The Mitogenome of Norway Spruce and a Reappraisal of Mitochondrial Recombination in Plants

Abstract

Plant mitogenomes can be difficult to assemble because they are structurally dynamic and prone to intergenomic DNA transfers, leading to the unusual situation where an organelle genome is far outnumbered by its nuclear counterparts. As a result, comparative mitogenome studies are in their infancy and some key aspects of genome evolution are still known mainly from pregenomic, qualitative methods. To help address these limitations, we combined machine learning and in silico enrichment of mitochondrial-like long reads to assemble the bacterial-sized mitogenome of Norway spruce (Pinaceae: Picea abies). We conducted comparative analyses of repeat abundance, intergenomic transfers, substitution and rearrangement rates, and estimated repeat-by-repeat homologous recombination rates. Prompted by our discovery of highly recombinogenic small repeats in P. abies, we assessed the genomic support for the prevailing hypothesis that intramolecular recombination is predominantly driven by repeat length, with larger repeats facilitating DNA exchange more readily. Overall, we found mixed support for this view: Recombination dynamics were heterogeneous across vascular plants and highly active small repeats (ca. 200 bp) were present in about one-third of studied mitogenomes. As in previous studies, we did not observe any robust relationships among commonly studied genome attributes, but we identify variation in recombination rates as a underinvestigated source of plant mitogenome diversity.

Siberian larch (Larix sibirica Ledeb.) mitochondrial genome assembled using both short and long nucleotide sequence reads is currently the largest known mitogenome

“…Almost all studies that used whole genome sequencing data followed similar strategies to assemble and verify putative mitochondrial sequences. They separated mitochondrial sequences from nuclear and chloroplast by their length, depth of coverage, and GC content [35,36,38], additionally checking for contamination by aligning obtained sequences either to the NCBI GenBank nucleotide (nt) database [37] or to custom database of plant mitogenomes [38]. Annotation process for abovementioned species included BLAST search against database of homologous genes from available plant mt genomes [32,36] or use of MAKER and Prokka software [35].…”

The complete mitochondrial genome of Taxus cuspidata (Taxaceae): eight protein-coding genes have transferred to the nuclear genome

“…In angiosperms, a large number of protein-coding genes have been lost in some lineages, although most of the oldest groups still exhibit near stasis in mitochondrial gene content [46,47,54,55]. Previous studies showed that the Cycas, Ginkgo, Picea and Pinus mitogenomes contain 41 protein-coding genes [3][4][5][6]56]. However, Welwitschia mirabilis lost eleven protein-coding genes [4], including ten ribosomal protein genes (rpl2, rpl5, rps1, rps2, rps7, rps10, rps11, rps13, rps14, and rps19), and the sdh3 gene.…”

“…However, Welwitschia mirabilis lost eleven protein-coding genes [4], including ten ribosomal protein genes (rpl2, rpl5, rps1, rps2, rps7, rps10, rps11, rps13, rps14, and rps19), and the sdh3 gene. It seems that gene loss is an uncommon phenomenon in gymnosperm mitogenomes because gene loss has been detected in only one of the four lineages [5]. However, it is intriguing that nine protein-coding genes (rpl2, rpl10, rps1, rps2, rps7, rps10, rps11, rps14, and sdh3) have been lost from the newly sequenced Taxus cuspidata mitogenome.…”

“…Most (121) sequenced plant mitogenomes are from angiosperms. In contrast to the numerous sequenced angiosperm mitogenomes, however, mitogenomic sequences have been generated for only 6 gymnosperm species, i.e., Cycas taitungensis [3], Ginkgo biloba, Welwitschia mirabilis [4], Pinus taeda (direct submission, MF991879.1, http://www.ncbi.nlm.nih.gov/), Picea abies [5], and Picea sitchensis [6].…”

“…The mitogenome of three species of Pinaceae (Picea abies, ca. 4.90 MB; Picea sitchensis, 5.5 Mb; Pinus taeda, 1.19 Mb) is extremely expanded [5,6] and larger than that of Cycas, Ginkgo and Welwitschia [3,4]. Although all of these Pinaceae mitogenomes have gene and intron contents similar to those in the Cycas and Ginkgo mitogenomes [5][6][7], these mitogenomes from different gymnosperm lineages are different in many other aspects, such as genome structure, repeats, turnover rates, and foreign sequence ratios [4].…”