Complex phylogenetic distribution of a non-canonical genetic code in green algae

Abstract

BackgroundA non-canonical nuclear genetic code, in which TAG and TAA have been reassigned from stop codons to glutamine, has evolved independently in several eukaryotic lineages, including the ulvophycean green algal orders Dasycladales and Cladophorales. To study the phylogenetic distribution of the standard and non-canonical genetic codes, we generated sequence data of a representative set of ulvophycean green algae and used a robust green algal phylogeny to evaluate different evolutionary scenarios that may account for the origin of the non-canonical code.ResultsThis study demonstrates that the Dasycladales and Cladophorales share this alternative genetic code with the related order Trentepohliales and the genus Blastophysa, but not with the Bryopsidales, which is sister to the Dasycladales. This complex phylogenetic distribution whereby all but one representative of a single natural lineage possesses an identical deviant genetic code is unique.ConclusionsWe compare different evolutionary scenarios for the complex phylogenetic distribution of this non-canonical genetic code. A single transition to the non-canonical code followed by a reversal to the canonical code in the Bryopsidales is highly improbable due to the profound genetic changes that coincide with codon reassignment. Multiple independent gains of the non-canonical code, as hypothesized for ciliates, are also unlikely because the same deviant code has evolved in all lineages. Instead we favor a stepwise acquisition model, congruent with the ambiguous intermediate model, whereby the non-canonical code observed in these green algal orders has a single origin. We suggest that the final steps from an ambiguous intermediate situation to a non-canonical code have been completed in the Trentepohliales, Dasycladales, Cladophorales and Blastophysa but not in the Bryopsidales. We hypothesize that in the latter lineage an initial stage characterized by translational ambiguity was not followed by final reassignment of both stop codons to glutamine. Instead the standard code was retained by the disappearance of the ambiguously decoding tRNAs from the genome. We correlate the emergence of a non-canonical genetic code in the Ulvophyceae to their multinucleate nature.

Phylogeny and Molecular Evolution of the Green Algae

“…More recently, a 10-gene phylogenetic analysis recovered the class as a well supported monophyletic group, and confirmed the divergence of two main ulvophycean clades (Cocquyt et al, 2010b). These two discrete clades are also supported by independent molecular data, including the distribution of elongation factor genes and a deviant genetic code Gile et al, 2009;Cocquyt et al, 2010a). The phylogeny of Cocquyt et al (2010b) recovered the Trentepohliales as the sister lineage of the Bryopsidales, Cladophorales, and Dasycladales.…”

“…Early work on cDNA of the nuclear-encoded small subunit of the Rubisco gene showed that the stop codons UAA and UAG were reassigned to code for glutamine in the siphonous dasycladalean green seaweeds Acetabularia and Batophora (Schneider et al, 1989;Schneider & Degroot, 1991). More recently, the evolution of these codon reassignments among the Ulvophyceae was studied in more detail using multi-gene datasets (Gile et al, 2009;Cocquyt et al, 2010a). These studies have shown a complex distribution of the alternative genetic code, the canonical genetic code being used in early-branching Ulvophyceae and the Bryopsidales, and the alternative code being used in Dasycladales, Cladophorales and Trentepohliales (Fig.…”

“…6). Several explanations for the observation that the Bryopsidales, which have the canonical code, are nested in a clade of which all other representatives have the alternative code are compared by Cocquyt et al (2010a). These authors suggest that a stepwise acquisition model involving ambiguous intermediates (Fig.…”

Complex Ancestries of Isoprenoid Synthesis in Dinoflagellates

“…The parasitic chlorophytes Cephaleuros parasitucs and Trentepohlia annulata presented the exception since they use an alternate genetic code (e.g., Cocquyt et al. ) and were translated using the ciliate genetic code.…”

Rewriting the Genetic Code

“…Recent eukaryotic genome/transcriptome analyses identified that ( a ) Pachysolen tannophilus , a yeast species distinct from Candida spp., reassigns CUG to alanine (Ala; 92, 125) (Figure 2); ( b ) diverse single-celled eukaryotes that are nonciliate also reassign stop codons to amino acids (17, 19, 59, 62, 63, 115, 157) (Figure 2); ( c ) not only Gln but also Leu, tyrosine (Tyr), and glutamic acid (Glu) are assigned to UAR [R denotes adenosine (A) and guanine (G)] (45, 134) or to UAG (115) (Figure 2); and ( d ) ciliates Parduczia sp. and Condylostoma magnum and trypanosomatids Blastocrithidia spp.…”