title: Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family.
abstract: 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 co-occurrence with those in operons, indicating complex constraints beyond gene function that determine the evolutionary survival time of plastid regions in nonphotosynthetic plants.
authors.affiliation: Department of Systematic and Evolutionary Botany, University of Viena, A-1030 Viena, Austria.
authors.forename: Susann
authors.initials: S
authors.lastname: Wicke
authors.forename: Kai F
authors.initials: KF
authors.lastname: Müller
authors.forename: Claude W
authors.initials: CW
authors.lastname: de Pamphilis
authors.forename: Dietmar
authors.initials: D
authors.lastname: Quandt
authors.forename: Norman J
authors.initials: NJ
authors.lastname: Wickett
authors.forename: Yan
authors.initials: Y
authors.lastname: Zhang
authors.forename: Susanne S
authors.initials: SS
authors.lastname: Renner
authors.forename: Gerald M
authors.initials: GM
authors.lastname: Schneeweiss
mesh_terms: D001482:Base Composition; D001499:Bayes Theorem; D005075:Biological Evolution; D055028:Comparative Genomic Hybridization; D017353:Gene Deletion; D015321:Gene Rearrangement; D020043:Genes, Essential; D054628:Genome, Chloroplast; D018745:Genome, Plant; D008957:Models, Genetic; D016366:Open Reading Frames; D031670:Orobanchaceae / Q000235:genetics* / Q000502:physiology; D010788:Photosynthesis / Q000235:genetics*; D010802:Phylogeny; D020161:Physical Chromosome Mapping; D012091:Repetitive Sequences, Nucleic Acid; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA