Abstract

BackgroundWith three origins of holoparasitism, Orobanchaceae provides an ideal system to study the evolution of holoparasitic lifestyle in plants. The evolution of holoparasitism can be revealed by plastid genome degradation and coordinated changes in the nuclear genome, since holoparasitic plants lost the capability of photosynthesis. Among the three clades with holoparasitic plants in Orobanchaceae, only Clade VI has no available plastid genome sequences for holoparasitic plants. In this study, we sequenced the plastome and transcriptome of Aeginetia indica, a holoparasitic plant in Clade VI of Orobanchaceae, to study its plastome evolution and the corresponding changes in the nuclear genome as a response of the loss of photosynthetic function.ResultsThe plastome of A. indica is reduced to 86,212 bp in size, and almost all photosynthesis-related genes were lost. Massive fragments of the lost plastid genes were transferred into the mitochondrial and/or nuclear genomes. These fragments could not be detected in its transcriptomes, suggesting that they were non-functional. Most protein coding genes in the plastome showed the signal of relaxation of purifying selection. Plastome and transcriptome analyses indicated that the photosynthesis pathway is completely lost, and that the porphyrin and chlorophyll metabolism pathway is partially retained, although chlorophyll synthesis is not possible.ConclusionsOur study suggests the loss of photosynthesis-related functions in A. indica in both the nuclear and plastid genomes. The lost plastid genes are transferred into its nuclear and/or mitochondrial genomes, and exist in very small fragments with no expression and are thus non-functional. The Aeginetia indica plastome also provides a resource for comparative studies on the repeated evolution of holoparasitism in Orobanchaceae.

Highlights

  • With three origins of holoparasitism, Orobanchaceae provides an ideal system to study the evolution of holoparasitic lifestyle in plants

  • The plastid genome of Aeginetia indica, a holoparasitic plant from Clade VI of Orobanchaceae, was de novo assembled in this study

  • Its plastid genome shows a reduction in size, accompanied with loss or pseudogenization of almost all photosynthesis related genes and some structural rearrangements

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Summary

Introduction

With three origins of holoparasitism, Orobanchaceae provides an ideal system to study the evolution of holoparasitic lifestyle in plants. Plastid genome sizes of holoparasites in Clade III range from 45,673 (Conopholis americana) to 120,840 bp (Orobanche californica) [9]. The number of intact genes in the plastid genomes of Conopholis americana and Orobanche species ranges from 21 to 34 [9], and almost all genes related to photosynthesis (pet, psa, psb, and rbcL) were lost or became pseudogenes. Whereas in the plastid genome of Lathraea squamaria, there are 46 intact genes including many genes related to photosynthesis (such as psa, psb and pet). This might be due to holoparasitic lineages in Clade V is younger than those in Clade III [12]

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