Comparative Chloroplast Genome Analyses of Streptophyte Green Algae Uncover Major Structural Alterations in the Klebsormidiophyceae, Coleochaetophyceae and Zygnematophyceae

Lemieux, Claude; Otis, Christian; Turmel, Monique

doi:10.3389/fpls.2016.00697

Cited by 60 publications

(69 citation statements)

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“…Though a divergent protein, our YCF1 phylogeny (fig. 1 a ) shows remarkable resemblance to the most recent species phylogeny based on the phylogenetic analysis of 88 plastid-encoded proteins (Lemieux et al. 2016; fig.…”

Section: Klebsormidium Spp Ycf1 Proteins Stand Outmentioning

confidence: 80%

The Carboxy Terminus of YCF1 Contains a Motif Conserved throughout >500 Myr of Streptophyte Evolution

Vries

Archibald

Gould

2017

Genome Biology and Evolution

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Plastids evolved from cyanobacteria by endosymbiosis. During the course of evolution, the coding capacity of plastid genomes shrinks due to gene loss or transfer to the nucleus. In the green lineage, however, there were apparent gene gains including that of ycf1. Although its function is still debated, YCF1 has proven to be a useful marker for plastid evolution. YCF1 sequence and predicted structural features unite the plastid genomes of land plants with those of their closest algal relatives, the higher streptophyte algae; YCF1 appears to have undergone pronounced changes during the course of streptophyte algal evolution. Using new data, we show that YCF1 underwent divergent evolution in the common ancestor of higher streptophyte algae and Klebsormidiophycae. This divergence resulted in the origin of an extreme, klebsormidiophycean-specific YCF1 and the higher streptophyte Ste-YCF1. Most importantly, our analysis uncovers a conserved carboxy-terminal sequence stretch within YCF1 that is unique to higher streptophytes and hints at an important, yet unexplored function.

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Section: Klebsormidium Spp Ycf1 Proteins Stand Outmentioning

confidence: 80%

The Carboxy Terminus of YCF1 Contains a Motif Conserved throughout >500 Myr of Streptophyte Evolution

Vries

Archibald

Gould

2017

Genome Biology and Evolution

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“…These unusual sequences were probably gained through horizontal transfer of mobile elements, but the donor(s) remain(s) unknown. Genes with similar functions have been documented in the organelle genomes of diverse green algal lineages (Turmel et al, 2009; Turmel, Otis & Lemieux, 2013; Civan et al, 2014; Leliaert & Lopez-Bautista, 2015; Turmel, Otis & Lemieux, 2015; Lemieux, Otis & Turmel, 2016), and intriguingly, homologs of the Oedocladium ORFs have also been localized within or very near the IR in distantly related chlorophytes (Turmel, Otis & Lemieux, 1999b; Turmel et al, 2009; Smith et al, 2013). Considering this observation and the unlikely hypothesis that these sequences were transmitted by vertical descent from a very distant algal ancestor, we suggest that the IR could be a hot spot for the integration of foreign sequences.…”

Section: Discussionmentioning

confidence: 93%

“…A positive correlation has rather been observed between the level of gene rearrangements and the amount of dispersed repeats in land plant lineages displaying highly rearranged genomes (Weng et al, 2014; Blazier et al, 2016). But this correlation does not appear to hold for several green algal lineages (Turmel, Otis & Lemieux, 2015; Lemieux, Otis & Turmel, 2016), including the Oedogoniales in which the repeat-poor and gene-dense Oedogonium cpDNA differs from the repeat-rich Oedocladium cpDNA by a single reversal.…”

Section: Discussionmentioning

confidence: 97%

“…As reported for the Streptophyta (Lemieux, Otis & Turmel, 2000; Lemieux, Otis & Turmel, 2016), the ancestral quadripartite structure of chlorophyte cpDNA is characterized by the presence of two identical copies of a large inverted repeat (IR) separated from one another by large and small single-copy (SC) regions that are highly conserved in gene content (Turmel et al, 1999a; Turmel, Otis & Lemieux, 2015; Turmel et al, 2016a). While most of the investigated chlorophycean genomes have retained an IR that encodes the rRNA operon (consisting of rrs , trnI (gau), trnA (ugc), rrl , and rrf ), partitioning of genes among the SC regions differs considerably relative to ancestral-type chlorophyte genomes and other chlorophyte genomes with a derived quadripartite structure (e.g., in ulvophycean cpDNAs: (Pombert et al, 2005; Pombert, Lemieux & Turmel, 2006).…”

Section: Introductionmentioning

confidence: 96%

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Proliferation of group II introns in the chloroplast genome of the green algaOedocladium carolinianum(Chlorophyceae)

