Extensive plastome reduction and loss of photosynthesis genes in Diphelypaea coccinea, a holoparasitic plant of the family Orobanchaceae.

Eugeny V Gruzdev,Andrey V Mardanov,Alexey V Beletsky,Vitaly V Kadnikov,Nikolai V Ravin

doi:10.7717/peerj.7830

Eugeny V Gruzdev, Andrey V Mardanov + Show 3 more

Open Access

https://doi.org/10.7717/peerj.7830

Copy DOI

Abstract

BackgroundParasitic plants have the ability to obtain nutrients from their hosts and are less dependent on their own photosynthesis or completely lose this capacity. The reduction in plastid genome size and gene content in parasitic plants predominantly results from loss of photosynthetic genes. Plants from the family Orobanchaceae are used as models for studying plastid genome evolution in the transition from an autotrophic to parasitic lifestyle. Diphelypaea is a poorly studied genus of the Orobanchaceae, comprising two species of non-photosynthetic root holoparasites. In this study, we sequenced the plastid genome of Diphelypaea coccinea and compared it with other Orobanchaceae, to elucidate patterns of plastid genome evolution. In addition, we used plastid genome data to define the phylogenetic position of Diphelypaea spp.MethodsThe complete nucleotide sequence of the plastid genome of D. coccinea was obtained from total plant DNA, using pyrosequencing technology.ResultsThe D. coccinea plastome is only 66,616 bp in length, and is highly rearranged; however, it retains a quadripartite structure. It contains only four rRNA genes, 25 tRNA genes and 25 protein-coding genes, being one of the most highly reduced plastomes among the parasitic Orobanchaceae. All genes related to photosynthesis, including the ATP synthase genes, had been lost, whereas most housekeeping genes remain intact. The plastome contains two divergent, but probably intact clpP genes. Intron loss had occurred in some protein-coding and tRNA genes. Phylogenetic analysis yielded a fully resolved tree for the Orobanchaceae, with Diphelypaea being a sister group to Orobanche sect. Orobanche.

Highlights

About 1% of all angiosperm species can parasitize other flowering plants or mycorrhizal fungi (Nickrent et al, 1997)
The D. coccinea plastome lacks the ATP synthase genes that are retained intact in most parasitic Orobanchaceae (Wicke et al, 2013)
Being only 66,616 bp in size and containing 54 presumably intact unique genes, the plastome of D. coccinea is one of the most highly reduced among the parasitic Orobanchaceae

Summary

Introduction

About 1% of all angiosperm species can parasitize other flowering plants or mycorrhizal fungi (Nickrent et al, 1997). Extensive plastome reduction and loss of photosynthesis genes in Diphelypaea coccinea, a holoparasitic plant of the family Orobanchaceae. Most evident is a functional and physical reduction of the plastid genome (plastome), which correlates with a loss of genes encoding the photosynthetic machinery and related functions, increased substitution rates, and structural rearrangements (DePamphilis & Palmer, 1990; Wolfe, Morden & Palmer, 1992; Barrett et al, 2014). The reduction in plastid genome size and gene content in parasitic plants predominantly results from loss of photosynthetic genes. Plants from the family Orobanchaceae are used as models for studying plastid genome evolution in the transition from an autotrophic to parasitic lifestyle. The D. coccinea plastome is only 66,616 bp in length, and is highly rearranged; it retains a quadripartite structure It contains only four rRNA genes, 25 tRNA genes and 25 protein-coding genes, being one of the most highly reduced plastomes among the parasitic Orobanchaceae.

Methods

Results

Conclusion