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 holoparasit...

Full description

Bibliographic Details
Main Authors: Jingfang Chen, Runxian Yu, Jinhong Dai, Ying Liu, Renchao Zhou
Format: Article
Language:English
Published: BMC 2020-05-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-020-02415-2
_version_ 1818383723449548800
author Jingfang Chen
Runxian Yu
Jinhong Dai
Ying Liu
Renchao Zhou
author_facet Jingfang Chen
Runxian Yu
Jinhong Dai
Ying Liu
Renchao Zhou
author_sort Jingfang Chen
collection DOAJ
description 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.
first_indexed 2024-12-14T03:10:54Z
format Article
id doaj.art-5f513ca8eada4cf2b47143f55b1c1ecb
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-12-14T03:10:54Z
publishDate 2020-05-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-5f513ca8eada4cf2b47143f55b1c1ecb2022-12-21T23:19:16ZengBMCBMC Plant Biology1471-22292020-05-0120111010.1186/s12870-020-02415-2The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indicaJingfang Chen0Runxian Yu1Jinhong Dai2Ying Liu3Renchao Zhou4State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen UniversityAbstract 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.http://link.springer.com/article/10.1186/s12870-020-02415-2Aeginetia indicaPlastid genomeTranscriptome
spellingShingle Jingfang Chen
Runxian Yu
Jinhong Dai
Ying Liu
Renchao Zhou
The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica
BMC Plant Biology
Aeginetia indica
Plastid genome
Transcriptome
title The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica
title_full The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica
title_fullStr The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica
title_full_unstemmed The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica
title_short The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica
title_sort loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant aeginetia indica
topic Aeginetia indica
Plastid genome
Transcriptome
url http://link.springer.com/article/10.1186/s12870-020-02415-2
work_keys_str_mv AT jingfangchen thelossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT runxianyu thelossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT jinhongdai thelossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT yingliu thelossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT renchaozhou thelossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT jingfangchen lossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT runxianyu lossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT jinhongdai lossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT yingliu lossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica
AT renchaozhou lossofphotosynthesispathwayandgenomiclocationsofthelostplastidgenesinaholoparasiticplantaeginetiaindica