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

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.

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

“…The Acacia dpo has only 55% similarity at the protein level to sequences in other angiosperm mtDNAs, in agreement with a study that reported greater sequence divergence between plasmid-derived sequences than between other mitochondrial genes (Warren et al 2016). The A. ligulata mtDNA also contains 22 MTPTs encompassing 3.2% of the genome (Table 1), a similar value to that of other legume mitochondrial genomes (Gandini & Sanchez-Puerta 2017;Sloan & Wu 2014). Of these, two were previously described as foreign because they were closely related to sequences in Piperales and Salicales, respectively (Gandini & Sanchez-Puerta 2017).…”

“…The A. ligulata mtDNA also contains 22 MTPTs encompassing 3.2% of the genome (Table 1), a similar value to that of other legume mitochondrial genomes (Gandini & Sanchez-Puerta 2017;Sloan & Wu 2014). Of these, two were previously described as foreign because they were closely related to sequences in Piperales and Salicales, respectively (Gandini & Sanchez-Puerta 2017).…”

“…This model states that only mitochondrial sequences are transferred into the recipient plant mitochondria, that only species from the green lineage are compatible donors because they share a similar mitochondrial fusion mechanism with the recipient plant, and that plant mitochondrial genomes will recombine to form a chimeric mtDNA (Rice et al 2013). A corollary to the model is that foreign plastid or nuclear sequences are first acquired by the donor mitochondria by intracellular gene transfer from the plastid and nuclear genomes and later horizontallytransferred to the recipient mitochondria by mitochondrion-to-mitochondrion (mt-to-mt) HGT (Gandini & Sanchez-Puerta 2017;Rice et al 2013). Several natural mechanisms that enable the transfer of whole mitochondria have been proposed, including direct transmission involving tissue grafts, illegitimate pollination, or host-parasite interactions, and indirect transmission mediated by vectors such as viruses, bacteria, insects, and fungi (Keeling & Palmer 2008;Mower et al 2004;Sanchez-Puerta et al 2008;Stegemann & Bock 2009).…”

Chlorella vulgaris genome assembly and annotation reveals the molecular basis for metabolic acclimation to high light conditions

“…rpoC2 was usually found in the chloroplast genome coding for a RNA polymerase beta subunit (Shimada et al ., ) but traces of rpoC2 plastid gene in the mitochondrial genome have been already reported occasionally in mitochondrial genome of land plants (Goremykin et al ., ; Straub et al ., ). This result suggests an uncommon horizontal gene transfer from chloroplast to mitochondrial genome in Chlorophyta which was previously reported only upon land colonization (Wang et al ., ; Gandini and Sanchez‐Puerta, ).…”

The big, the bad, and the beautiful: Biology of the world's largest flowers

“…These plastid genes were transferred into the host mitochondria via intergenomic transfer in the Tetrastigma host, and subsequently acquired horizontally by Rafflesiaceae, underscoring the importance of thorough phylogenetic and synteny analyses to discern vertically and horizontally inherited gene copies. The phenomenon of intergenomic transfer from plastid to mitochondrial genome within species followed by mitochondrial to mitochondrial HGT between species has been recently verified at a broader scale in plants (Gandini & Sanchez-Puerta, 2017). In Rafflesiaceae, some of the horizontally transferred mitochondrial genes appear derived from Cucurbitaceae and Apiaceae.…”