictmentioning

confidence: 99%

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: Antagonistic Coevolution and Plastid-nuclear Conflictmentioning

confidence: 99%

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

et al. 2016

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“…Regardless of the initial trigger, this mechanism could explain both previous observations of positive selection on Clp subunits and the high correlation between their evolutionary rates. There has been speculation that such a positive feedback loop in the plastid Clp could be due to antagonistic interactions between the plastid and nuclear genomes (Rockenbach et al ., 2016), and recent studies have implicated other plastid loci in selfish interactions with the nucleus (Bogdanova et al ., 2015; Sobanski et al ., 2018), but direct evidence for this or any other trigger for coevolutionary change is currently lacking.…”

Section: Discussionmentioning

confidence: 99%

Extreme variation in rates of evolution in the plastid Clp protease complex

Williams

Friso

Wijk

et al. 2018

Preprint

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1Eukaryotic cells represent an intricate collaboration between multiple genomes, even down to the 2 level of multisubunit complexes in mitochondria and plastids. One such complex in plants is the 3 caseinolytic protease (Clp), which plays an essential role in plastid protein turnover. The 4 proteolytic core of Clp comprises subunits from one plastid-encoded gene (clpP1) and multiple 5 nuclear genes. The clpP1 gene is highly conserved across most green plants, but it is by far the 6 fastest evolving plastid-encoded gene in some angiosperms. To better understand these extreme 7 and mysterious patterns of divergence, we investigated the history of clpP1 molecular evolution 8 across green plants by extracting sequences from 988 published plastid genomes. We find that 9 clpP1 has undergone remarkably frequent bouts of accelerated sequence evolution and 10 architectural changes (e.g., loss of introns and RNA-editing sites) within seed plants. Although 11 clpP1 is often assumed to be a pseudogene in such cases, multiple lines of evidence suggest that 12 this is rarely the case. We applied comparative native gel electrophoresis of chloroplast protein 13 complexes followed by protein mass spectrometry in two species within the angiosperm genus 14 Silene, which has highly elevated and heterogeneous rates of clpP1 evolution. We confirmed that 15 clpP1 is expressed as a stable protein and forms oligomeric complexes with the nuclear-encoded 16 Clp subunits, even in one of the most divergent Silene species. Additionally, there is a tight 17 correlation between amino-acid substitution rates in clpP1 and the nuclear-encoded Clp subunits 18 across a broad sampling of angiosperms, suggesting ongoing selection on interactions within this 19 complex. 21Rates of sequence evolution vary dramatically across genes and genomes. Understanding 22 the forces that determine such variation is one of the defining goals in the field of molecular 23 evolution. In seed plants, the plastid genome (plastome) generally evolves two-to six-fold more 24 slowly than the nuclear genome (Wolfe et al., 1987; Drouin et al., 2008; Smith and Keeling, 25 2015). However, among angiosperms, there is considerable heterogeneity in the rate of plastome 26 evolution. Many lineages have maintained a slowly-evolving plastome, while others have 27 experienced drastic rate increases (Jansen et al., 2007). For instance, among close relatives 28 within the tribe Sileneae there have been at least three recent and independent increases in 29 plastome evolutionary rate (Erixon and Oxelman, 2008; Sloan, Triant, Forrester, et al., 2014). 30 Similar accelerations have been documented in the Campanulaceae (Haberle et al., 2008; a structural level, plastome gene order has largely been conserved, with most angiosperms 34 retaining the structural organization that was present in the most recent common ancestor of this 35 group (Raubeson and Jansen, 2005). However, the sporadic increases in rates of plastome 36 sequence evolution have often been accompanied by structural ...

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“…In contrast, Campanulastrum, again displaying biparental chloroplast inheritance (9) has lost accD from the chloroplast genome, and its ycf2 is under accelerated evolution (52). In pea, which usually shows uniparental chloroplast inheritance, one strain with biparental chloroplast inheritance exists and biparental transmission is accompanied by chloroplast/nuclear genome incompatibility in the resulting hybrid (53), with repeats in accD implicated as being responsible (54). Analysis of a very similar chloroplast/nuclear genome incompatibility in Oenothera also identifies repeats in accD as causative (55).…”

Section: Discussionmentioning

confidence: 99%

Chloroplast competition is controlled by lipid biosynthesis in evening primroses

Sobanski

Giavalisco

Fischer

et al. 2018

Preprint

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In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primroseOenothera. Repeats in the regulatory region ofaccD(the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate limiting step of lipid biosynthesis), as well as inycf2(a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turn-over rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, since plastid competitiveness can result in uniparental inheritance (through elimination of the “weak” plastid) or biparental inheritance (when two similarly “strong” plastids are transmitted).Significance statementPlastids and mitochondria are usually uniparentally inherited, typically maternally. When the DNA-containing organelles are transmitted to the progeny by both parents, evolutionary theory predicts that the maternal and paternal organelles will compete in the hybrid. As their genomes do not undergo sexual recombination, one organelle will “try” to outcompete the other, thus favoring the evolution and spread of aggressive cytoplasms. The investigations described here in the evening primrose, a model species for biparental plastid transmission, have discovered that chloroplast competition is a metabolic phenotype. It is conferred by rapidly evolving genes that are encoded on the chloroplast genome and control lipid biosynthesis. Due to their high mutation rate these loci can evolve and become fixed in a population very quickly.

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Nuclear-Cytoplasmic Conflict in Pea (Pisum sativum L.) Is Associated with Nuclear and Plastidic Candidate Genes Encoding Acetyl-CoA Carboxylase Subunits

Cited by 42 publications

References 52 publications

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

Extreme variation in rates of evolution in the plastid Clp protease complex

Chloroplast competition is controlled by lipid biosynthesis in evening primroses

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