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Journal ArticleDOI

Mechanisms of Functional and Physical Genome Reduction in Photosynthetic and Nonphotosynthetic Parasitic Plants of the Broomrape Family

TL;DR: The authors report the complete plastomes of 10 photosynthetic and nonphotosynthetic parasites plus their nonparasitic sister from the broomrape family (Orobanchaceae), finding that the establishment of obligate parasitism triggers the relaxation of selective constraints.
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.
Citations
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Journal ArticleDOI
TL;DR: The mitochondrial genome of an aerobic parasitic plant, the mistletoe Viscum scurruloideum, is presented, which is miniaturized, shows clear signs of rapid and degenerative evolution, and lacks all genes for complex I of the respiratory electron-transfer chain.
Abstract: Despite the enormous diversity among parasitic angiosperms in form and structure, life-history strategies, and plastid genomes, little is known about the diversity of their mitogenomes. We report the sequence of the wonderfully bizarre mitogenome of the hemiparasitic aerial mistletoe Viscum scurruloideum. This genome is only 66 kb in size, making it the smallest known angiosperm mitogenome by a factor of more than three and the smallest land plant mitogenome. Accompanying this size reduction is exceptional reduction of gene content. Much of this reduction arises from the unexpected loss of respiratory complex I (NADH dehydrogenase), universally present in all 300+ other angiosperms examined, where it is encoded by nine mitochondrial and many nuclear nad genes. Loss of complex I in a multicellular organism is unprecedented. We explore the potential relationship between this loss in Viscum and its parasitic lifestyle. Despite its small size, the Viscum mitogenome is unusually rich in recombinationally active repeats, possessing unparalleled levels of predicted sublimons resulting from recombination across short repeats. Many mitochondrial gene products exhibit extraordinary levels of divergence in Viscum, indicative of highly relaxed if not positive selection. In addition, all Viscum mitochondrial protein genes have experienced a dramatic acceleration in synonymous substitution rates, consistent with the hypothesis of genomic streamlining in response to a high mutation rate but completely opposite to the pattern seen for the high-rate but enormous mitogenomes of Silene. In sum, the Viscum mitogenome possesses a unique constellation of extremely unusual features, a subset of which may be related to its parasitic lifestyle.

213 citations

Journal ArticleDOI
TL;DR: The inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastids genome, or if present is found in cryptic form at very low levels.
Abstract: Rafflesia is a genus of holoparasitic plants endemic to Southeast Asia that has lost the ability to undertake photosynthesis. With short-read sequencing technology, we assembled a draft sequence of the mitochondrial genome of Rafflesia lagascae Blanco, a species endemic to the Philippine island of Luzon, with ~350 sequencing depth coverage. Using multiple approaches, however, we were only able to identify small fragments of plastid sequences at low coverage depth (<2) and could not recover any substantial portion of a chloroplast genome. The gene fragments we identified included photosynthesis and energy production genes (atp,ndh,pet,psa,psb,rbcL), ribosomal RNA genes (rrn16,rrn23), ribosomal protein genes (rps7,rps11,rps16), transfer RNA genes, as well as matK,accD,ycf2, and multiple nongenic regions from the inverted repeats. None of the identified plastid gene sequences had intact reading frames. Phylogenetic analysis suggests that ~33% of these remnant plastid genes may have been horizontally transferred from the host plant genus Tetrastigma with the rest having ambiguous phylogenetic positions (<50% bootstrap support), except for psaB that was strongly allied with the plastid homolog in Nicotiana. Our inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches—despite success in identifying and developing a draft assembly of the much larger mitochondrial genome—suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastid genome, or if presen ti s found in cryptic form at very low levels.

164 citations


Cites background from "Mechanisms of Functional and Physic..."

  • ...6-kb plastome of Conopholis americana (Orobanchaceae) is the smallest published plastid genome to date (Colwell 1994; Wicke et al. 2013)....

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  • ...The 45.6-kb plastome of Conopholis americana (Orobanchaceae) is the smallest published plastid genome to date (Colwell 1994; Wicke et al. 2013)....

