The prodigious chloroplast genome of Cladophorales green algae

After more than 10 years of research, and sequencing millions of reads, we were finally able to uncover secrets of the chloroplast genome of Cladophorales green algae. In stark contrast to other algae, little was known about the gene content and structure of the chloroplast genome in this ecologically important group of marine and freshwater green algae. Most previous attempts to amplify common chloroplast genes have failed, and an atypical plastid genome has been suggested by the presence of abundant plasmid-like DNA in the chloroplasts of several species. Pioneering work of John La Claire and colleagues in the 1990-ies revealed that these structures are single-stranded DNA molecules of 1.5-3.0 kb that fold in a hairpin configuration, and contain putatively transcribed sequences with similarity to chloroplast genes.

In a recent study, we describe intriguing features of the plastid genome of Cladophorales. Through the integration of different DNA sequencing methods, combined with RNA sequencing, we found that chloroplast protein-coding genes are highly expressed and encoded on 1-7 kb linear single-stranded DNA molecules. Due to the wide-spread presence of inverted repeats, these molecules fold into a hairpin configuration. The chloroplast genes are highly divergent from their corresponding orthologs, and display an alternative genetic code. The origin of this highly deviant chloroplast genome likely occurred before the emergence of the Cladophorales, and coincided with an elevated transfer of chloroplast genes to the nucleus. A chloroplast genome that is composed only of linear DNA molecules is unprecedented among eukaryotes and highlights unexpected variation in plastid genome architecture.

cladophorales_cp_DNA
Schematic representation of Boodlea chloroplast genome

Del Cortona A, Leliaert F, Bogaert KA, Turmel M, Boedeker C, Janouškovec J, Lopez-Bautista JM, Verbruggen H, Vandepoele K, De Clerck O. 2017. The plastid genome in Cladophorales green algae is encoded by hairpin chromosomes. Current Biology 24:3771–3782 doi:10.1016/j.cub.2017.11.004.

Smith DR. 2017. Evolution: In Chloroplast Genomes, Anything Goes. Current Biology 27:R1305-R1307 doi:10.1016/j.cub.2017.10.049.

Advertisements

Shedding new light on old algae

The existence of massive cryptic diversity in algae makes linking DNA-based lineages to existing taxa exceedingly difficult. A better integration of historical collections into modern taxonomic research is therefore highly desirable. Using the brown algal genus Lobophora as a test case, we explore the feasibility of linking taxonomic names to clades in modern phylogenies.

vieira_2016
Phylogeny of Lobophora with holotypes indicated in red and epitypes and a neotype in green

Despite Lobophora being a pantropical genus with probably more than 100 species, traditionally only a handful of species have been recognized. In this study we reevaluated the identity of 17 historical taxa thought to belong to Lobophora by attempting DNA amplification of herbarium material as well as specimens recently collected from the type localities (epitypes). In an attempt to assign them to Molecular Operational Taxonomic Units, the obtained sequences were integrated in a global Lobophora phylogeny based upon data derived from more than 650 specimens. Our results indicate that although five sequences were obtained from type specimens, exclusive reliance on information preserved in type specimens is problematic. Epitype material proved a more successful way forward, but this route often comes with a considerable degree of uncertainty, especially in tropical regions where the extent of sympatry among Lobophora lineages is often considerable. More problematic from a broader perspective is the fact that for 35% of historical taxa, either the type could not be traced or permission was not granted to extract DNA from the types. Such a low accessibility rate may reduce our reliance on type material and jeopardize future efforts to integrate historical taxa into a framework of a modern DNA-based taxonomy.

Vieira C, Camacho O, Wynne MJ, Mattio L, Anderson RJ, Bolton JJ, Sansón M, D’Hondt S, Leliaert F, Fredericq S, Payri C, De Clerck O. 2016. Shedding new light on old algae: Matching names and sequences in the brown algal genus Lobophora (Dictyotales, Phaeophyceae). Taxon 65:689-707.

A new class of green algae: Palmophyllophyceae class. nov.

In a recent study, published in Scientific Reports, we provide solid phylogenetic evidence that the enigmatic green seaweed order Palmophyllales together with the unicellular planktonic Prasinococcales (= prasinophyte clade VI) form the deepest-branching clade of the Chlorophyta. Our analyses are based on chloroplast genomic, and nuclear rDNA data.

 

cpDNA_phylogeny_palmophyllophyceae
Phylogeny of the green plants inferred from 71 concatenated plastid genes showing the position of the new class Palmophyllophyceae.

Species of Palmophyllales typically grow in deep marine waters and other shady habitats. The group is characterized by a unique form of multicellularity, forming macroscopic plants that are composed of isolated and undifferentiated spherical cells embedded in an amorphous gelatinous matrix. In 2010, we showed that the Palmophyllales formed an early-diverging lineage of green plants, but the exact phylogenetic position could not be determined with certainty.

Our phylogenetic results improve our understanding of morphological evolution in the green algae. Until present, the early-diverging lineages of the Chlorophyta (the prasinophytes) were only known to comprise unicellular planktonic algae. Our results point to an independent origin of macroscopic growth and multicellularity outside of the core Chlorophyta.

Our study also contributes to a better understanding of plastid genome evolution in green plants. The small, compact and intronless chloroplast genome (cpDNA) of V. peltata shows striking similarities in gene content and organization with the cpDNAs of Prasinococcales and the streptophyte Mesostigma viride, indicating that cpDNA architecture has been extremely well conserved in these deep-branching lineages of green plants.

The phylogenetic distinctness of the Palmophyllales-Prasinococcales clade, characterized by unique ultrastructural features, warrants recognition of a new class of green plants, Palmophyllophyceae class. nov.

 

Leliaert F, Tronholm A, Lemieux C, Turmel M, et al. 2016. Chloroplast phylogenomic analyses reveal the deepest-branching lineage of the Chlorophyta, Palmophyllophyceae class. nov. Scientific Reports 6:25367. article

Leliaert F, Verbruggen H, Zechman FW. 2011. Into the deep: New discoveries at the base of the green plant phylogeny. BioEssays 33:683-692. article

Zechman FW, Verbruggen H, Leliaert F, Ashworth M, et al. 2010. An unrecognized ancient lineage of green plants persists in deep marine waters. Journal of Phycology 46:1288-1295. article

New book

Hot off the press: Part 2/1 of Engler’s Syllabus of Plant Families – Photoautotrophic eukaryotic Algae provides a thorough treatise of the world-wide morphological and molecular diversity of the Glaucocystophyta, Cryptophyta, Dinophyta/Dinozoa, Haptophyta, Heterokontophyta/Ochrophyta, Chlorarachniophyta/Cercozoa, Euglenophyta/Euglenozoa, Chlorophyta, and Streptophyta (p.p.) (The red algae will be treated in Part 2/2).

Part 2/1 of Engler's Syllabus of Plant Families - Photoautotrophic eukaryotic Algae
Part 2/1 of Engler’s Syllabus of Plant Families – Photoautotrophic eukaryotic Algae

Engler’s Syllabus of Plant Families has since its first publication in 1887 aimed to provide a concise survey of the plant kingdom as a whole, presenting all higher systematic units right down to families and genera of plants and fungi. In 1954, more than 60 years ago, the 12th edition of the well-known “Syllabus der Pflanzenfamilien” (“Syllabus of Plant Families”) was published.

Now, the completely restructured and revised 13th edition of Engler’s Syllabus published in 5 parts and in English language for the first time also considers molecular data, which have only recently become available in order to provide an up-to-date evolutionary and systematic overview of the plant groups treated.

Advertisements

Diversity and Evolution of Algae