Intronic and plasmid-derived regions contribute to the large mitochondrial genome sizes of Agaricomycetes

Current Genetics, Jul 2014

Sizes of mitochondrial genomes vary extensively between fungal species although they typically contain a conserved set of core genes. We have characterised the mitochondrial genome of the conifer root rot pathogen Heterobasidion irregulare and compared the size, gene content and structure of 20 Basidiomycete mitochondrial genomes. The mitochondrial genome of H. irregulare was 114, 193 bp and contained a core set of 15 protein coding genes, two rRNA genes and 26 tRNA genes. In addition, we found six non-conserved open reading frames (ORFs) and four putative plasmid genes clustered in three separate regions together with 24 introns and 14 intronic homing endonuclease genes, unequally spread across seven of the core genes. The size differences among the 20 Basidiomycetes can largely be explained by length variation of intergenic regions and introns. The Agaricomycetes contained the nine largest mitochondrial genomes in the Basidiomycete group and Agaricomycete genomes are significantly (p < 0.001) larger than the other Basidiomycetes. A feature of the Agaricomycete mitochondrial genomes in this study was the simultaneous occurrence of putative plasmid genes and non-conserved ORFs, with Cantharellus cibarius as only exception, where no non-conserved ORF was identified. This indicates a mitochondrial plasmid origin of the non-conserved ORFs or increased mitochondrial genome dynamics of species harbouring mitochondrial plasmids. We hypothesise that two independent factors are the driving forces for large mitochondrial genomes: the homing endonuclease genes in introns and integration of plasmid DNA.

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Intronic and plasmid-derived regions contribute to the large mitochondrial genome sizes of Agaricomycetes

Kajsa Himmelstrand ke Olson Mikael Brandstrm Durling Magnus Karlsson Jan Stenlid 0 ) . Olson M. Brandstrm Durling M. Karlsson J. stenlid Department of Forest Mycology and Plant Pathology, Uppsala BioCenter, swedish University of agricultural sciences , Box 7026, 750 07 Uppsala, sweden sizes of mitochondrial genomes vary extensively between fungal species although they typically contain a conserved set of core genes. We have characterised the mitochondrial genome of the conifer root rot pathogen Heterobasidion irregulare and compared the size, gene content and structure of 20 Basidiomycete mitochondrial genomes. the mitochondrial genome of H. irregulare was 114, 193 bp and contained a core set of 15 protein coding genes, two rRNa genes and 26 tRN a genes. In addition, we found six non-conserved open reading frames (ORFs) and four putative plasmid genes clustered in three separate regions together with 24 introns and 14 intronic homing endonuclease genes, unequally spread across seven of the core genes. the size differences among the 20 Basidiomycetes can largely be explained by length variation of intergenic regions and introns. the agaricomycetes contained the nine largest mitochondrial genomes in the Basidiomycete group and agaricomycete genomes are significantly (p < 0.001) larger than the other Basidiomycetes. a feature of the agaricomycete mitochondrial genomes in this study was the simultaneous occurrence of putative plasmid genes and non-conserved ORFs, with Cantharellus cibarius as only exception, where no non-conserved ORF was identified. this indicates a mitochondrial plasmid origin of the non-conserved ORFs or increased mitochondrial genome dynamics of species harbouring mitochondrial plasmids. We hypothesise that two independent factors are the driving forces for large mitochondrial genomes: the homing endonuclease genes in introns and integration of plasmid DNa. - Mitochondria are believed to have a monophyletic origin from an endosymbiotic -proteobacterium that was engulfed, more than one billion years ago, by a eukaryotic common ancestor (Gray et al. 2001; Bullerwell and lang 2005; Koumandou et al. 2013). the mitochondrial (mt) genomes contain considerably fewer genes than freeliving -proteobacteria and many of the genes that are required for its function seem to have been transferred to the nucleus or replaced by already existing nuclear genes with similar function (adams and Palmer 2003). Mitochondrial genomes occur either as circular or linear molecules (Burger et al. 2003). Genes encoded by the mt genome can be divided into two groups: core genes and exchangeable genes. Core genes are involved in respiration, oxidative phosphorylation and translation (Burger et al. 2003), while exchangeable genes are characterised by variation in type and number among species. there are relatively few differences of mt core genes between and within kingdoms and phyla, although the exact compositions can vary (adams and Palmer 2003). the exchangeable genes can be intronic genes, plasmid-derived genes and non-conserved open reading frames (ORFs). Mitochondrial plasmids are commonly found in plant and fungal mitochondria and are selfreplicating genetic elements that have little or no homology to the mt DNa, hence thought to have a separate evolutionary history from their hosts (Cahan and Kennell 2005; Formighieri et al. 2008). In Basidiomycetes, mt plasmids have been found in for example Flammulina velutipes (Nakai et al. 2000) and Pleurotus ostreatus (Yui et al. 1988) and integrated in mt genomes in Agaricus bisporus (Ferandon et al. 2013), P. ostreatus (Wang et al. 2008) and Moniliophthora perniciosa (Formighieri et al. 2008). the core genes in fungal mt genomes often contain introns with conserved RNa secondary structures involved in autocatalytic splicing (lang et al. 2007). Many of these introns contain ORFs encoding homing endonuclease genes (heGs) that can insert the intron into another intronless gene through a mechanism where the target gene is cleaved at rare recognition sites (lang et al. 2007). this mechanism is called intron homing and could be the reason for the great variability of intron number between species. some of the heGs are also functioning as maturases that promote the RNa folding of the introns (Belfort 2003). Mitochondrial sizes vary extensively in animals and plants with fungal mt sizes being intermediate (12236 kb). at present, there are annotated mt genomes from 165 fungal species (http://www.ncbi.nlm.nih.gov/genomes/GenomesGr oup.cgi?opt=organelle&taxid=4751&sort=Genome). the fungal species investigated so far have a core set of 1315 protein coding genes and two rRNa genes (rns, rnl) in common, although atp9 are lost in euascomycetes (adams and Palmer 2003). t wo other genes, rps3 and rnpB, are repeatedly lost in various fungal lineages (adams and Palmer 2003; Bullerwell and lang 2005). seven genes that encode subunits of the NaDh dehydrogenase complex are lost in the (...truncated)


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Himmelstrand, Kajsa, Olson, Åke, Brandström Durling, Mikael, Karlsson, Magnus, Stenlid, Jan. Intronic and plasmid-derived regions contribute to the large mitochondrial genome sizes of Agaricomycetes, Current Genetics, 2014, pp. 303-313, Volume 60, Issue 4, DOI: 10.1007/s00294-014-0436-z