Molecular Evolution of Plastid Genomes in Parasitic Flowering Plants

Wicke, Susann; Naumann, Julia

doi:10.1016/bs.abr.2017.11.014

Cited by 113 publications

(172 citation statements)

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“…Its map is represented in Figure 1, in a linear form, for convenience. The protein-coding gene content is quite typical for highly reduced plastid genomes of completely heterotrophic plants (Wicke and Naumann, 2018). The plastid genome of R. phalloides possesses the genes accD, clpP, ycf1, ycf2…”

Section: Resultsmentioning

confidence: 99%

“…The increase in the AT content in the plastid genomes of heterotrophic plants, as well as the increase in their substitution rates, are known and many times discussed phenomena (Bromham et al, 2013;Wicke et al, 2016;Hadariová et al, 2018;Wicke and Naumann, 2018). However, their origin is still unknown.…”

Section: Known Sizes Of Nuclear Genomes Of Plants From Santalales Varmentioning

confidence: 99%

“…Genomic studies of heterotrophic plants are mostly focused on plastid genomes, since 1) most of the plastid genes are related to photosynthesis, and thus changes in the plastid genomes are expected to be more prominent compared to mitochondrial and nuclear genomes, and 2) plastid genomes are smaller than nuclear and mitochondrial ones and usually have higher copy numbers and are thus easier to sequence (Daniell et al, 2016;Gualberto and Newton, 2017;Sakamoto and Takami, 2018). The main feature of the plastid genomes of complete heterotrophs is the loss of genes responsible for photosynthesis and respective shortening of the genomes, from approximately 150 kbp (typical of autotrophic plants) to, in the most extreme known case, 12 kbp (Bellot and Renner, 2015;Wicke and Naumann, 2018). The remaining genes are the ones with functions not related to photosynthesis.…”

Section: Introductionmentioning

confidence: 99%

“…In addition to the expected shortening of the genome, there are some peculiar and still unexplained features in the plastid genomes of heterotrophic plants, namely their increased mutation accumulation rate (Bromham et al, 2013;Wicke and Naumann, 2018) and increased AT content (Wicke and Naumann, 2018). In the most extreme cases, plastid genomes of heterotrophic plants may accumulate mutations approximately 100 times faster than their closest autotrophic relatives (Bellot and Renner, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Rhopalocnemis phalloides has one of the most reduced and mutated plastid genomes known

Schelkunov

Nuraliev

Logacheva

2018

Preprint

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Although most plant species are photosynthetic, several hundred species have lost the ability to photosynthesize and instead obtain nutrients via various types of heterotrophic feeding. Their genomes, especially plastid genomes, markedly differ from the genomes of photosynthetic plants. In this work, we describe the sequenced plastid genome of the heterotrophic plant Rhopalocnemis phalloides, which belongs to the family Balanophoraceae and feeds by parasitizing on other plants. The genome is highly reduced (18 622 base pairs versus approximately 150 kilobase pairs in autotrophic plants) and possesses an outstanding AT content, 86.8%, the highest of all sequenced plant plastid genomes. The gene content of this genome is quite typical of heterotrophic plants, with all of the genes related to photosynthesis having been lost. The remaining genes are notably distorted by a high mutation rate and the aforementioned AT content. The high AT content has led to sequence convergence between some of the remaining genes and their homologues from AT-rich plastid genomes of protists. Overall, the plastid genome of R. phalloides is one of the most unusual plastid genomes known.

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Section: Resultsmentioning

confidence: 99%

Section: Known Sizes Of Nuclear Genomes Of Plants From Santalales Varmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Rhopalocnemis phalloides has one of the most reduced and mutated plastid genomes known

Schelkunov

Nuraliev

Logacheva

2018

Preprint

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“…Interactions between them were repeatedly suggested (46,47); e.g. the loss of ycf1, ycf2 and accD genes from the plastome of grasses (48), as well as their common retention in many plastomes of non-photosynthetic parasites (49) provides room for speculation about functional interaction (46). In addition, Silene, a genus in which biparental chloroplast transmission is described (50), exhibits accelerated evolution of accD (51).…”

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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Phylogenomics and plastome evolution of a Brazilian mycoheterotrophic orchid, Pogoniopsis schenckii

Klimpert

Mayer

Sarzi

et al. 2022

American J of Botany

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Premise Pogoniopsis likely represents an independent photosynthesis loss in orchids. We use phylogenomic data to better identify the phylogenetic placement of this fully mycoheterotrophic taxon, and investigate its molecular evolution. Methods We performed likelihood analysis of plastid and mitochondrial phylogenomic data to localize the position of Pogoniopsis schenckii in orchid phylogeny, and investigated the evolution of its plastid genome. Results All analyses place Pogoniopsis in subfamily Epidendroideae, with strongest support from mitochondrial data, which also place it near tribe Sobralieae with moderately strong support. Extreme rate elevation in Pogoniopsis plastid genes broadly depresses branch support; in contrast, mitochondrial genes are only mildly rate elevated and display very modest and localized reductions in bootstrap support. Despite considerable genome reduction, including loss of photosynthesis genes and multiple translation apparatus genes, gene order in Pogoniopsis plastomes is identical to related autotrophs, apart from moderately shifted inverted repeat (IR) boundaries. All cis‐spliced introns have been lost in retained genes. Two plastid genes (accD, rpl2) show significant strengthening of purifying selection. A retained plastid tRNA gene (trnE‐UUC) of Pogoniopsis lacks an anticodon; we predict that it no longer functions in translation but retains a secondary role in heme biosynthesis. Conclusions Slowly evolving mitochondrial genes clarify the placement of Pogoniopsis in orchid phylogeny, a strong contrast with analysis of rate‐elevated plastome data. We documented the effects of the novel loss of photosynthesis: for example, despite massive gene loss, its plastome is fully colinear with other orchids, and it displays only moderate shifts in selective pressure in retained genes.

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Molecular Evolution of Plastid Genomes in Parasitic Flowering Plants

Cited by 113 publications

References 95 publications

Rhopalocnemis phalloides has one of the most reduced and mutated plastid genomes known

Rhopalocnemis phalloides has one of the most reduced and mutated plastid genomes known

Chloroplast competition is controlled by lipid biosynthesis in evening primroses

Phylogenomics and plastome evolution of a Brazilian mycoheterotrophic orchid, Pogoniopsis schenckii

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