Abstract
Chromosome rearrangements are important drivers in genome and gene evolution, with implications ranging from speciation to development to disease. In the flagellate Diplonema papillatum (Euglenozoa), mitochondrial genome rearrangements have resulted in nearly hundred chromosomes and a systematic dispersal of gene fragments across the multipartite genome. Maturation into functional RNAs involves separate transcription of gene pieces, joining of precursor RNAs via trans-splicing, and RNA editing by substitution and uridine additions both reconstituting crucial coding sequence. How widespread these unusual features are across diplonemids is unclear. We have analyzed the mitochondrial genomes and transcriptomes of four species from the Diplonema/Rhynchopus clade, revealing a considerable genomic plasticity. Although gene breakpoints, and thus the total number of gene pieces (~80), are essentially conserved across this group, the number of distinct chromosomes varies by a factor of two, with certain chromosomes combining up to eight unrelated gene fragments. Several internal protein-coding gene pieces overlap substantially, resulting, for example, in a stretch of 22 identical amino acids in cytochrome c oxidase subunit 1 and NADH dehydrogenase subunit 5. Finally, the variation of post-transcriptional editing patterns across diplonemids indicates compensation of two adverse trends: rapid sequence evolution and loss of genetic information through unequal chromosome segregation.
Highlights
Chromosome rearrangements are important drivers in genome and gene evolution, with implications ranging from speciation to development to disease
We investigate mitochondrial genome rearrangements across diplonemids, examining whether the eccentric, yet orderly mitochondrial genome structure of D. papillatum mitochondria is a landmark of diplonemids at large, or rather just one instance among a broad range of resourceful mitochondrial DNA (mtDNA) architectures
These species, together with D. papillatum examined earlier, represent the diversity of the Diplonema/Rhynchopus (D/R) clade according to nuclear-gene phylogenies[14,25]
Summary
Chromosome rearrangements are important drivers in genome and gene evolution, with implications ranging from speciation to development to disease. In the flagellate Diplonema papillatum (Euglenozoa), mitochondrial genome rearrangements have resulted in nearly hundred chromosomes and a systematic dispersal of gene fragments across the multipartite genome. Maturation into functional RNAs involves separate transcription of gene pieces, joining of precursor RNAs via transsplicing, and RNA editing by substitution and uridine additions both reconstituting crucial coding sequence. How widespread these unusual features are across diplonemids is unclear. The large body of data on genome rearrangements in mitochondria documents sequence deletions, insertions, and reshuffling[8,9], and change of topology by linearization of the originally circular chromosome, Department Computer Science, and Interdisciplinary Center for Bioinformatics, University Leipzig, Härtelstrasse 16-18, D-04107, Leipzig, Germany. As of not a single species of the DSPD-clades has been isolated
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