Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae)

M. Virginia Sanchez-Puerta, Alejandro Edera, Carolina L. Gandini, Anna V. Williams, Katharine A. Howell, Paul G. Nevill, Ian Small

Research output: Contribution to journalArticle

4 Citations (Scopus)
84 Downloads (Pure)

Abstract

Angiosperm mitochondrial horizontal gene transfer (HGT) has been widely reported during the past decades. With a few exceptions, foreign sequences are mitochondrial genes or intronic regions from other plants, indicating that HGT has played a major role in shaping mitochondrial genome evolution. Host-parasite relationships are a valuable system to study this phenomenon due to the high frequency of HGT. In particular, the interaction between mimosoid legumes and holoparasites of the genus Lophophytum represents an outstanding opportunity to discern HGT events. The mitochondrial genome of the holoparasite L. mirabile has remarkable properties, the most extraordinary of which is the presence of 34 out of 43 mitochondrial protein genes acquired from its legume host, with the stunning replacement of up to 26 native homologs. However, the origin of the intergenic sequences that represent the majority (> 90%) of the L. mirabile mtDNA remains largely unknown. The lack of mitochondrial sequences available from the donor angiosperm lineage (mimosoid legumes) precluded a large-scale evolutionary study. We sequenced and assembled the mitochondrial genome of the mimosoid Acacia ligulata and performed genome wide comparisons with L. mirabile. The A. ligulata mitochondrial genome is almost 700 kb in size, encoding 60 genes. About 60% of the L. mirabile mtDNA had greatest affinity to members of the family Fabaceae (similar to 49% to mimosoids in particular) with an average sequence identity of similar to 96%, including genes but mostly intergenic regions. These findings strengthen the mitochondrial fusion compatibility model for angiosperm mitochondrion-to-mitochondrion HGT.

Original languageEnglish
Pages (from-to)243-250
Number of pages8
JournalMolecular Phylogenetics and Evolution
Volume132
DOIs
Publication statusPublished - Mar 2019

Cite this

Virginia Sanchez-Puerta, M. ; Edera, Alejandro ; Gandini, Carolina L. ; Williams, Anna V. ; Howell, Katharine A. ; Nevill, Paul G. ; Small, Ian. / Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae). In: Molecular Phylogenetics and Evolution. 2019 ; Vol. 132. pp. 243-250.
@article{03160ecac6e841e993797044e9f600c3,
title = "Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae)",
abstract = "Angiosperm mitochondrial horizontal gene transfer (HGT) has been widely reported during the past decades. With a few exceptions, foreign sequences are mitochondrial genes or intronic regions from other plants, indicating that HGT has played a major role in shaping mitochondrial genome evolution. Host-parasite relationships are a valuable system to study this phenomenon due to the high frequency of HGT. In particular, the interaction between mimosoid legumes and holoparasites of the genus Lophophytum represents an outstanding opportunity to discern HGT events. The mitochondrial genome of the holoparasite L. mirabile has remarkable properties, the most extraordinary of which is the presence of 34 out of 43 mitochondrial protein genes acquired from its legume host, with the stunning replacement of up to 26 native homologs. However, the origin of the intergenic sequences that represent the majority (> 90{\%}) of the L. mirabile mtDNA remains largely unknown. The lack of mitochondrial sequences available from the donor angiosperm lineage (mimosoid legumes) precluded a large-scale evolutionary study. We sequenced and assembled the mitochondrial genome of the mimosoid Acacia ligulata and performed genome wide comparisons with L. mirabile. The A. ligulata mitochondrial genome is almost 700 kb in size, encoding 60 genes. About 60{\%} of the L. mirabile mtDNA had greatest affinity to members of the family Fabaceae (similar to 49{\%} to mimosoids in particular) with an average sequence identity of similar to 96{\%}, including genes but mostly intergenic regions. These findings strengthen the mitochondrial fusion compatibility model for angiosperm mitochondrion-to-mitochondrion HGT.",
keywords = "Acacia, Lophophytum, Holoparasite, HGT, Evolution, mtDNA, HORIZONTAL TRANSFER, GENE-TRANSFER, PLANT-MITOCHONDRIA, PARASITIC PLANT, GENERATION, FREQUENT, FUSION, TOOL, EXCHANGE, SEQUENCE",
author = "{Virginia Sanchez-Puerta}, M. and Alejandro Edera and Gandini, {Carolina L.} and Williams, {Anna V.} and Howell, {Katharine A.} and Nevill, {Paul G.} and Ian Small",
year = "2019",
month = "3",
doi = "10.1016/j.ympev.2018.12.006",
language = "English",
volume = "132",
pages = "243--250",
journal = "Molecular Phylogenetics and Evolution",
issn = "1055-7903",
publisher = "Academic Press",

}

Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae). / Virginia Sanchez-Puerta, M.; Edera, Alejandro; Gandini, Carolina L.; Williams, Anna V.; Howell, Katharine A.; Nevill, Paul G.; Small, Ian.

