Nuclear Integrants of Organellar DNA Contribute to Genome Structure and Evolution in Plants

Abstract

The transfer of genetic material from the mitochondria and plastid to the nucleus gives rise to nuclear integrants of mitochondrial DNA (NUMTs) and nuclear integrants of plastid DNA (NUPTs). This frequently occurring DNA transfer is ongoing and has important evolutionary implications. In this review, based on previous studies and the analysis of NUMT/NUPT insertions of more than 200 sequenced plant genomes, we analyzed and summarized the general features of NUMTs/NUPTs and highlighted the genetic consequence of organellar DNA insertions. The statistics of organellar DNA integrants among various plant genomes revealed that organellar DNA-derived sequence content is positively correlated with the nuclear genome size. After integration, the nuclear organellar DNA could undergo different fates, including elimination, mutation, rearrangement, fragmentation, and proliferation. The integrated organellar DNAs play important roles in increasing genetic diversity, promoting gene and genome evolution, and are involved in sex chromosome evolution in dioecious plants. The integrating mechanisms, involving non-homologous end joining at double-strand breaks were also discussed.

Organelle Genetics in Plants

“…In this Special Issue “Organelle Genetics in Plants,” 11 articles were accepted with four reviews and seven original research articles covering outstanding advances in different chloroplast and plant mitochondria research fields ( Table 1 ). These works focus on topics related to organellar gene expression (OGE) (chloroplast RNA editing in soybean [ 5 ], mitochondria RNA editing and intron splicing in soybean during nodulation [ 6 ] and the roles of transcriptional and post-transcriptional regulation of OGE in responses to environmental stress [ 7 , 8 ]); the analysis of nuclear integrants of mitochondrial DNA (NUMTs) or plastid DNA (NUPTs) [ 9 ]; the sequencing and characterization of organellar genomes (the mitogenomes of common bean [ 10 ] and four Trifolium species [ 11 ], and the chloroplast genomes (plastomes) of Trentepohlia odorata [ 12 ], three Utricularia amethystina morphotypes [ 13 ], and three plant parasitic Macrosolen species [ 14 ]); and finally, the most recent advances in plastid genome engineering [ 15 ]. In this editorial, we sum up the main findings of these eleven insightful manuscripts.…”

Evolutionary analysis of the Moringa oleifera genome reveals a recent burst of plastid to nucleus gene duplications

“…Although the simultaneous duplication of large regions of the plastid genome at specific locations of the nuclear genome was responsible of most plastid DNA detected, abundant insertions of very diverse sizes were also found in many different locations of the nuclear genome. Altogether, the fraction of plastid DNA found in the Moringa nuclear genome represented 4.71%, the largest so far reported for a plant genome 49 .…”

“…In most species, plastid DNA represents only a small fraction of less than 1% of the nuclear genome. Very few species have more than 1%, including Ziziphus jujuba, whose genome is composed of up to 1.49% of repeated insertions of small fragments of plastid DNA 49 .…”

“…Plastid genes are usually inactive upon arrival into the nuclear genome because they lack the regulatory motifs required for proper gene expression. Most of them are thus expected to evolve as pseudogenes or non-coding sequences 25 , 49 . Studies performed on Arabidopsis and rice reveal organellar DNA insertions decay over evolutionary time into smaller fragments with more divergent sequences 53 .…”

“…The expression of multiple copies of fragmented RBCL genes, if properly retargeted to the plastid, might impact the structure and function of the RuBisCo multiprotein complex 57 , encoded by both plastid and nuclear genes. Moreover, in certain occasions newly arrived organellar genes have been reported to gain expression capabilities in the nucleus or to reshape nuclear genes by adding extra coding sequences, both contributing to enhance genetic diversity and opportunity for the origin of new gene functions 49 , 58 . The repeated transfer of large chunks of plastid DNA to the nuclear genome may have thus provided the plant with a formidable source of genetic material to modify pre-existing gene functions and/or acquire novel ones.…”