Foreign Plastid Sequences in Plant Mitochondria are Frequently Acquired Via Mitochondrion-to-Mitochondrion Horizontal Transfer

C L Gandini,M V Sanchez-Puerta

doi:10.1038/srep43402

Abstract

Angiosperm mitochondrial genomes (mtDNA) exhibit variable quantities of alien sequences. Many of these sequences are acquired by intracellular gene transfer (IGT) from the plastid. In addition, frequent events of horizontal gene transfer (HGT) between mitochondria of different species also contribute to their expanded genomes. In contrast, alien sequences are rarely found in plastid genomes. Most of the plant-to-plant HGT events involve mitochondrion-to-mitochondrion transfers. Occasionally, foreign sequences in mtDNAs are plastid-derived (MTPT), raising questions about their origin, frequency, and mechanism of transfer. The rising number of complete mtDNAs allowed us to address these questions. We identified 15 new foreign MTPTs, increasing significantly the number of those previously reported. One out of five of the angiosperm species analyzed contained at least one foreign MTPT, suggesting a remarkable frequency of HGT among plants. By analyzing the flanking regions of the foreign MTPTs, we found strong evidence for mt-to-mt transfers in 65% of the cases. We hypothesize that plastid sequences were initially acquired by the native mtDNA via IGT and then transferred to a distantly-related plant via mitochondrial HGT, rather than directly from a foreign plastid to the mitochondrial genome. Finally, we describe three novel putative cases of mitochondrial-derived sequences among angiosperm plastomes.

Highlights

Angiosperm mitochondrial genomes exhibit variable quantities of alien sequences
Plant mitochondrial genomes commonly incorporate nuclear and plastid sequences acquired by intracellular gene transfer (IGT) as well as foreign mitochondrial DNA from other plant species obtained by horizontal gene transfer (HGT)
We analyzed the mitochondrial genomes of 136 diverse species of the green lineage and only identified mtDNAs are plastid-derived (MTPT) in gymnosperms (13 sequences) and angiosperms (1,372 sequences), and none among non-seed plants (Table S1)

Summary

Plant Mitochondria are Frequently

Mitochondrion Horizontal Transfer received: 08 December 2016 accepted: 24 January 2017. Angiosperm mitochondrial genomes (mtDNA) exhibit variable quantities of alien sequences Many of these sequences are acquired by intracellular gene transfer (IGT) from the plastid. We hypothesize that plastid sequences were initially acquired by the native mtDNA via IGT and transferred to a distantlyrelated plant via mitochondrial HGT, rather than directly from a foreign plastid to the mitochondrial genome. Plant mitochondrial genomes (mtDNA) commonly incorporate nuclear and plastid sequences acquired by IGT as well as foreign mitochondrial DNA from other plant species obtained by HGT. Some MTPTs were acquired by HGT from distant angiosperm species[8,14,15,16,17] Whether these sequences were acquired directly from the donor plastid or indirectly from the donor mitochondria is still unclear and it is the focus of the present study. We take advantage of the recent increase in plant organellar sequences in public databases to study the extent of MTPTs and PTMTs among flowering plants, and to weigh evidence on the genomic origin of foreign MTPTs

Results and Discussion

HGT in flanking regions

Gossypium harknessii

Materials and Methods

Author Contributions

Additional Information