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

Abstract

The plastid genome (plastome) of heterotrophic plants like mycoheterotrophs and parasites shows massive gene losses in consequence to the relaxation of functional constraints on photosynthesis. To understand the patterns of this convergent plastome reduction syndrome in heterotrophic plants, we studied 12 closely related orchids of three different lifeforms from the tribe Neottieae (Orchidaceae). We employ a comparative genomics approach to examine structural and selectional changes in plastomes within Neottieae. Both leafy and leafless heterotrophic species have functionally reduced plastid genome. Our analyses show that genes for the NAD(P)H dehydrogenase complex, the photosystems, and the RNA polymerase have been lost functionally multiple times independently. The physical reduction proceeds in a highly lineage-specific manner, accompanied by structural reconfigurations such as inversions or modifications of the large inverted repeats. Despite significant but minor selectional changes, all retained genes continue to evolve under purifying selection. All leafless Neottia species, including both visibly green and nongreen members, are fully mycoheterotrophic, likely evolved from leafy and partially mycoheterotrophic species. The plastomes of Neottieae span many stages of plastome degradation, including the longest plastome of a mycoheterotroph, providing invaluable insights into the mechanisms of plastome evolution along the transition from autotrophy to full mycoheterotrophy.

On the brink: the highly reduced plastomes of nonphotosynthetic Ericaceae

“…matK is nearly ubiquitous in angiosperm plastomes, with the exception of Cuscuta subgenus Grammica and fully MH monocots, such as Rhizanthella gardneri, Epipogium, and Neottia (McNeal et al, 2009;Delannoy et al, 2011;Logacheva et al, 2011;Schelkunov et al, 2015;Feng et al, 2016). We did observe a truncated version of matK in Monotropsis despite the presence of genes with group IIa introns (rpl2 and rps23).…”

“…Typically, plastomes contain seven group IIA introns, all of which are spliced with the assistance of a plastid intron maturase ( matK ; Vogel et al ., ). matK is nearly ubiquitous in angiosperm plastomes, with the exception of Cuscuta subgenus Grammica and fully MH monocots, such as Rhizanthella gardneri , Epipogium , and Neottia (McNeal et al ., ; Delannoy et al ., ; Logacheva et al ., ; Schelkunov et al ., ; Feng et al ., ). We did observe a truncated version of matK in Monotropsis despite the presence of genes with group IIa introns ( rpl2 and rps23 ).…”

Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication

“…The r8s method was used instead of BEAST because the former has been shown to be effective in recent studies (Carbonell-Caballero et al 2015; de Casas et al 2016; Feng et al 2016; Plazzi et al 2016) and the latter would require much more computational time with this large datasets here. The fossils used here were from a survey of literature and online resources on Paleobiology Database website (https://www.paleobiodb.org/; last accessed November 12, 2016) for the oldest fossil of the corresponding MRCA nodes.…”

Dense infraspecific sampling reveals rapid and independent trajectories of plastome degradation in a heterotrophic orchid complex

“…() reported a difference of 11 063 bp in the plastomes of congeners Epipogium aphyllum (30 650 bp) and E. roseum (19 047 bp), explained by the loss of one copy of the inverted repeat. Comparable length variation is observed among species in a fully mycoheterotrophic clade of Neottia , with plastomes of 110 246 bp in N. listeroides and 83 190 bp in N. acuminata (Feng et al ., ). Extensive variation is also observed among genera of fully mycoheterotrophic Ericaceae (Gruzdev et al ., ; Logacheva et al ., ; Ravin et al ., ; Braukmann et al ., ) and parasitic broomrapes (Cusimano & Wicke, ).…”