Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes

Abstract

Contents 48I.48II.50III.5354References54 Summary We examine recent evidence for ratchet‐like genome degradation in mycoheterotrophs, plants that obtain nutrition from fungi. Initial loss of the NADH dehydrogenase‐like (NDH) complex may often set off an irreversible evolutionary cascade of photosynthetic gene losses. Genes for plastid‐encoded subunits of RNA polymerase and photosynthetic enzymes with secondary functions (Rubisco and ATP synthase) can persist initially, with nonsynchronous and quite broad windows in the relative timing of their loss. Delayed losses of five core nonbioenergetic genes (especially trnE and accD, which respectively code for glutamyl tRNA and a subunit of acetyl‐CoA carboxylase) probably explain long‐term persistence of heterotrophic plastomes. The observed range of changes of mycoheterotroph plastomes is similar to that of holoparasites, although greater diversity of both probably remains to be discovered. These patterns of gene loss/retention can inform research programs on plastome function.

On the brink: the highly reduced plastomes of nonphotosynthetic Ericaceae

“…(), and Graham et al . (), who hypothesize that plastid gene loss in heterotrophic plants happens sequentially, starting with the NAD(P)H complex (ndh genes), followed by photosynthetic genes ( rbcL , psa , psb , pet , ycf3 , cemA , ccsA , and ycf4 genes), plastid‐encoded RNA polymerase ( rpo genes), and ATP synthase ( atp genes). The last genes to be lost include the ribosomal protein genes ( rpl and rps ), ribosomal RNA genes ( rrn ), plastid tRNAs ( trn genes), an initiation factor ( infA ), an intron maturase ( matK ), acetyl CoA‐carboxylase ( accD ), a protease subunit involved in ATP‐dependent degradation of photosynthetic complexes ( clpP ), and two genes involved in a number of cellular process ( ycf1 and ycf2 ).…”

“…By contrast, full heterotrophs rely solely on their hosts to supply their water, fixed carbon, and nutrients. The transition from autotrophy to heterotrophy is associated with drastic changes in morphology (loss/reduction of vegetative organs; Leake, 1994;Manen et al, 2004), physiology (near loss of chlorophyll and high stomatal conductivity; Stewart & Press, 1990;Leake, 1994;Manen et al, 2004), and genome (rampant sequence divergence and loss of genes; McNeal et al, 2007a;Braukmann & Stefanovi c, 2012;Wicke et al, 2016;Graham et al, 2017).…”

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

“…These include overall decreases in genome size, decreases in GC content, increasing frequency of rearrangements, accumulation of indels, losses of introns, etc. (Wicke et al ., , , ; Barrett & Davis, ; Barrett et al ., ; Naumann et al ., ; reviewed in Graham et al ., ).…”

Plastid genomes hit the big time

“…The surest ways to shrink a ptDNA is to ditch photoautotrophy (Figueroa‐Martinez et al ., ; Braukmann et al ., ; Graham et al ., ). Such a switch immediately removes the necessity for maintaining photosynthesis‐related genes in the plastid (and nuclear) genome, allowing them to be purged.…”

“…Plastid genomes in nonphotosynthetic species typically bottom out at c . 34 kb, but some heterotrophic land plants are taking ptDNA contraction to new lows (Braukmann et al ., ; Graham et al ., ). A Cameroonian isolate of the mycoheterotrophic orchid Epipogium roseum has a plastome measuring only 18 339 nt and containing 29 genes (Schelkunov et al ., ).…”