On the brink: the highly reduced plastomes of nonphotosynthetic Ericaceae

Abstract

Ericaceae (the heather family) is a large and diverse group of plants that forms elaborate symbiotic relationships with mycorrhizal fungi, and includes several nonphotosynthetic lineages. Using an extensive sample of fully mycoheterotrophic (MH) species, we explored inter- and intraspecific variation as well as selective constraints acting on the plastomes of these unusual plants. The plastomes of seven MH genera were analysed in a phylogenetic context with two geographically disparate individuals sequenced for Allotropa, Monotropa, and Pityopus. The plastomes of nonphotosynthetic Ericaceae are highly reduced in size (c. 33-41 kbp) and content, having lost all photosynthesis-related genes, and are reduced to encoding housekeeping genes as well as a protease subunit (clpP)-like and acetyl-CoA carboxylase subunit D (accD)-like open reading frames. Despite an increase in the rate of their nucleotide substitutions, the remaining protein-coding genes are typically under purifying selection in full MHs. We also identified ribosomal proteins under relaxed or neutral selection. These plastomes also exhibit striking structural rearrangements. Intraspecific variation within MH Ericaceae ranges from a few differences (Allotropa) to extensive population divergences (Monotropa, Hypopitys), which indicates that cryptic speciation may be occurring in several lineages. The pattern of gene loss within fully MH Ericaceae plastomes suggests an advanced state of degradation.

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

“…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, ). The range in plastome length observed here is not caused by the loss of an inverted repeat copy, but by differential rates of deletion in the bentleyi – involuta clade vs C .…”

“…These have been of great importance in the elucidation of the large-scale patterns of plastome evolution as a result of relaxed purifying selective constraints on photosynthesis, revealing convergent patterns of gene degradation (Wolfe et al, 1992;Funk et al, 2007;McNeal et al, 2007;Wickett et al, 2008;Delannoy et al, 2011;Logacheva et al, 2011;Barrett & Davis, 2012;Li et al, 2013;Lam et al, 2015;Bellot & Renner, 2016;Lim et al, 2016;Naumann et al, 2016;Roquet et al, 2016;Samigullin et al, 2016). Recently, phylogenetic, comparative approaches have been taken across families, tribes or genera containing parasites, representing a shift away from single-plastome studies (Wicke et al, 2013;Barrett et al, 2014;Feng et al, 2016;Braukmann et al, 2017). Such studies allow powerful phylogenetic comparisons of plastid genome evolution within related lineages.…”

“…Yet, no research has focused on the infraspecific level. Such studies would be highly informative on fine-scale mutational processes that ultimately result in the drastic changes observed at higher taxonomic levels, such as family or genus, and their timing (Wicke et al, 2013Barrett et al, 2014;Feng et al, 2016;Braukmann et al, 2017). Comparisons of plastid genome evolution at higher taxonomic levels (e.g.…”

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 ., ).…”