The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica

Abstract

Background: With 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. Results: The 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. Conclusions: Our 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.

Comparative Analysis of Plastid Genomes in the Non-photosynthetic Genus Thismia Reveals Ongoing Gene Set Reduction

“…A notable case is the plastome of Thismia thaithongiana , for which the equilibrium AT-content is approximately 92%. AT-content of plastid genes more than 90% is known for Balanophoraceae ( Schelkunov et al, 2019 ; Su et al, 2019 ; Chen et al, 2020 ), therefore it may be possible to actually achieve such a high AT-content. However, mutation spectra and selection in Thismia may change in the future thus making the current equilibrium AT-contents different from stable AT-contents that Thismia will finally reach.…”

“…The variation of the overall plastome structure in heterotrophs of recent origin is typically minor. The middle stages of plastome reduction have been also extensively studied in both parasitic and mycoheterotrophic plants ( Wicke et al, 2016 ; Lallemand et al, 2019 ; Chen et al, 2020 ). These studies have shown that the patterns of gene loss in general follow the model of Barrett and Davis ( Barrett and Davis, 2012 ).…”

Complete Plastid and Mitochondrial Genomes of Aeginetia indica Reveal Intracellular Gene Transfer (IGT), Horizontal Gene Transfer (HGT), and Cytoplasmic Male Sterility (CMS)

“…The present study was undertaken to determine the plastome and mitogenome of A. indica and to compare these with previously reported results [ 31 ], especially with respect to mitogenome size, gene, and intron contents and repeats, and to analyze the HGT, IGT, and CMS genes in the A. indica mitogenome.…”

“…Previous phylogenetic studies have shown that A. indica is united with Stiga , Buchera , Radmaea, and Harveya [ 29 , 30 ]. The plastome of A. indica has been reported to be 86,212 bp in size and to have lost almost all photosynthesis-related genes [ 31 ].…”

Genomic comparison of non-photosynthetic plants from the family Balanophoraceae with their photosynthetic relatives

“…It was hypothesised that the chlorophyll may have some functions other than photosynthesis (Cummings & Welschmeyer, 1998). Analyses of transcriptomes and genomes showed that the pathways for synthesis and breakdown of the chlorophyll are indeed probably retained in some non-photosynthetic species (Wickett et al, 2011; Schelkunov, Penin & Logacheva, 2018; Marcin et al, 2020), though likely lost in some others (Ng et al, 2018; Schelkunov, Penin & Logacheva, 2018; Chen et al, 2020b). In Rhopalocnemis phalloides and Balanophora fungosa the RBH analysis indicates complete disappearance of chlorophyll synthesis and breakdown genes.…”