Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta

McNeal, Joel R.; Kuehl, Jennifer V.; Boore, Jeffrey L.; Pamphilis, Claude W. de

doi:10.1186/1471-2229-7-57

Cited by 171 publications

(236 citation statements)

References 66 publications

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“…The hypothesized turnover ratedependent rate shifts will be attenuated in genes that are required over longer periods, such as the ATP synthase (atp) genes or RuBisCO (rbcL), possibly because they take over or continue to carry out alternative functions (23,24). Therefore, nonphotosynthetic parasites such as M. californica, Orobanche (11), or some Cuscuta species (7,25), which all retain intact genes for the ATP synthase despite the loss of other photosynthesis genes, also have lower base-level evolutionary rates. The eventual deletion of all dispensable regions may reconstitute the compactness of the plastid chromosome with its typically low amounts of nongenic and low-complexity DNA regions (1).…”

Section: Discussionmentioning

confidence: 99%

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Wicke

Müller²,

dePamphilis

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

160

281

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Because novel environmental conditions alter the selection pressure on genes or entire subgenomes, adaptive and nonadaptive changes will leave a measurable signature in the genomes, shaping their molecular evolution. We present herein a model of the trajectory of plastid genome evolution under progressively relaxed functional constraints during the transition from autotrophy to a nonphotosynthetic parasitic lifestyle. We show that relaxed purifying selection in all plastid genes is linked to obligate parasitism, characterized by the parasite's dependence on a host to fulfill its life cycle, rather than the loss of photosynthesis. Evolutionary rates and selection pressure coevolve with macrostructural and microstructural changes, the extent of functional reduction, and the establishment of the obligate parasitic lifestyle. Inferred bursts of gene losses coincide with periods of relaxed selection, which are followed by phases of intensified selection and rate deceleration in the retained functional complexes. Our findings suggest that the transition to obligate parasitism relaxes functional constraints on plastid genes in a stepwise manner. During the functional reduction process, the elevation of evolutionary rates reaches several new rate equilibria, possibly relating to the modified protein turnover rates in heterotrophic plastids.parasitism | relaxed selection | evolutionary rates | plastid genomes | Orobanchaceae L ineages change over time as they adapt to new environments. Novel conditions determine the selection in genes or cellular genomes and shape their functional and structural evolution. A system well suited to study the evolution of genomic traits in the context of altered selective regimes that is also tractable technically (due to its small size and high copy number) is the plastid genome (plastome). The prime function of plastids is photosynthesis, but this essential plant organelle also produces starch, lipids, amino acids, sulfur compounds, and pigments. As a result of the strong selective pressure on plastid gene function, plastid genomes have a conserved gene content (1; but see ref.2) and their genes functioning in photosynthesis (atp, ndh, pet, psa, psb, ccsA, cemA, ycf3/4, rbcL), transcription, transcript maturation or translation (rpo, matK, rpl, rps, infA), and other pathways (accD, clpP, ycf1, and ycf2) evolve at lower evolutionary rates than nuclear genes (3). However, in eukaryotic lineages such as Apicomplexan pathogens and nongreen plants that independently made the transition from an autotrophic to a parasitic way of life, plastomes have experienced convergent reductions and accelerations of evolutionary rates (4). Although there is a general understanding of the association of the nonphotosynthetic lifestyle with plastome degradation and rate acceleration, the precise trajectory of plastome evolution under progressively reduced function along the way from being a full autotroph to an obligate nonphotosynthetic parasite remains unknown.Parasitic plants are an excellent system for stu...

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Section: Discussionmentioning

confidence: 99%

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Wicke

Müller²,

dePamphilis

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

160

281

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“…As they have lost photosynthesis, one would expect all the genes related to this process to be gone as well, and in several cases they are (Wilson et al 1996;de Koning & Keeling 2006). In other cases, however, some of the genes that have been retained are of interest given the absence of photosynthesis, such as ATP synthase genes in Prototheca or rubisco subunits in nonphotosynthetic heterokonts and plants (Wolfe & dePamphilis 1997;Knauf & Hachtel 2002;Sekiguchi et al 2002;McNeal et al 2007;Barrett & Freudenstein 2008;Krause 2008). …”

Section: Plastid Loss and Cryptic Plastidsmentioning

confidence: 99%

The endosymbiotic origin, diversification and fate of plastids

Keeling

2010

Phil. Trans. R. Soc. B

557

471

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Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.

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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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Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta

Cited by 171 publications

References 66 publications

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

The endosymbiotic origin, diversification and fate of plastids

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

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