In: Molecular Phylogenetics and Evolution, Vol. 132, 03.2019, p. 243-250.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae)

AU - Virginia Sanchez-Puerta, M.

AU - Edera, Alejandro

AU - Gandini, Carolina L.

AU - Williams, Anna V.

AU - Howell, Katharine A.

AU - Nevill, Paul G.

AU - Small, Ian

PY - 2019/3

Y1 - 2019/3

N2 - Angiosperm mitochondrial horizontal gene transfer (HGT) has been widely reported during the past decades. With a few exceptions, foreign sequences are mitochondrial genes or intronic regions from other plants, indicating that HGT has played a major role in shaping mitochondrial genome evolution. Host-parasite relationships are a valuable system to study this phenomenon due to the high frequency of HGT. In particular, the interaction between mimosoid legumes and holoparasites of the genus Lophophytum represents an outstanding opportunity to discern HGT events. The mitochondrial genome of the holoparasite L. mirabile has remarkable properties, the most extraordinary of which is the presence of 34 out of 43 mitochondrial protein genes acquired from its legume host, with the stunning replacement of up to 26 native homologs. However, the origin of the intergenic sequences that represent the majority (> 90%) of the L. mirabile mtDNA remains largely unknown. The lack of mitochondrial sequences available from the donor angiosperm lineage (mimosoid legumes) precluded a large-scale evolutionary study. We sequenced and assembled the mitochondrial genome of the mimosoid Acacia ligulata and performed genome wide comparisons with L. mirabile. The A. ligulata mitochondrial genome is almost 700 kb in size, encoding 60 genes. About 60% of the L. mirabile mtDNA had greatest affinity to members of the family Fabaceae (similar to 49% to mimosoids in particular) with an average sequence identity of similar to 96%, including genes but mostly intergenic regions. These findings strengthen the mitochondrial fusion compatibility model for angiosperm mitochondrion-to-mitochondrion HGT.

AB - Angiosperm mitochondrial horizontal gene transfer (HGT) has been widely reported during the past decades. With a few exceptions, foreign sequences are mitochondrial genes or intronic regions from other plants, indicating that HGT has played a major role in shaping mitochondrial genome evolution. Host-parasite relationships are a valuable system to study this phenomenon due to the high frequency of HGT. In particular, the interaction between mimosoid legumes and holoparasites of the genus Lophophytum represents an outstanding opportunity to discern HGT events. The mitochondrial genome of the holoparasite L. mirabile has remarkable properties, the most extraordinary of which is the presence of 34 out of 43 mitochondrial protein genes acquired from its legume host, with the stunning replacement of up to 26 native homologs. However, the origin of the intergenic sequences that represent the majority (> 90%) of the L. mirabile mtDNA remains largely unknown. The lack of mitochondrial sequences available from the donor angiosperm lineage (mimosoid legumes) precluded a large-scale evolutionary study. We sequenced and assembled the mitochondrial genome of the mimosoid Acacia ligulata and performed genome wide comparisons with L. mirabile. The A. ligulata mitochondrial genome is almost 700 kb in size, encoding 60 genes. About 60% of the L. mirabile mtDNA had greatest affinity to members of the family Fabaceae (similar to 49% to mimosoids in particular) with an average sequence identity of similar to 96%, including genes but mostly intergenic regions. These findings strengthen the mitochondrial fusion compatibility model for angiosperm mitochondrion-to-mitochondrion HGT.

KW - Acacia

KW - Lophophytum

KW - Holoparasite

KW - HGT

KW - Evolution

KW - mtDNA

KW - HORIZONTAL TRANSFER

KW - GENE-TRANSFER

KW - PLANT-MITOCHONDRIA

KW - PARASITIC PLANT

KW - GENERATION

KW - FREQUENT

KW - FUSION

KW - TOOL

KW - EXCHANGE

KW - SEQUENCE

U2 - 10.1016/j.ympev.2018.12.006

DO - 10.1016/j.ympev.2018.12.006

M3 - Article

VL - 132

SP - 243

EP - 250

JO - Molecular Phylogenetics and Evolution

JF - Molecular Phylogenetics and Evolution

SN - 1055-7903

ER -