Alternative translation initiation codons for the plastid maturase MatK: unraveling the pseudogene misconception in the Orchidaceae

Abstract

BackgroundThe plastid maturase MatK has been implicated as a possible model for the evolutionary “missing link” between prokaryotic and eukaryotic splicing machinery. This evolutionary implication has sparked investigations concerning the function of this unusual maturase. Intron targets of MatK activity suggest that this is an essential enzyme for plastid function. The matK gene, however, is described as a pseudogene in many photosynthetic orchid species due to presence of premature stop codons in translations, and its high rate of nucleotide and amino acid substitution.ResultsSequence analysis of the matK gene from orchids identified an out-of-frame alternative AUG initiation codon upstream from the consensus initiation codon used for translation in other angiosperms. We demonstrate translation from the alternative initiation codon generates a conserved MatK reading frame. We confirm that MatK protein is expressed and functions in sample orchids currently described as having a matK pseudogene using immunodetection and reverse-transcription methods. We demonstrate using phylogenetic analysis that this alternative initiation codon emerged de novo within the Orchidaceae, with several reversal events at the basal lineage and deep in orchid history.ConclusionThese findings suggest a novel evolutionary shift for expression of matK in the Orchidaceae and support the function of MatK as a group II intron maturase in the plastid genome of land plants including the orchids.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0491-1) contains supplementary material, which is available to authorized users.

Lineage-Specific Reductions of Plastid Genomes in an Orchid Tribe with Partially and Fully Mycoheterotrophic Species

“…matK ). The latter has been shown recently to be expressed in Neottieae ( Barthet et al 2015 ), but our data indicate that some of the mycoheterotrophs may utilize an alternative start codon. The gene clpP encoding a subunit of the Clp protease), which is retained also in most other nonphotosynthetic lineages except for Apodanthaceae ( Bellot and Renner 2015 ), may produce a protein that is ten amino acids shorter in the three leafless Neottia species than in other Neottieae ( fig.…”

DNA barcoding of tuberous Orchidoideae: a resource for identification of orchids used in Salep

“…Mat K had the lowest amplification success, and it has been shown that this locus cannot be amplified with ‘universal’ orchid primers due to the presence of alternative translation initiation codons in orchids (Barthet et al . ), and therefore requires ‘case by case’ optimization for each genus.…”

“…Sequencing success for nrITS might be affected by fungal contamination during the drying process and orchid mycorrhizal associations producing a mix of plant and fungal nrITS sequences. MatK had the lowest amplification success, and it has been shown that this locus cannot be amplified with 'universal' orchid primers due to the presence of alternative translation initiation codons in orchids (Barthet et al 2015), and therefore requires 'case by case' optimization for each genus.…”

Phylogenetic analysis of Andinia (Pleurothallidinae; Orchidaceae) and a systematic re-circumscription of the genus

“…The aligned matK matrix, which consisted of 53 taxa with 821 positions, was analyzed by MP and ML in MEGA 6 with 1,000 bootstrap replicates. Plastid matK sequences were analyzed as both coding and non-coding sequence, since there is still some debate as to whether matK is a pseudogene in Orchidaceae (Barthet et al 2015).…”