Oral Paper

         Comparative Genomics/Transcriptomics

A novel loss of photosynthesis in fully mycoheterotrophic Afrothismia (Dioscoreales), and its effect on plastid genome evolution

Presenting Author
Nathaniel Klimpert
Description
Mycoheterotrophic plants obtain most or all of their carbon from fungal associates instead of photosynthesis. This transition in trophic mode is associated with at least 50 independent losses of photosynthesis in land plants. These losses provide multiple evolutionary experiments in the convergent, divergent and unique ways in which plastid genomes evolve in heterotrophic lineages. Afrothismia represents one such independent loss in the yam order, Dioscoreales. Comprising up to 23 species, the lineage is endemic to tropical Africa; more than half of the species are endangered or critically endangered. The taxon was recently inferred to be the sister group of Taccaceae and Thismiaceae in Dioscoreales, but has received only limited attention in molecular systematics studies, and to date only nuclear and mitochondrial genes have been recovered from Afrothismia species. Here we sequenced and assembled full plastid genomes of three Afrothismia species to characterize the consequences of photosynthesis loss in the clade. All three plastid genomes have experienced extreme reductions in size and gene content (lacking all photosynthesis-related genes), and represent among the most reduced plastid genomes known (~12–15 kb). These plastomes lack the large inverted repeats typical of most photosynthetic taxa, but are otherwise nearly colinear with photosynthetic relatives, ignoring the gene losses and their substantially reduced intergenic spacer regions. Group IIA cis-spliced introns are retained in two plastid genes despite loss of the matK maturase gene, and a trans-spliced intron is retained in two of three species. All three species retain only 12 of 79 protein-coding genes, with just one of these (accD) involved in a function (fatty-acid biosynthesis) unrelated to protein synthesis. The protein-coding genes display massive rate elevation in phylogenetic analysis; despite this, they are predicted to all be evolving under strong purifying selection. The plastomes retain only two (of four) ribosomal RNA genes (16S and 23S rDNA), and one (of 30) transfer RNA gene (trnfM), implying import of nuclear or mitochondrial homologs for some or all of the missing translation apparatus genes, if plastid translation is functional. The trnE gene, which serves a critical role in heme biosynthesis in most heterotrophic plants in addition to its role in plastid translation, has been lost from the plastid genome, which has not been observed in any other mycoheterotrophic lineage. The plastid protein-coding genes of two species (Afrothismia hydra and A. winkleri) have multiple premature and in-frame TGA stop codons, and consistently use only one type of stop codon (TAA) at the end of genes. This pattern is potentially consistent with a change in the plastid genome genetic code, rather than RNA editing.