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  • ...The evolution of the chloroplast genome in parasitic plants, particularly nonphotosynthetic holoparasites, can lead to significantly reconfigured plastomes (Wicke et al. 2013)....

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  • ...The fates of other essential plastid genes, such as the clpP and ycf2 loci (Wicke et al. 2013), are unknown, and must await detailed genomic and biochemical studies on these parasitic plant species....

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  • ...In these plants many photosystem and energy production genes are lost from the plastome (Krause 2008; Li et al. 2013; Wicke et al. 2013)....

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Journal ArticleDOI
TL;DR: This study represents the most comprehensively sampled matrix of plastomes assembled for monocot angiosperms, providing genome-scale support for phylogenetic relationships of monocots, and lays the phylogenetic groundwork for comparative analyses of the drivers and correlates of such drastic differences in substitution rates across a diverse and significant clade.
Abstract: Despite progress based on multilocus, phylogenetic studies of the palms (order Arecales, family Arecaceae), uncertainty remains in resolution/support among major clades and for the placement of the palms among the commelinid monocots. Palms and related commelinids represent a classic case of substitution rate heterogeneity that has not been investigated in the genomic era. To address questions of relationships, support and rate variation among palms and commelinid relatives, 39 plastomes representing the palms and related family Dasypogonaceae were generated via genome skimming and integrated within a monocot-wide matrix for phylogenetic and molecular evolutionary analyses. Support was strong for 'deep' relationships among the commelinid orders, among the five palm subfamilies, and among tribes of the subfamily Coryphoideae. Additionally, there was extreme heterogeneity in the plastid substitution rates across the commelinid orders indicated by model based analyses, with c. 22 rate shifts, and significant departure from a global clock. To date, this study represents the most comprehensively sampled matrix of plastomes assembled for monocot angiosperms, providing genome-scale support for phylogenetic relationships of monocot angiosperms, and lays the phylogenetic groundwork for comparative analyses of the drivers and correlates of such drastic differences in substitution rates across a diverse and significant clade.

163 citations

Book ChapterDOI
TL;DR: This chapter presents an overview of some of the seminal and contemporary research that has contributed to the current understanding of plastome evolution and attempt to highlight the relationship between evolutionary mechanisms and tools ofplastid genetic engineering.
Abstract: The plastid genome (plastome) has proved a valuable source of data for evaluating evolutionary relationships among angiosperms. Through basic and applied approaches, plastid transformation technology offers the potential to understand and improve plant productivity, providing food, fiber, energy and medicines to meet the needs of a burgeoning global population. The growing genomic resources available to both phylogenetic and biotechnological investigations are allowing novel insights and expanding the scope of plastome research to encompass new species. In this chapter we present an overview of some of the seminal and contemporary research that has contributed to our current understanding of plastome evolution and attempt to highlight the relationship between evolutionary mechanisms and tools of plastid genetic engineering.

160 citations

Journal ArticleDOI
TL;DR: Corallorhiza spans the early stages of a general model of plastome degradation and has added critical insight for understanding the process of plastsome evolution in heterotrophic angiosperms.
Abstract: Parasitic organisms exemplify morphological and genomic reduction. Some heterotrophic, parasitic plants harbor drastically reduced and degraded plastid genomes resulting from relaxed selective pressure on photosynthetic function. However, few studies have addressed the initial stages of plastome degradation in groups containing both photosynthetic and nonphotosynthetic species. Corallorhiza is a genus of leafless, heterotrophic orchids that contains both green, photosynthetic species and nongreen, putatively nonphotosynthetic species, and represents an ideal system in which to assess the beginning of the transition to a "minimal plastome." Complete plastomes were generated for nine taxa of Corallorhiza using Illumina paired-end sequencing of genomic DNA to assess the degree of degradation among taxa, and for comparison with a general model of degradation among angiosperms. Quantification of total chlorophyll suggests that nongreen Corallorhiza still produce chlorophyll, but at 10-fold lower concentrations than green congeners. Complete plastomes and partial nuclear rDNA cistrons yielded a fully resolved tree for Corallorhiza, with at least two independent losses of photosynthesis, evidenced by gene deletions and pseudogenes in Co. striata and nongreen Co. maculata. All Corallorhiza show some evidence of degradation in genes of the NAD(P)H dehydrogenase complex. Among genes with open reading frames, photosynthesis-related genes displayed evidence of neutral evolution in nongreen Corallorhiza, whereas genes of the ATP synthase complex displayed some evidence of positive selection in these same groups, though for reasons unknown. Corallorhiza spans the early stages of a general model of plastome degradation and has added critical insight for understanding the process of plastome evolution in heterotrophic angiosperms.

