Massive intracellular gene transfer during plastid genome reduction in nongreen Orobanchaceae

Abstract

SummaryPlastid genomes (plastomes) of nonphotosynthetic plants experience extensive gene losses and an acceleration of molecular evolutionary rates. Here, we inferred the mechanisms and timing of reductive genome evolution under relaxed selection in the broomrape family (Orobanchaceae).We analyzed the plastomes of several parasites with a major focus on the genus Orobanche using genome-descriptive and Bayesian phylogenetic-comparative methods. Besides this, we scanned the parasites' other cellular genomes to trace the fate of all genes that were purged from their plastomes.Our analyses indicate that the first functional gene losses occurred within 10 Myr of the transition to obligate parasitism in Orobanchaceae, and that the physical plastome reduction proceeds by small deletions that accumulate over time. Evolutionary rate shifts coincide with the genomic reduction process in broomrapes, suggesting that the shift of selectional constraints away from photosynthesis to other molecular processes alters the plastid rate equilibrium. Most of the photosynthesis-related genes or fragments of genes lost from the plastomes of broomrapes have survived in their nuclear or mitochondrial genomes as the results of multiple intracellular transfers and subsequent fragmentation.Our findings indicate that nonessential DNA is eliminated much faster in the plastomes of nonphotosynthetic parasites than in their other cellular genomes.

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

“…We compared nonsynonymous (dN) and synonymous (dS) nucleotide substitution rates of all Orobanchaceae with closely related nonparasites ( Fig. 1), building on phylogenetic relationships established earlier (10,11). In gene-by-gene likelihood ratio tests (LRTs), the facultatively hemiparasitic Triphysaria versicolor shows hardly any significant rate shifts in plastid genes compared with nonparasitic plants (Fig.…”

“…This first phase of selection relaxation is characterized by a steady increase of microstructural changes and the acceleration of dN and dS. Following this episode of selectional shift, evolutionary rates in the plastome evolve at a new equilibrium, perhaps matching the modified transcript and protein requirements (11). This molecular evolutionary regime shift is repeated once selective constraints on plastid proteins (e.g., ATP synthase) that continue to function for a longer period are lost or functionally replaced (functional loss 3 in Fig.…”

“…All components that together explained at least 90% of the variance were used as fixed effects in phylogenetic MCMC-GLMM analysis (as above). To evaluate the time series of genetic changes, we traced dN, dS, and indels on dated phylogenies, which we obtained by using penalized likelihood (48) implemented in ape (45), setting the root age boundary to 51-71 million years ago (11). Details of all coevolutionary analyses are provided in SI Materials and Methods.…”

Chloroplast Genome Evolution in Actinidiaceae: clpP Loss, Heterogenous Divergence and Phylogenomic Practice

“…Selective pressure leads to divergent traits during plant evolution, which may be tracked in chloroplast genomes, for instance, the non-photosynthetic lifestyle of certain plant groups such as Epipogium aphyllum and Epipogium roseum [5], Orobanche [13], and Petrosavia stellaris [55] tends to be associated with the enormously reduced cp genome size. Complete sequencing and comparative analyses here revealed that the Clematoclethra species ( C .…”

“…orchids [8], Campanulaceae [9] and Rafflesiaceae [10]. Additionally, gene transfer between plastome, chondrome and nucleus has also been revealed in plants [11–13]. It has been proven that cp genome structural variations are accompanied by speciation over time, which likely provides evolutionary information [14].…”