This review bridges functional and evolutionary aspects of plastid chromosome architecture in land plants and their putative ancestors. We provide an overview on the structure and composition of the plastid genome of land plants as well as the functions of its genes in an explicit phylogenetic and evolutionary context. We will discuss the architecture of land plant plastid chromosomes, including gene content and synteny across land plants. Moreover, we will explore the functions and roles of plastid encoded genes in metabolism and their evolutionary importance regarding gene retention and conservation. We suggest that the slow mode at which the plastome typically evolves is likely to be influenced by a combination of different molecular mechanisms. These include the organization of plastid genes in operons, the usually uniparental mode of plastid inheritance, the activity of highly effective repair mechanisms as well as the rarity of plastid fusion. Nevertheless, structurally rearranged plastomes can be found in several unrelated lineages (e.g. ferns, Pinaceae, multiple angiosperm families). Rearrangements and gene losses seem to correlate with an unusual mode of plastid transmission, abundance of repeats, or a heterotrophic lifestyle (parasites or myco-heterotrophs). While only a few functional gene gains and more frequent gene losses have been inferred for land plants, the plastid Ndh complex is one example of multiple independent gene losses and will be discussed in detail. Patterns of ndh-gene loss and functional analyses indicate that these losses are usually found in plant groups with a certain degree of heterotrophy, might rendering plastid encoded Ndh1 subunits dispensable.
(G.M.S.).Nonphotosynthetic plants possess strongly reconfigured plastomes attributable to convergent losses of photosynthesis and housekeeping genes, making them excellent systems for studying genome evolution under relaxed selective pressures. We report the complete plastomes of 10 photosynthetic and nonphotosynthetic parasites plus their nonparasitic sister from the broomrape family (Orobanchaceae). By reconstructing the history of gene losses and genome reconfigurations, we find that the establishment of obligate parasitism triggers the relaxation of selective constraints. Partly because of independent losses of one inverted repeat region, Orobanchaceae plastomes vary 3.5-fold in size, with 45 kb in American squawroot (Conopholis americana) representing the smallest plastome reported from land plants. Of the 42 to 74 retained unique genes, only 16 protein genes, 15 tRNAs, and four rRNAs are commonly found. Several holoparasites retain ATP synthase genes with intact open reading frames, suggesting a prolonged function in these plants. The loss of photosynthesis alters the chromosomal architecture in that recombinogenic factors accumulate, fostering large-scale chromosomal rearrangements as functional reduction proceeds. The retention of DNA fragments is strongly influenced by both their proximity to genes under selection and the cooccurrence with those in operons, indicating complex constraints beyond gene function that determine the evolutionary survival time of plastid regions in nonphotosynthetic plants.
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...
The Convention on Biological Diversity (CBD) aims at the conservation of all three levels of biodiversity, that is, ecosystems, species and genes. Genetic diversity represents evolutionary potential and is important for ecosystem functioning. Unfortunately, genetic diversity in natural populations is hardly considered in conservation strategies because it is difficult to measure and has been hypothesised to co-vary with species richness. This means that species richness is taken as a surrogate of genetic diversity in conservation planning, though their relationship has not been properly evaluated. We tested whether the genetic and species levels of biodiversity co-vary, using a large-scale and multi-species approach. We chose the high-mountain flora of the Alps and the Carpathians as study systems and demonstrate that species richness and genetic diversity are not correlated. Species richness thus cannot act as a surrogate for genetic diversity. Our results have important consequences for implementing the CBD when designing conservation strategies.
Background and AimsThe spatial distribution of cytotypes can provide valuable insights into evolutionary patterns of polyploid complexes. In a previous study the macro-scale distribution of the three main cytotypes in Senecio carniolicus (Asteraceae) within the Eastern Alps was characterized. Employing a roughly 12-fold extended sampling, the present study focuses on unravelling patterns of cytotype distribution on the meso- and microscale and on correlating those with ecological properties of the growing sites.MethodsDAPI flow cytometry of dried samples was used to determine DNA ploidy level in 5033 individuals from 100 populations spread over the entire Eastern Alpine distribution area of S. carniolicus. Descriptors of microhabitats as well as spatial data were recorded in the field, and analysed with a mixed-effects ANOVA.Key ResultsExtensive variation in DNA ploidy levels (2x, 3x, 4x, 5x, 6x, 7x, 8x, 9x) was detected. Of the main cytotypes, diploids and hexaploids were widespread and had strongly overlapping distributions resulting in the frequent occurrence of cytotype mixtures (half of the investigated populations), whereas tetraploids were disjunctly distributed and occurred in the south-west and the east of the species' distribution area. In spite of the frequent co-occurrence of cytotypes, only 1 % of the samples belonged to secondary cytotypes (3x, 5x, 7x, 8x, 9x). Diploids, tetraploids and hexaploids were altitudinally segregated, but with broad overlap. Similarly, highly significant differences in vegetation and rock cover as well as microhabitat exposure were found between the main cytotypes.ConclusionsSenecio carniolicus shows a remarkable diversity of cytotypes. The distribution of the three main cytotypes (2x, 4x, 6x) has been shaped by Pleistocene glaciations to different extents. Whereas tetraploids are nearly entirely restricted to refugia, hexaploids colonized areas that were extensively glaciated. Diploid and hexaploid individuals often co-occur in mixed populations, where they are spatially and ecologically segregated at both the meso-scale (altitudinal differentiation, exposure of the growing site) and the micro-scale (cover of vegetation and bare rock). With regard to the ecological parameters investigated, the tetraploid cytotype occupies an intermediate position. The rareness of secondary cytotypes suggests the presence of strong pre- or post-zygotic mating barriers.
Conservation biology aims at identifying areas of rich biodiversity. Currently recognized global biodiversity hotspots are spatially too coarse for conservation management and identification of hotspots at a finer scale is needed. This might be achieved by identification of areas of endemism. Here, we identify areas of endemism in Iran, a major component of the Irano-Anatolian biodiversity hotspot, and address their ecological correlates. Using the extremely diverse sunflower family (Asteraceae) as our model system, five consensus areas of endemism were identified using the approach of endemicity analysis. Both endemic richness and degree of endemicity were positively related to topographic complexity and elevational range. The proportion of endemic taxa at a certain elevation (percent endemism) was not congruent with the proportion of total surface area at this elevation, but was higher in mountain ranges. While the distribution of endemic richness (i.e., number of endemic taxa) along an elevational gradient was hump-shaped peaking at mid-elevations, the percentage of endemism gradually increased with elevation. Patterns of endemic richness as well as areas of endemism identify mountain ranges as main centres of endemism, which is likely due to high environmental heterogeneity and strong geographic isolation among and within mountain ranges. The herein identified areas can form the basis for defining areas with conservation priority in this global biodiversity hotspot.
Polyploidy, the possession of more than 2 complete genomes, is a major force in plant evolution known to affect the genetic and genomic constitution and the phenotype of an organism, which will have consequences for its ecology and geography as well as for lineage diversification and speciation. In this review, we discuss phylogenetic patterns in the incidence of polyploidy including possible underlying causes, the role of polyploidy for diversification, the effects of polyploidy on geographical and ecological patterns, and putative underlying mechanisms as well as chromosome evolution and evolution of repetitive DNA following polyploidization. Spurred by technological advances, a lot has been learned about these aspects both in model and increasingly also in nonmodel species. Despite this enormous progress, long-standing questions about polyploidy still cannot be unambiguously answered, due to frequently idiosyncratic outcomes and insufficient integration of different organizational levels (from genes to ecology), but likely this will change in the near future. See also the sister article focusing on animals by Choleva and Janko in this themed issue.
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