141 citations


Cites background from "Mechanisms of Functional and Physic..."

  • ...…Chang et al. 2006; Funk et al. 2007; McNeal et al. 2007; Braukmann et al. 2009; Blazier et al. 2011; Braukmann and Stefanovic 2012; Braukmann et al. 2013; Iles et al. 2013; Peredo et al. 2013; Wicke et al. 2013), including some of the leafy, photosynthetic orchid plastomes included in figure 3....

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  • ...Chlorophyll has been detected in other strictly heterotrophic plants (Cummings and Welschmeyer 1998), including members of Orobanchaceae and the monotropoid Ericaceae....

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  • ...3 and references therein, including discussion in Wicke et al. 2013)....

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  • ...Examples of heterotrophic taxa for which plastome evolution has been studied include various Orobanchaceae (e.g., Epifagus, Wolfe et al. 1992; Conopholis, Wimpee et al. 1991; Hyobanche/Harveya, Wolfe and dePamphilis 1998; Randle and Wolfe 2005; family-wide representative genera, Wicke et al. 2013), Convolvulaceae (Cuscuta, Funk et al. 2007; McNeal et al. 2007; Braukmann et al. 2013), monotropoid Ericaceae (Braukmann and Stefanovic 2012; Broe M and Freudenstein J, personal communication), and monocots including Orchidaceae (Delannoy et al. 2011; Logacheva et al. 2011, 2014; Barrett and Davis 2012)....

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  • ...Orobanchaceae range from 38.08% GC in the hemiparasitic Schwalbea to 31.09% in the holoparasitic Phelipanche purpurea....

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References
More filters
Journal ArticleDOI
TL;DR: The program MODELTEST uses log likelihood scores to establish the model of DNA evolution that best fits the data.
Abstract: Summary: The program MODELTEST uses log likelihood scores to establish the model of DNA evolution that best fits the data. Availability: The MODELTEST package, including the source code and some documentation is available at http://bioag.byu.edu/zoology/crandall―lab/modeltest.html. Contact: dp47@email.byu.edu.

20,105 citations

Journal ArticleDOI
25 Jun 2010-PLOS ONE
TL;DR: A new method to align two or more genomes that have undergone rearrangements due to recombination and substantial amounts of segmental gain and loss is described, demonstrating high accuracy in situations where genomes have undergone biologically feasible amounts of genome rearrangement, segmental loss and loss.
Abstract: Background Multiple genome alignment remains a challenging problem. Effects of recombination including rearrangement, segmental duplication, gain, and loss can create a mosaic pattern of homology even among closely related organisms.

3,302 citations


"Mechanisms of Functional and Physic..." refers methods in this paper

  • ...1 (Darling et al., 2010) using a seed weight of 21 and a custom gap open penalty of 2200 to account for (relatively) small gaps....

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  • ...To circumvent this problem, we determined the maximum amount of locally colinear blocks among all sequenced Orobanchaceae genomes with progressive Mauve 2.3.1 (Darling et al., 2010) using a seed weight of 21 and a custom gap open penalty of 2200 to account for (relatively) small gaps....

