RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants

Abstract Background While photosynthesis is the most notable trait of plants, several lineages of plants (so-called full heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic lev...

Full description

Bibliographic Details
Published in:BMC Genomics
Main Authors: Mikhail I. Schelkunov, Aleksey A. Penin, Maria D. Logacheva
Format: Article
Language:English
Published: BMC 2018-08-01
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-4968-3
_version_ 1857114338401189888
author Mikhail I. Schelkunov
Aleksey A. Penin
Maria D. Logacheva
author_facet Mikhail I. Schelkunov
Aleksey A. Penin
Maria D. Logacheva
author_sort Mikhail I. Schelkunov
collection DOAJ
container_title BMC Genomics
description Abstract Background While photosynthesis is the most notable trait of plants, several lineages of plants (so-called full heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic levels. Results Here, we characterize the transcriptomes of three species representing two lineages of mycoheterotrophic plants: orchids (Epipogium aphyllum and Epipogium roseum) and Ericaceae (Hypopitys monotropa). Comparative analysis is used to highlight the parallelism between distantly related fully heterotrophic plants. In both lineages, we observed genome-wide elimination of nuclear genes that encode proteins related to photosynthesis, while systems associated with protein import to plastids as well as plastid transcription and translation remain active. Genes encoding components of plastid ribosomes that have been lost from the plastid genomes have not been transferred to the nuclear genomes; instead, some of the encoded proteins have been substituted by homologs. The nuclear genes of both Epipogium species accumulated nucleotide substitutions twice as rapidly as their photosynthetic relatives; in contrast, no increase in the substitution rate was observed in H. monotropa. Conclusions Full heterotrophy leads to profound changes in nuclear gene content. The observed increase in the rate of nucleotide substitutions is lineage specific, rather than a universal phenomenon among non-photosynthetic plants.
format Article
id doaj-art-e2d84d0814654ec2bc3ac8b1c70dcd50
institution Directory of Open Access Journals
issn 1471-2164
language English
publishDate 2018-08-01
publisher BMC
record_format Article
spelling doaj-art-e2d84d0814654ec2bc3ac8b1c70dcd502025-08-19T19:11:21ZengBMCBMC Genomics1471-21642018-08-0119111610.1186/s12864-018-4968-3RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plantsMikhail I. Schelkunov0Aleksey A. Penin1Maria D. Logacheva2Institute for Information Transmission Problems, Russian Academy of SciencesInstitute for Information Transmission Problems, Russian Academy of SciencesInstitute for Information Transmission Problems, Russian Academy of SciencesAbstract Background While photosynthesis is the most notable trait of plants, several lineages of plants (so-called full heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic levels. Results Here, we characterize the transcriptomes of three species representing two lineages of mycoheterotrophic plants: orchids (Epipogium aphyllum and Epipogium roseum) and Ericaceae (Hypopitys monotropa). Comparative analysis is used to highlight the parallelism between distantly related fully heterotrophic plants. In both lineages, we observed genome-wide elimination of nuclear genes that encode proteins related to photosynthesis, while systems associated with protein import to plastids as well as plastid transcription and translation remain active. Genes encoding components of plastid ribosomes that have been lost from the plastid genomes have not been transferred to the nuclear genomes; instead, some of the encoded proteins have been substituted by homologs. The nuclear genes of both Epipogium species accumulated nucleotide substitutions twice as rapidly as their photosynthetic relatives; in contrast, no increase in the substitution rate was observed in H. monotropa. Conclusions Full heterotrophy leads to profound changes in nuclear gene content. The observed increase in the rate of nucleotide substitutions is lineage specific, rather than a universal phenomenon among non-photosynthetic plants.http://link.springer.com/article/10.1186/s12864-018-4968-3EricaceaeLoss of photosynthesisMycoheterotrophic plantsNuclear genomeOrchidaceaeRNA-seq
spellingShingle Mikhail I. Schelkunov
Aleksey A. Penin
Maria D. Logacheva
RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
Ericaceae
Loss of photosynthesis
Mycoheterotrophic plants
Nuclear genome
Orchidaceae
RNA-seq
title RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
title_full RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
title_fullStr RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
title_full_unstemmed RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
title_short RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
title_sort rna seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of fully mycoheterotrophic plants
topic Ericaceae
Loss of photosynthesis
Mycoheterotrophic plants
Nuclear genome
Orchidaceae
RNA-seq
url http://link.springer.com/article/10.1186/s12864-018-4968-3
work_keys_str_mv AT mikhailischelkunov rnaseqhighlightsparallelandcontrastingpatternsintheevolutionofthenucleargenomeoffullymycoheterotrophicplants
AT alekseyapenin rnaseqhighlightsparallelandcontrastingpatternsintheevolutionofthenucleargenomeoffullymycoheterotrophicplants
AT mariadlogacheva rnaseqhighlightsparallelandcontrastingpatternsintheevolutionofthenucleargenomeoffullymycoheterotrophicplants