Complete Plastid Genome of the Recent Holoparasite Lathraea squamaria Reveals Earliest Stages of Plastome Reduction in Orobanchaceae.

Tahir H Samigullin,Maria D Logacheva,Aleksey A Penin,Carmen M Vallejo-Roman

doi:10.1371/journal.pone.0150718

Tahir H Samigullin, Maria D Logacheva + Show 2 more

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https://doi.org/10.1371/journal.pone.0150718

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Abstract

Plants from the family Orobanchaceae are widely used as a model to study different aspects of parasitic lifestyle including host–parasite interactions and physiological and genomic adaptations. Among the latter, the most prominent are those that occurred due to the loss of photosynthesis; they include the reduction of the photosynthesis-related gene set in both nuclear and plastid genomes. In Orobanchaceae, the transition to non-photosynthetic lifestyle occurred several times independently, but only one lineage has been in the focus of evolutionary studies. These studies included analysis of plastid genomes and transcriptomes and allowed the inference of patterns and mechanisms of genome reduction that are thought to be general for parasitic plants. Here we report the plastid genome of Lathraea squamaria, a holoparasitic plant from Orobanchaceae, clade Rhinantheae. We found that in this plant the degree of plastome reduction is the least among non-photosynthetic plants. Like other parasites, Lathraea possess a plastome with elevated absolute rate of nucleotide substitution. The only gene lost is petL, all other genes typical for the plastid genome are present, but some of them–those encoding photosystem components (22 genes), cytochrome b6/f complex proteins (4 genes), plastid-encoded RNA polymerase subunits (2 genes), ribosomal proteins (2 genes), ccsA and cemA–are pseudogenized. Genes for cytochrome b6/f complex and photosystems I and II that do not carry nonsense or frameshift mutations have an increased ratio of non-synonymous to synonymous substitution rates, indicating the relaxation of purifying selection. Our divergence time estimates showed that transition to holoparasitism in Lathraea lineage occurred relatively recently, whereas the holoparasitic lineage Orobancheae is about two times older.

Highlights

Photosynthesis has been lost independently numerous times in flowering plant lineages during the transition to a parasitic lifestyle
Faster rate of plastome nucleotide substitutions was reported in another group of heterotrophic plants, mycoheterotrophs [16, 17], and in some photosynthetic plants; in this latter case it is usually correlated with highly rearranged plastid genome [19, 20]
The complete plastid genome of L. squamaria is a circular molecule 150,504 bp in length and possesses a typical architecture with a large single-copy (LSC) region of 81,981 bp separated from the 16,061 bp small single-copy (SSC) region by two inverted repeats (IRs), each of 26,231 bp

Summary

Introduction

Photosynthesis has been lost independently numerous times in flowering plant lineages during the transition to a parasitic lifestyle. 2047 species of 89 genera [2] and includes both a single autotrophic lineage, the genus Lindenbergia Lehm., and all types of parasitism: facultative, obligate hemiparasites, and holoparasites (plants that completely lack photosynthetic activity) [3]. There are sixteen Orobanchaceae parasitic species for which complete sequences of the plastid genome are available, including Epifagus virginiana (L.) W.P.C.Barton, the first parasitic plant with a fully sequenced plastome [8], the hemiparasite Schwalbea americana L., and holoparasites Boulardia latisquama F.W.Schultz, Cistanche phelypaea Cout., Conopholis americana (L.) Wallr., Myzorrhiza californica Faster rate of plastome nucleotide substitutions was reported in another group of heterotrophic plants, mycoheterotrophs [16, 17] (but see [18]), and in some photosynthetic plants; in this latter case it is usually correlated with highly rearranged plastid genome [19, 20]

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