Mitochondrial genome evolution in Alismatales: Size reduction and extensive loss of ribosomal protein genes

Abstract

The order Alismatales is a hotspot for evolution of plant mitochondrial genomes characterized by remarkable differences in genome size, substitution rates, RNA editing, retrotranscription, gene loss and intron loss. Here we have sequenced the complete mitogenomes of Zostera marina and Stratiotes aloides, which together with previously sequenced mitogenomes from Butomus and Spirodela, provide new evolutionary evidence of genome size reduction, gene loss and transfer to the nucleus. The Zostera mitogenome includes a large portion of DNA transferred from the plastome, yet it is the smallest known mitogenome from a non-parasitic plant. Using a broad sample of the Alismatales, the evolutionary history of ribosomal protein gene loss is analyzed. In Zostera almost all ribosomal protein genes are lost from the mitogenome, but only some can be found in the nucleus.

Fig 1. Maps of mitogenomes of Zostera marina and Stratiotes aloides.

For Zostera upper genes are transcribed forward; lower genes are transcribed reverse. For Stratiotes inner genes are transcribed clockwise; outer genes are transcribed counter-clockwise. Genes are color coded as indicated in the lower left corner. The names of trans-spliced genes are followed by exon numbers. Only genes assumed to be functional are shown. The figure was created using OGDRAW [38].

Fig 2. Distribution of mitochondrial ribosomal protein genes in Alismatales mitogenomes.

Blank boxes indicate absence of a gene from the mitogenome. Dark grey boxes indicate presence of a gene assumed to be functional. Light grey boxes and Ψ indicates a pseudogene or fragment of gene in the mitogenome. N indicates presence of a gene annotated as of mitochondrial origin in the nuclear genome of Zostera marina. (n) indicates likely presence of a gene in the nuclear genome of Zostera marina, though not annotated as of mitochondrial origin. *Zostera noltii has the same mitochondrial genes, but the potential nuclear location of genes is unknown.

Fig 3. Loss and pseudogenization of mitochondrial ribosomal protein genes in Alismatales.

Bars represent events of loss or pseudogenization. Black bars mark unique events of gene loss from the mitogenome. Red (pseudogenization) and blue (loss) bars mark homoplasious gene changes.