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

Abstract

Because novel environmental conditions alter the selection pressure on genes or entire subgenomes, adaptive and nonadaptive changes will leave a measurable signature in the genomes, shaping their molecular evolution. We present herein a model of the trajectory of plastid genome evolution under progressively relaxed functional constraints during the transition from autotrophy to a nonphotosynthetic parasitic lifestyle. We show that relaxed purifying selection in all plastid genes is linked to obligate parasitism, characterized by the parasite's dependence on a host to fulfill its life cycle, rather than the loss of photosynthesis. Evolutionary rates and selection pressure coevolve with macrostructural and microstructural changes, the extent of functional reduction, and the establishment of the obligate parasitic lifestyle. Inferred bursts of gene losses coincide with periods of relaxed selection, which are followed by phases of intensified selection and rate deceleration in the retained functional complexes. Our findings suggest that the transition to obligate parasitism relaxes functional constraints on plastid genes in a stepwise manner. During the functional reduction process, the elevation of evolutionary rates reaches several new rate equilibria, possibly relating to the modified protein turnover rates in heterotrophic plastids.parasitism | relaxed selection | evolutionary rates | plastid genomes | Orobanchaceae L ineages change over time as they adapt to new environments. Novel conditions determine the selection in genes or cellular genomes and shape their functional and structural evolution. A system well suited to study the evolution of genomic traits in the context of altered selective regimes that is also tractable technically (due to its small size and high copy number) is the plastid genome (plastome). The prime function of plastids is photosynthesis, but this essential plant organelle also produces starch, lipids, amino acids, sulfur compounds, and pigments. As a result of the strong selective pressure on plastid gene function, plastid genomes have a conserved gene content (1; but see ref.2) and their genes functioning in photosynthesis (atp, ndh, pet, psa, psb, ccsA, cemA, ycf3/4, rbcL), transcription, transcript maturation or translation (rpo, matK, rpl, rps, infA), and other pathways (accD, clpP, ycf1, and ycf2) evolve at lower evolutionary rates than nuclear genes (3). However, in eukaryotic lineages such as Apicomplexan pathogens and nongreen plants that independently made the transition from an autotrophic to a parasitic way of life, plastomes have experienced convergent reductions and accelerations of evolutionary rates (4). Although there is a general understanding of the association of the nonphotosynthetic lifestyle with plastome degradation and rate acceleration, the precise trajectory of plastome evolution under progressively reduced function along the way from being a full autotroph to an obligate nonphotosynthetic parasite remains unknown.Parasitic plants are an excellent system for stu...

Limited mitogenomic degradation in response to a parasitic lifestyle in Orobanchaceae

“…These mutations in the well-conserved ndh genes are likely to lead to a reduction or loss of gene function. This pattern of ndh- specific degradation in the C. paramensis plastome is similar to observations in other Orobanchaceae hemiparasites and some species of Cuscuta (Figure S3)2356. The draft plastome from the hemiparasite Bartsia inaequalis also lacks intact, full-length copies of several ndh genes ( ndhD , ndhE , ndhG , and ndhI ), although it cannot be ruled out that these genes were missed due to the incomplete nature of the genome39.…”

“…The C. paramensis plastome thus provides strong support for the idea that loss of the NAD(P)H dehydrogenase complex is the first step of plastome degradation in the evolution of heterotrophy in plants340. By contrast, the plastomes from nonphotosynthetic holoparasites are generally much more degraded than those of hemiparasites, affecting not only the full spectrum of photosynthetic genes but also many genes not directly related to photosynthesis (Figure S3)2389. Taken together, the collective evidence from available parasitic plastomes suggests a connection between the degree of plastomic degeneration and heterotrophic dependence.…”

“…Like C. paramensis , the obligate hemiparasite S. americana has also lost functionality of several ndh genes (pseudogenization of ndhA , ndhD , ndhF , ndhG , ndhJ and loss of ndhI ), whereas Orobanchaceae holoparasites including Cistanche , Conopholis , and Orobanche have lost ~70% of all of their genes, including nearly all of the photosynthesis-related genes and numerous tRNAs (Figure S3)31011. Similar patterns of minor degeneration in hemiparasites and more extensive degeneration in holoparasites were observed in a recent broad analysis of Orobanchaceae species2.…”

“…Studies of parasitic plant plastomes have established a wide range of genomic degradation, defined primarily by the presence or absence of photosynthetic activity and degree of dependence of the host. For example, in Orobanchaceae, the facultative hemiparasite Triphysaria versicolor has not lost any plastid genes, while the obligate hemiparasites Schwalbea americana and Striga hermonthica (also in Orobanchaceae) exhibit minimal pseudogenization/loss of only a few ndh genes, which encode subunits of the plastid NAD(P)H dehydrogenase complex23. Plastomes of hemiparasitic mistletoes (Viscaceae) are slightly more degraded, exhibiting both a reduction in size (down to 126–147 kb) and the loss of all 11 ndh genes plus a small number (1–6) of non-photosynthetic genes4.…”

“…Other Cuscuta species are clearly non-photosynthetic and their plastomes have lost numerous photosynthetic and non-photosynthetic genes78. Plastomes in the holoparasitic species of Orobanchaceae are also heavily degraded2391011, most extensively in Conopholis americana whose plastome is only 46 kb in size with just 21 intact protein-coding genes. Similar levels of degradation were found in the plastomes of other holoparasites in Cynomoriaceae and Hydnoraceae1213.…”