Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA

Daryi Wang, Yu Wei Wu, Arthur Chun Chieh Shih, Chung Shien Wu, Ya Nan Wang, Shu Miaw Chaw

Research output: Contribution to journalArticle

50 Citations (Scopus)

Abstract

With the completion of the first gymnosperm mitochondrial genome (mtDNA) from Cycas taitungensis and the availability of more mtDNA taxa in the past 5 years, we have conducted a systematic analysis of DNA transfer from chloroplast genomes (cpDNAs) to mtDNAs (mtpts) in 11 plants, including 2 algae, 1 liverwort, 1 moss, 1 gymnosperm, 3 monocots, and 3 eudicots. By using shared gene order and boundaries between different mtpts as the criterion, the timing of cpDNA transfer during plant evolution was estimated from the phylogenetic tree reconstructed independently from concatenated protein-coding genes of 11 available mtDNAs. Several interesting findings emerged. First, frequent DNA transfer from cpDNA to mtDNA occurred at least as far back as the common ancestor of extant gymnosperms and angiosperms, about 300 MYA. The oldest mtpt is trnV(uac)-trnM(cau)-atpE-atpB-rbcL. Three other mtpts - psaA-psaB, rps19-trnH(gug)-rpl2-rpl23, and psbE-psbF - were dated to the common ancestor of extant angiosperms, at least 150 MYA. However, all protein-coding genes of mtpts have degenerated since their first transfer. Therefore, mtpts contribute nothing to the functioning of mtDNA but junk sequences. We discovered that the cpDNA transfers have occurred randomly at any positions of the cpDNAs. We provide strong evidence that the cp-derived tRNA-trnM(cau) is the only mtpt (1 out of 3 cp-derived tRNA shared by seed plants) truly transferred from cpDNA to mtDNA since the time of the common ancestor of extant gymnosperms and angiosperms. Our observations support the proposition of Richly and Leister (2004) that "primary insertions of organellar DNAs are large and then diverge and fragment over evolutionary time."

Original languageEnglish
Pages (from-to)2040-2048
Number of pages9
JournalMolecular Biology and Evolution
Volume24
Issue number9
DOIs
Publication statusPublished - Sep 2007
Externally publishedYes

Fingerprint

Chloroplast DNA
Mitochondrial Genome
Gymnosperms
gymnosperm
Mitochondrial DNA
chloroplast
genomics
common ancestry
chloroplast DNA
mitochondrial DNA
chloroplasts
genome
Angiosperms
Genes
angiosperm
DNA
transfer DNA
Angiospermae
ancestry
gene

Keywords

  • Chloroplast genome
  • Gene transfer
  • Mitochondrial genome
  • mtpt
  • Seed plants

ASJC Scopus subject areas

  • Genetics
  • Biochemistry
  • Genetics(clinical)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Ecology, Evolution, Behavior and Systematics
  • Agricultural and Biological Sciences (miscellaneous)
  • Molecular Biology

Cite this

Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. / Wang, Daryi; Wu, Yu Wei; Shih, Arthur Chun Chieh; Wu, Chung Shien; Wang, Ya Nan; Chaw, Shu Miaw.

In: Molecular Biology and Evolution, Vol. 24, No. 9, 09.2007, p. 2040-2048.

Research output: Contribution to journalArticle

Wang, Daryi ; Wu, Yu Wei ; Shih, Arthur Chun Chieh ; Wu, Chung Shien ; Wang, Ya Nan ; Chaw, Shu Miaw. / Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. In: Molecular Biology and Evolution. 2007 ; Vol. 24, No. 9. pp. 2040-2048.
@article{1ff38b7f40df4d339a897209eaf0202f,
title = "Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA",
abstract = "With the completion of the first gymnosperm mitochondrial genome (mtDNA) from Cycas taitungensis and the availability of more mtDNA taxa in the past 5 years, we have conducted a systematic analysis of DNA transfer from chloroplast genomes (cpDNAs) to mtDNAs (mtpts) in 11 plants, including 2 algae, 1 liverwort, 1 moss, 1 gymnosperm, 3 monocots, and 3 eudicots. By using shared gene order and boundaries between different mtpts as the criterion, the timing of cpDNA transfer during plant evolution was estimated from the phylogenetic tree reconstructed independently from concatenated protein-coding genes of 11 available mtDNAs. Several interesting findings emerged. First, frequent DNA transfer from cpDNA to mtDNA occurred at least as far back as the common ancestor of extant gymnosperms and angiosperms, about 300 MYA. The oldest mtpt is trnV(uac)-trnM(cau)-atpE-atpB-rbcL. Three other mtpts - psaA-psaB, rps19-trnH(gug)-rpl2-rpl23, and psbE-psbF - were dated to the common ancestor of extant angiosperms, at least 150 MYA. However, all protein-coding genes of mtpts have degenerated since their first transfer. Therefore, mtpts contribute nothing to the functioning of mtDNA but junk sequences. We discovered that the cpDNA transfers have occurred randomly at any positions of the cpDNAs. We provide strong evidence that the cp-derived tRNA-trnM(cau) is the only mtpt (1 out of 3 cp-derived tRNA shared by seed plants) truly transferred from cpDNA to mtDNA since the time of the common ancestor of extant gymnosperms and angiosperms. Our observations support the proposition of Richly and Leister (2004) that {"}primary insertions of organellar DNAs are large and then diverge and fragment over evolutionary time.{"}",
keywords = "Chloroplast genome, Gene transfer, Mitochondrial genome, mtpt, Seed plants",
author = "Daryi Wang and Wu, {Yu Wei} and Shih, {Arthur Chun Chieh} and Wu, {Chung Shien} and Wang, {Ya Nan} and Chaw, {Shu Miaw}",
year = "2007",
month = "9",
doi = "10.1093/molbev/msm133",
language = "English",
volume = "24",
pages = "2040--2048",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "9",

