Involvement of plastid, mitochondrial and nuclear genomes in plant-to-plant horizontal gene transfer

Abstract

This review focuses on plant-to-plant horizontal gene transfer (HGT) involving the three DNA-containing cellular compartments. It highlights the great incidence of HGT in the mitochondrial genome (mtDNA) of angiosperms, the increasing number of examples in plant nuclear genomes, and the lack of any convincing evidence for HGT in the well-studied plastid genome of land plants. Most of the foreign mitochondrial genes are non-functional, generally found as pseudogenes in the recipient plant mtDNA that maintains its functional native genes. The few exceptions involve chimeric HGT, in which foreign and native copies recombine leading to a functional and single copy of the gene. Maintenance of foreign genes in plant mitochondria is probably the result of genetic drift, but a possible evolutionary advantage may be conferred through the generation of genetic diversity by gene conversion between native and foreign copies. Conversely, a few cases of nuclear HGT in plants involve functional transfers of novel genes that resulted in adaptive evolution. Direct cell-to-cell contact between plants (e.g. host-parasite relationships or natural grafting) facilitate the exchange of genetic material, in which HGT has been reported for both nuclear and mitochondrial genomes, and in the form of genomic DNA, instead of RNA. A thorough review of the literature indicates that HGT in mitochondrial and nuclear genomes of angiosperms is much more frequent than previously expected and that the evolutionary impact and mechanisms underlying plant-to-plant HGT remain to be uncovered.

The First Evidence of a Host-to-Parasite Mitochondrial Gene Transfer in Orobanchaceae

“…A close physical association between a parasite and its host appears to be the major source of HGTs among flowering plants (Sanchez-Puerta, 2014;Davis and Xi, 2015).…”

“…Surprisingly, molecular relics such as the poly(A) tail at the end of a gene with an unknown function that was acquired by Striga hermonthica from Sorghum Moench suggest that HGT might be an mRNA-mediated process (Yoshida et al, 2010). On the other hand, many of the horizontally transferred DNA fragments are genes with introns or donor-specific introns that are considered to be footprints of HGT events (Renner and Bellot, 2012;Sanchez-Puerta, 2014). This may be explained by the direct uptake of genomic DNA without any cDNA intermediates.…”

“…For prokaryotes and several unicellular phagotrophic protists, HGT is a common and important way of acquiring novel genes (Ochman et al, 2000;Koonin et al, 2001;Keeling and Palmer, 2008). A number of studies have shown that HGT is also not uncommon in land plants, especially those with a parasitic lifestyle (Richardson and Palmer, 2007;Sanchez-Puerta, 2014). A common way to detect HGT is to search for incongruences between gene trees and widely accepted species relationships (Keeling and Palmer, 2008;Renner and Bellot, 2012;Davis and Xi, 2015).…”

“…Mitochondria are very active in the DNA uptake and have been shown to acquire both single and multiple genes via HGT (Bergthorsson et al, 2004;Richardson and Palmer, 2007;Xi et al, 2013;Mower et al, 2010). Horizontal transfers of nuclear genes are significantly less frequent and there is no conclusive evidence of plastid-to-plastid HGT (Richardson and Palmer, 2007;Zhang et al, 2014;Sanchez-Puerta, 2014).…”

Letter from the Editors

“…The absence of Rab5 suggests a significant modification or degradation of the endocytotic pathway in these algae. In turn, Sanchez-Puerta [8] presents available data on the participation of mitochondrial, plastid, and nuclear genomes in horizontal gene transfer between distinct plant species with a special emphasis on mitochondrial genomes. The paper by Krenz et al [9] is devoted to stromules, the peculiar extensions of the envelope of primary plastids.…”