Phylogenomics and comparative plastome analysis of mycoheterotrophic plants

Plastid genomes (plastomes) of fully mycoheterotrophic plants (which obtain nutrition from fungi and have lost photosynthesis) may exhibit accelerated substitution rates, gene losses and structural rearrangements compared to their more stable photosynthetic relatives. Distantly related lineages provide independent data points to study plastome degradation. I used Sanger sequencing to assess the utility of three nonphotosynthetic plastid genes in phylogenetic inference of seven monocot families that include mycoheterotrophic taxa. I also assembled full plastome genomes for multiple mycoheterotrophic monocots, a heterotrophic conifer (Parasitaxus, Podocarpaceae) and autotrophic relatives for comparative analysis. Phylogenomic inferences are robust to different likelihood approaches and often extensive gene loss, are generally congruent with the few-gene analyses, and are insensitive to long branches, in contrast to parsimony. Patterns of gene loss and retention are largely in agreement with hypothesized trajectories, starting with plastid NAD(P)H dehydrogenase, followed by the loss of other photosynthesis-related genes, and ending in gradual loss of transcriptional apparatus and other non-photosynthesis related genes. I observed retention (delayed loss?) of genes encoding subunits of plastid-encoded RNA polymerase (Parasitaxus and some species in Petrosavia, Petrosaviaceae), plastid ATP synthase (Petrosavia, perhaps Parasitaxus in modified form) and Rubisco (Petrosavia), consistent with secondary non-photosynthetic functions of the latter two complexes. Some group IIA introns appear to be retained despite the loss of the plastid intron maturase, matK. Retained open reading frames are generally under strong purifying selection in Sciaphila (Triuridaceae). Genome contraction is the major mode of genome rearrangement, with severe reduction seen in some lineages (e.g., Apteria in Burmanniaceae is reduced to ~16 kb). Some mycoheterotrophs are nearly or completely colinear with autotrophic lineages (Geosiris in Iridaceae, at ~123 kb). Others have multiple minor or major rearrangements, which may be unrelated to the presence or absence of an inverted repeat (IR). Four independent IR losses were observed (in Burmanniaceae, Corsiaceae, Petrosaviaceae and Triuridaceae), an extra IR copy evolved in Campylosiphon (Burmanniaceae), and an entire IR re-evolved in Parasitaxus. Shifts in IR boundaries were also found in all mycoheterotrophs. Within-taxon comparisons (e.g., in Corsiaceae and Petrosavia) also underline that idiosyncratic evolutionary changes may occur following each loss of photosynthesis.Science, Faculty ofBotany, Department ofGraduat