}

TY - JOUR

T1 - Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA

AU - Wang, Daryi

AU - Wu, Yu Wei

AU - Shih, Arthur Chun Chieh

AU - Wu, Chung Shien

AU - Wang, Ya Nan

AU - Chaw, Shu Miaw

PY - 2007/9

Y1 - 2007/9

N2 - With the completion of the first gymnosperm mitochondrial genome (mtDNA) from Cycas taitungensis and the availability of more mtDNA taxa in the past 5 years, we have conducted a systematic analysis of DNA transfer from chloroplast genomes (cpDNAs) to mtDNAs (mtpts) in 11 plants, including 2 algae, 1 liverwort, 1 moss, 1 gymnosperm, 3 monocots, and 3 eudicots. By using shared gene order and boundaries between different mtpts as the criterion, the timing of cpDNA transfer during plant evolution was estimated from the phylogenetic tree reconstructed independently from concatenated protein-coding genes of 11 available mtDNAs. Several interesting findings emerged. First, frequent DNA transfer from cpDNA to mtDNA occurred at least as far back as the common ancestor of extant gymnosperms and angiosperms, about 300 MYA. The oldest mtpt is trnV(uac)-trnM(cau)-atpE-atpB-rbcL. Three other mtpts - psaA-psaB, rps19-trnH(gug)-rpl2-rpl23, and psbE-psbF - were dated to the common ancestor of extant angiosperms, at least 150 MYA. However, all protein-coding genes of mtpts have degenerated since their first transfer. Therefore, mtpts contribute nothing to the functioning of mtDNA but junk sequences. We discovered that the cpDNA transfers have occurred randomly at any positions of the cpDNAs. We provide strong evidence that the cp-derived tRNA-trnM(cau) is the only mtpt (1 out of 3 cp-derived tRNA shared by seed plants) truly transferred from cpDNA to mtDNA since the time of the common ancestor of extant gymnosperms and angiosperms. Our observations support the proposition of Richly and Leister (2004) that "primary insertions of organellar DNAs are large and then diverge and fragment over evolutionary time."

AB - With the completion of the first gymnosperm mitochondrial genome (mtDNA) from Cycas taitungensis and the availability of more mtDNA taxa in the past 5 years, we have conducted a systematic analysis of DNA transfer from chloroplast genomes (cpDNAs) to mtDNAs (mtpts) in 11 plants, including 2 algae, 1 liverwort, 1 moss, 1 gymnosperm, 3 monocots, and 3 eudicots. By using shared gene order and boundaries between different mtpts as the criterion, the timing of cpDNA transfer during plant evolution was estimated from the phylogenetic tree reconstructed independently from concatenated protein-coding genes of 11 available mtDNAs. Several interesting findings emerged. First, frequent DNA transfer from cpDNA to mtDNA occurred at least as far back as the common ancestor of extant gymnosperms and angiosperms, about 300 MYA. The oldest mtpt is trnV(uac)-trnM(cau)-atpE-atpB-rbcL. Three other mtpts - psaA-psaB, rps19-trnH(gug)-rpl2-rpl23, and psbE-psbF - were dated to the common ancestor of extant angiosperms, at least 150 MYA. However, all protein-coding genes of mtpts have degenerated since their first transfer. Therefore, mtpts contribute nothing to the functioning of mtDNA but junk sequences. We discovered that the cpDNA transfers have occurred randomly at any positions of the cpDNAs. We provide strong evidence that the cp-derived tRNA-trnM(cau) is the only mtpt (1 out of 3 cp-derived tRNA shared by seed plants) truly transferred from cpDNA to mtDNA since the time of the common ancestor of extant gymnosperms and angiosperms. Our observations support the proposition of Richly and Leister (2004) that "primary insertions of organellar DNAs are large and then diverge and fragment over evolutionary time."

KW - Chloroplast genome

KW - Gene transfer

KW - Mitochondrial genome

KW - mtpt

KW - Seed plants

UR - http://www.scopus.com/inward/record.url?scp=34548410837&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34548410837&partnerID=8YFLogxK

U2 - 10.1093/molbev/msm133

DO - 10.1093/molbev/msm133

M3 - Article

C2 - 17609537

AN - SCOPUS:34548410837

VL - 24

SP - 2040

EP - 2048

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 9

ER -