Brouard

Turmel

Otis

et al. 2016

PeerJ

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BackgroundThe chloroplast genome sustained extensive changes in architecture during the evolution of the Chlorophyceae, a morphologically and ecologically diverse class of green algae belonging to the Chlorophyta; however, the forces driving these changes are poorly understood. The five orders recognized in the Chlorophyceae form two major clades: the CS clade consisting of the Chlamydomonadales and Sphaeropleales, and the OCC clade consisting of the Oedogoniales, Chaetophorales, and Chaetopeltidales. In the OCC clade, considerable variations in chloroplast DNA (cpDNA) structure, size, gene order, and intron content have been observed. The large inverted repeat (IR), an ancestral feature characteristic of most green plants, is present in Oedogonium cardiacum (Oedogoniales) but is lacking in the examined members of the Chaetophorales and Chaetopeltidales. Remarkably, the Oedogonium 35.5-kb IR houses genes that were putatively acquired through horizontal DNA transfer. To better understand the dynamics of chloroplast genome evolution in the Oedogoniales, we analyzed the cpDNA of a second representative of this order, Oedocladium carolinianum.MethodsThe Oedocladium cpDNA was sequenced and annotated. The evolutionary distances separating Oedocladium and Oedogonium cpDNAs and two other pairs of chlorophycean cpDNAs were estimated using a 61-gene data set. Phylogenetic analysis of an alignment of group IIA introns from members of the OCC clade was performed. Secondary structures and insertion sites of oedogonialean group IIA introns were analyzed.ResultsThe 204,438-bp Oedocladium genome is 7.9 kb larger than the Oedogonium genome, but its repertoire of conserved genes is remarkably similar and gene order differs by only one reversal. Although the 23.7-kb IR is missing the putative foreign genes found in Oedogonium, it contains sequences coding for a putative phage or bacterial DNA primase and a hypothetical protein. Intergenic sequences are 1.5-fold longer and dispersed repeats are more abundant, but a smaller fraction of the Oedocladium genome is occupied by introns. Six additional group II introns are present, five of which lack ORFs and carry highly similar sequences to that of the ORF-less IIA intron shared with Oedogonium. Secondary structure analysis of the group IIA introns disclosed marked differences in the exon-binding sites; however, each intron showed perfect or nearly perfect base pairing interactions with its target site.DiscussionOur results suggest that chloroplast genes rearrange more slowly in the Oedogoniales than in the Chaetophorales and raise questions as to what was the nature of the foreign coding sequences in the IR of the common ancestor of the Oedogoniales. They provide the first evidence for intragenomic proliferation of group IIA introns in the Viridiplantae, revealing that intron spread in the Oedocladium lineage likely occurred by retrohoming after sequence divergence of the exon-binding sites.

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“…One of several groups postulated to be closely related to embryophytes ( Karol et al, 2001 ; Lewis and McCourt, 2004 ;McCourt et al, 2004 ;Turmel et al, 2006 ;Finet et al, 2010 ;Leliaert et al, 2012 ;Pérez et al, 2014 ;Lemieux et al, 2016 ), the Characeae are unique among green algae in the complexity of their vegetative thallus and sexual structures, including multicellular oogonia and antheridia ( Wood and Imahori, 1965 ). Th alli have a main axis of large, multinucleate, single-celled internodes, punctuated by multicellular nodes composed of small, uninucleate cells.…”

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confidence: 99%

First discovery of the charophycean green alga Lychnothamnus barbatus (Charophyceae) extant in the New World

Karol

Skawinski

McCourt

et al. 2017

American J of Botany

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PREMISE OF THE STUDY:Although some species of Characeae, known as stoneworts, can be found on every continent except Antarctica, many species and some genera have limited geographic distributions. The genus Lychnothamnus , represented by a single extant species L. barbatus , was known only from scattered localities in Europe and Australasia until it was recently discovered in North America. METHODS:Morphological identifi cations were made from specimens collected in Minnesota and Wisconsin, USA. DNA sequences were obtained for three plastid-encoded genes ( atpB , psbC , rbcL ) from seven putative Lychnothamnus samples from two states in the USA Distribution and abundance were estimated in each lake using point intercept surveys where surveyors sampled aquatic vegetation.KEY RESULTS: Fourteen lakes in Wisconsin and two lakes in Minnesota, USA, were found to harbor Lychnothamnus barbatus . These represent the fi rst report of this rare charophycean extant in the New World. The North American specimens matched the morphological description for L. barbatus and were compared directly with the neotype. Phylogenetic results using three plastid-encoded genes confi rmed the identifi cation placing New World samples with those from Europe and Australasia. Our phylogenetic analyses also confi rmed the sister relationship between L. barbatus and Nitellopsis obtusa . CONCLUSIONS:Because this taxon is not known for aggressive invasiveness in its native range, it may have existed in heretofore-undiscovered native populations, although the possibility that it is a recent introduction cannot be eliminated. The potential for discovery of novel lineages of green algae in even well-studied regions is apparently far from exhausted.

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Comparative Chloroplast Genome Analyses of Streptophyte Green Algae Uncover Major Structural Alterations in the Klebsormidiophyceae, Coleochaetophyceae and Zygnematophyceae

Cited by 60 publications

References 80 publications

The Carboxy Terminus of YCF1 Contains a Motif Conserved throughout >500 Myr of Streptophyte Evolution

The Carboxy Terminus of YCF1 Contains a Motif Conserved throughout >500 Myr of Streptophyte Evolution

Proliferation of group II introns in the chloroplast genome of the green algaOedocladium carolinianum(Chlorophyceae)

First discovery of the charophycean green alga Lychnothamnus barbatus (Charophyceae) extant in the New World

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