Cytonuclear coevolution in a holoparasitic plant with highly disparate organellar genomes.


Journal

Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343

Informations de publication

Date de publication:
Aug 2022
Historique:
received: 25 11 2021
accepted: 18 03 2022
pubmed: 2 4 2022
medline: 30 7 2022
entrez: 1 4 2022
Statut: ppublish

Résumé

Contrasting substitution rates in the organellar genomes of Lophophytum agree with the DNA repair, replication, and recombination gene content. Plastid and nuclear genes whose products form multisubunit complexes co-evolve. The organellar genomes of the holoparasitic plant Lophophytum (Balanophoraceae) show disparate evolution. In the plastid, the genome has been severely reduced and presents a > 85% AT content, while in the mitochondria most protein-coding genes have been replaced by homologs acquired by horizontal gene transfer (HGT) from their hosts (Fabaceae). Both genomes carry genes whose products form multisubunit complexes with those of nuclear genes, creating a possible hotspot of cytonuclear coevolution. In this study, we assessed the evolutionary rates of plastid, mitochondrial and nuclear genes, and their impact on cytonuclear evolution of genes involved in multisubunit complexes related to lipid biosynthesis and proteolysis in the plastid and those in charge of the oxidative phosphorylation in the mitochondria. Genes from the plastid and the mitochondria (both native and foreign) of Lophophytum showed extremely high and ordinary substitution rates, respectively. These results agree with the biased loss of plastid-targeted proteins involved in angiosperm organellar repair, replication, and recombination machinery. Consistent with the high rate of evolution of plastid genes, nuclear-encoded subunits of plastid complexes showed disproportionate increases in non-synonymous substitution rates, while those of the mitochondrial complexes did not show different rates than the control (i.e. non-organellar nuclear genes). Moreover, the increases in the nuclear-encoded subunits of plastid complexes were positively correlated with the level of physical interaction they possess with the plastid-encoded ones. Overall, these results suggest that a structurally-mediated compensatory factor may be driving plastid-nuclear coevolution in Lophophytum, and that mito-nuclear coevolution was not altered by HGT.

Identifiants

pubmed: 35359176
doi: 10.1007/s11103-022-01266-9
pii: 10.1007/s11103-022-01266-9
doi:

Substances chimiques

Chloroplast Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

673-688

Subventions

Organisme : Agencia Nacional de Promoción Científica y Tecnológica
ID : PICT-2017-0691
Organisme : Universidad Nacional de Cuyo
ID : 06/A724

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature B.V.

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Auteurs

Luis F Ceriotti (LF)

Facultad de Ciencias Agrarias, IBAM, Universidad Nacional de Cuyo, CONICET, Almirante Brown 500, Chacras de Coria, M5528AHB, Mendoza, Argentina.
Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Padre Jorge Contreras 1300, M5502JMA, Mendoza, Argentina.

Leonardo Gatica-Soria (L)

Facultad de Ciencias Agrarias, IBAM, Universidad Nacional de Cuyo, CONICET, Almirante Brown 500, Chacras de Coria, M5528AHB, Mendoza, Argentina.
Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Padre Jorge Contreras 1300, M5502JMA, Mendoza, Argentina.

M Virginia Sanchez-Puerta (MV)

Facultad de Ciencias Agrarias, IBAM, Universidad Nacional de Cuyo, CONICET, Almirante Brown 500, Chacras de Coria, M5528AHB, Mendoza, Argentina. mvsanchezpuerta@fca.uncu.edu.ar.
Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Padre Jorge Contreras 1300, M5502JMA, Mendoza, Argentina. mvsanchezpuerta@fca.uncu.edu.ar.

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