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Journal ArticleDOI
TL;DR: The Dual Organellar GenoMe Annotator (DOGMA) automates the annotation of organellar genomes and allows the use of BLAST searches against a custom database, and conservation of basepairing in the secondary structure of animal mitochondrial tRNAs to identify and annotate genes.
Abstract: Summary: The Dual Organellar GenoMe Annotator (DOGMA) automates the annotation of organellar (plant chloroplast and animal mitochondrial) genomes. It is a Web-based package that allows the use of BLAST searches against a custom database, and conservation of basepairing in the secondary structure of animal mitochondrial tRNAs to identify and annotate genes. DOGMA provides a graphical user interface for viewing and editing annotations. Annotations are stored on our password-protected server to enable repeated sessions of working on the same genome. Finished annotations can be extracted for direct submission to GenBank. Availability: http://phylocluster.biosci.utexas.edu/dogma/ Supplementary information: Detailed documentation and tutorials for annotating both animal mitochondrial and plant chloroplast genomes can be found on the DOGMA home page.

2,754 citations


"Mechanisms of Functional and Physic..." refers methods in this paper

  • ...CAP3 contigs were preannotated using DOGMA, manually joined, and checked for incongruences with MIRA contigs....

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  • ...Contigs were preannotated using DOGMA (Wyman et al., 2004) and then overlapped manually....

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  • ...Annotation of finished plastid chromosome sequences was performed using DOGMAwith somemanual refinement....

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  • ...Positive matches were extracted and postassembled gene by gene with high stringency in SeqMan I. Contigs were preannotated using DOGMA (Wyman et al., 2004) and then overlapped manually....

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Journal ArticleDOI
TL;DR: Five sequences coding for proteins homologous to components of the respiratory‐chain NADH dehydrogenase from human mitochondria have been found and sequence and expression analyses indicate both prokaryotic and eukaryotic features of the chloroplast genes.
Abstract: The complete nucleotide sequence (155 844 bp) of tobacco (Nicotiana tabacum var. Bright Yellow 4) chloroplast DNA has been determined. It contains two copies of an identical 25 339 bp inverted repeat, which are separated by a 86 684 bp and a 18 482 bp single-copy region. The genes for 4 different rRNAs, 30 different tRNAs, 39 different proteins and 11 other predicted protein coding genes have been located. Among them, 15 genes contain introns. Blot hybridization revealed that all rRNA and tRNA genes and 27 protein genes so far analysed are transcribed in the chloroplast and that primary transcripts of the split genes hitherto examined are spliced. Five sequences coding for proteins homologous to components of the respiratory-chain NADH dehydrogenase from human mitochondria have been found. The 30 tRNAs predicted from their genes are sufficient to read all codons if the ;two out of three' and ;U:N wobble' mechanisms operate in the chloroplast. Two sequences which autonomously replicate in yeast have also been mapped. The sequence and expression analyses indicate both prokaryotic and eukaryotic features of the chloroplast genes.

2,184 citations

Journal ArticleDOI
TL;DR: A new statistical method is presented for analysing the relationship between two discrete characters that are measured across a group of hierarchically evolved species or populations and assessing whether a pattern of association across the group is evidence for correlated evolutionary change in the two characters.
Abstract: I present a new statistical method for analysing the relationship between two discrete characters that are measured across a group of hierarchically evolved species or populations. The method assesses whether a pattern of association across the group is evidence for correlated evolutionary change in the two characters. The method takes into account information on the lengths of the branches of phylogenetic trees, develops estimates of the rates of change of the discrete characters, and tests the hypothesis of correlated evolution without relying upon reconstructions of the ancestral character states. A likelihood ratio test statistic is used to discriminate between two models that are fitted to the data: one allowing only for independent evolution of the two characters, the other allowing for correlated evolution. Tests of specific directional hypotheses can also be made. The method is illustrated with an application to the Hominoidea.

1,643 citations


"Mechanisms of Functional and Physic..." refers methods in this paper

  • ...effect of branch lengths upon trait changes (Pagel, 1994); significance was again assessed by a LRT....

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  • ...…versus punctuated) by constraining the BayesTraits-specific parameter kappa (k) to k = 0 to measure the effect of branch lengths upon trait changes (Pagel, 1994); significance was again assessed by a LRT. Correlation of traits was further tested by constraining the covariance to zero and then…...

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