The Mitochondrial Genome of the Moss Physcomitrella patens Sheds New Light on Mitochondrial Evolution in Land Plants

Abstract

The phylogenetic positions of bryophytes and charophytes, together with their genome features, are important for understanding early land plant evolution. Here we report the complete nucleotide sequence (105,340 bp) of the circular-mapping mitochondrial DNA of the moss Physcomitrella patens. Available evidence suggests that the multipartite structure of the mitochondrial genome in flowering plants does not occur in Physcomitrella. It contains genes for 3 rRNAs (rnl, rns, and rrn5), 24 tRNAs, and 42 conserved mitochondrial proteins (14 ribosomal proteins, 4 ccm proteins, 9 nicotinamide adenine dinucleotide dehydrogenase subunits, 5 ATPase subunits, 2 succinate dehydrogenase subunits, apocytochrome b, 3 cytochrome oxidase subunits, and 4 other proteins). We estimate that 5 tRNA genes are missing that might be encoded by the nuclear genome. The overall mitochondrial genome structure is similar in Physcomitrella, Chara vulgaris, Chaetosphaeridium globosum, and Marchantia polymorpha, with easily identifiable inversions and translocations. Significant synteny with angiosperm and chlorophyte mitochondrial genomes was not detected. Phylogenetic analysis of 18 conserved proteins suggests that the moss-liverwort clade is sister to angiosperms, which is consistent with a previous analysis of chloroplast genes but is not consistent with some analyses using mitochondrial sequences. In Physcomitrella, 27 introns are present within 16 genes. Nine of its intron positions are shared with angiosperms and 4 with Marchantia, which in turn shares only one intron position with angiosperms. The phylogenetic analysis as well as the syntenic structure suggest that the mitochondrial genomes of Physcomitrella and Marchantia retain prototype features among land plant mitochondrial genomes.

Suppression of Repeat-Mediated Gross Mitochondrial Genome Rearrangements by RecA in the Moss Physcomitrella patens

“…To determine whether other short repeats participate in rearrangements of RECA1 disruptant mtDNA, we searched for repeats in the P. patens mtDNA sequence (Terasawa et al, 2007) using REPuter, a program that identifies repeated sequences (Kurtz and Schleiermacher, 1999). We identified 96 pairs of repeats longer than 40 bp.…”

“…The nuclear genome of P. patens, in which gene targeting occurs with an efficiency similar to that observed in yeast (Schaefer, 2001), was recently sequenced (Rensing et al, 2008), and the chloroplast and the mitochondrial genomes were previously sequenced (Sugiura et al, 2003;Terasawa et al, 2007), enabling advanced genetic and molecular biological approaches to be used in this organism. Here, we analyzed the in vivo roles of the P. patens mitochondrial RecA protein RECA1 by targeted nuclear gene inactivation.…”

Newly resolved relationships in an early land plant lineage: Bryophyta class Sphagnopsida (peat mosses)

“…Recent data sets appear to favor the hypothesis that liverworts (phylum Marchantiophyta) comprise the earliest-diverging lineage, followed by the mosses (Bryophyta) and hornworts (Anthocerophyta) ( Qiu et al, 1998 ;Nickrent et al, 2000 ;Shaw and Renzaglia, 2004 ). However, the most data-rich studies to date, based on chloroplast or mitochondrial organellar proteins, like analyses based on sperm cell morphology ( Garbary et al, 1993 ), identify a clade uniting liverworts and mosses, and additional data are still needed before we can consider the branching order of early land plant lineages to be fi nally resolved ( Nishiyama et al, 2004 ;Rodr í guez-Ezpeleta et al, 2007 ;Terasawa et al, 2007 ; but see also Qiu, et al, 2006 ).Notwithstanding that much remains to do, great progress has been made toward resolving phylogenetic relationships within the mosses (phylum Bryophyta s.s.) (e.g., Cox and Hedderson, 1999 ;Cox et al, 2000 ;Newton et al, 2000 ; Goffi net et al, 2001 ;Stech and Frey, 2008 ; Goffi net et al, 2009 ;Wahrmund et al, 2010 ). Major clades resolved by molecular data to a large extent mirror previous classifi cations based on morphology (e.g., Fleischer, 1923 ; Brotherus, 1924 Brotherus, -1925Vitt, 1984 • Premise of the study : The Sphagnopsida, an early-diverging lineage of mosses (phylum Bryophyta), are morphologically and ecologically unique and have profound impacts on global climate.…”

“…Recent data sets appear to favor the hypothesis that liverworts (phylum Marchantiophyta) comprise the earliest-diverging lineage, followed by the mosses (Bryophyta) and hornworts (Anthocerophyta) ( Qiu et al, 1998 ;Nickrent et al, 2000 ;Shaw and Renzaglia, 2004 ). However, the most data-rich studies to date, based on chloroplast or mitochondrial organellar proteins, like analyses based on sperm cell morphology ( Garbary et al, 1993 ), identify a clade uniting liverworts and mosses, and additional data are still needed before we can consider the branching order of early land plant lineages to be fi nally resolved ( Nishiyama et al, 2004 ;Rodr í guez-Ezpeleta et al, 2007 ;Terasawa et al, 2007 ; but see also Qiu, et al, 2006 ).…”

Transformation of the mitochondrial genome

“…As semiautonomous organelles, they possess their own genome, the mitochondrial DNA (mtDNA), that differs in form and size among the various organisms and occurs in multiple copies, varying from a few dozen up to several thousand copies per cell. The mtDNA can form circular molecules in mammals (Boore, 1999) and in some plants, such as bryophytes (liverworts, hornworts and mosses) (Terasawa et al, 2007). In contrast, some organisms, such as the unicellular green alga Chlamydomonas reinhardtii, show linear mtDNAs that end with defined terminal structures, called mitochondrial telomeres (Vahrenholz et al, 1993).…”