Abstract
Key Message
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.
Abstract
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 85% AT content, while in the mitochondria most protein-coding genes have been replaced by homologs acquired by horizontal gene transfer (HGT) from their hosts (Fabaceae).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.
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Acknowledgements
We thank M.E. Roulet for help with mitochondrial alignments. This work used the Toko Cluster from FCEN-UNCuyo, which is part of the SNCAD-MinCyT, Argentina, and the Sartoi Cluster from IBAM (FCA-UNCuyo).
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This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (PICT-2017-0691) and Universidad Nacional de Cuyo (06/A724) through funding to M.V.S-P.
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LFC and MVSP designed the study and wrote the manuscript. LFC and LGS analyzed the data and edited the manuscript. MVSP supervised the work.
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Ceriotti, L.F., Gatica-Soria, L. & Sanchez-Puerta, M.V. Cytonuclear coevolution in a holoparasitic plant with highly disparate organellar genomes. Plant Mol Biol 109, 673–688 (2022). https://doi.org/10.1007/s11103-022-01266-9
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DOI: https://doi.org/10.1007/s11103-022-01266-9