[Show abstract][Hide abstract] ABSTRACT: Plastid genomes of photosynthetic flowering plants are usually highly conserved in both structure and gene content. However, the plastomes of parasitic and mycoheterotrophic plants may be released from selective constraint due to the reduction or loss of photosynthetic ability. Here we present the greatly reduced and highly divergent, yet functional, plastome of the nonphotosynthetic holoparasite Hydnora visseri (Hydnoraceae, Piperales). The plastome is 27 kb in length, with 24 genes encoding ribosomal proteins, ribosomal RNAs, tRNAs and a few non-bioenergetic genes, but no genes related to photosynthesis. The inverted repeat and the small single copy region are only ~1.5 kb, and intergenic regions have been drastically reduced. Despite extreme reduction, gene order and orientation are highly similar to the plastome of Piper cenocladum, a related photosynthetic plant in Piperales. Gene sequences in Hydnora are highly divergent and several complementary approaches using the highest possible sensitivity were required for identification and annotation of this plastome. Active transcription is detected for all of the protein coding genes in the plastid genome, and one of two introns is appropriately spliced out of rps12 transcripts. The whole genome shotgun read depth is 1,400X coverage for the plastome, while the mitochondrial genome is covered at 40X and the nuclear genome at 2X. Despite the extreme reduction of the genome and high sequence divergence, the presence of syntenic, long transcriptionally-active open reading frames with distant similarity to other plastid genomes and a high plastome stoichiometry relative to the mitochondrial and nuclear genomes suggests that the plastome remains functional in Hydnora visseri. A four stage model of gene reduction, including the potential for complete plastome loss, is proposed to account for the range of plastid genomes in nonphotosynthetic plants.
Full-text · Article · Jan 2016 · Genome Biology and Evolution
[Show abstract][Hide abstract] ABSTRACT: Whereas de novo assemblies of RNA-Seq data are being published for a growing number of species across the tree of life, there are currently no broadly accepted methods for evaluating such assemblies. Here we present a detailed comparison of 99 transcriptome assemblies, generated with 6 de novo assemblers including CLC, Trinity, SOAP, Oases, ABySS and NextGENe. Controlled analyses of de novo assemblies for Arabidopsis thaliana and Oryza sativa transcriptomes provide new insights into the strengths and limitations of transcriptome assembly strategies. We find that the leading assemblers generate reassuringly accurate assemblies for the majority of transcripts. At the same time, we find a propensity for assemblers to fail to fully assemble highly expressed genes. Surprisingly, the instance of true chimeric assemblies is very low for all assemblers. Normalized libraries are reduced in highly abundant transcripts, but they also lack 1000s of low abundance transcripts. We conclude that the quality of de novo transcriptome assemblies is best assessed through consideration of a combination of metrics: 1) proportion of reads mapping to an assembly 2) recovery of conserved, widely expressed genes, 3) N50 length statistics, and 4) the total number of unigenes. We provide benchmark Illumina transcriptome data and introduce SCERNA, a broadly applicable modular protocol for de novo assembly improvement. Finally, our de novo assembly of the Arabidopsis leaf transcriptome revealed ~20 putative Arabidopsis genes lacking in the current annotation.
[Show abstract][Hide abstract] ABSTRACT: Coevolutionary interactions are thought to have spurred the evolution of key innovations and driven the diversification of much of life on Earth. However, the genetic and evolutionary basis of the innovations that facilitate such interactions remains poorly understood. We examined the coevolutionary interactions between plants (Brassicales) and butterflies (Pieridae), and uncovered evidence for an escalating evolutionary arms-race. Although gradual changes in trait complexity appear to have been facilitated by allelic turnover, key innovations are associated with gene and genome duplications. Furthermore, we show that the origins of both chemical defenses and of molecular counter adaptations were associated with shifts in diversification rates during the arms-race. These findings provide an important connection between the origins of biodiversity, coevolution, and the role of gene and genome duplications as a substrate for novel traits.
Full-text · Article · Jun 2015 · Proceedings of the National Academy of Sciences
[Show abstract][Hide abstract] ABSTRACT: Strigolactones are plant hormones with multiple functions, including regulating various aspects of plant architecture such as shoot branching, facilitating the colonization of plant roots by arbuscu-lar mycorrhizal fungi, and acting as seed germination stimulants for certain parasitic plants of the family Orobanchaceae. The obligate parasitic species Phelipanche aegyptiaca and Striga hermon-thica require strigolactones for germination, while the facultative parasite Triphysaria versicolor does not. It has been hypothesized that P. aegyptiaca and S. hermonthica would have undergone evolutionary loss of strigolactone biosynthesis as a part of their mechanism to enable specific detection of exogenous strigolactones. We analyzed the transcriptomes of P. aegyptiaca, S. hermon-thica and T. versicolor and identified genes known to act in strigolactone synthesis (D27, CCD7, CCD8, and MAX1), perception (MAX2 and D14) and transport (PDR12). These genes were then analyzed to assess likelihood of function. Transcripts of all strigolactone-related genes were found M. Das et al. 1152 in P. aegyptiaca and S. hermonthica, and evidence points to their encoding functional proteins. Gene open reading frames were consistent with homologs from Arabidopsis and other strigolac-tone-producing plants, and all genes were expressed in parasite tissues. In general, the genes related to strigolactone synthesis and perception appeared to be evolving under codon-based selective constraints in strigolactone-dependent species. Bioassays of S. hermonthica root extracts indicated the presence of strigolactone class stimulants on germination of P. aegyptiaca seeds. Tak-en together, these results indicate that Phelipanche aegyptiaca and S. hermonthica have retained functional genes involved in strigolactone biosynthesis, suggesting that the parasites use both en-dogenous and exogenous strigolactones and have mechanisms to differentiate the two.
Full-text · Article · Apr 2015 · American Journal of Plant Sciences
[Show abstract][Hide abstract] ABSTRACT: Reconstructing the origin and evolution of land plants and their
algal relatives is a fundamental problem in plant phylogenetics, and
is essential for understanding how critical adaptations arose, including
the embryo, vascular tissue, seeds, and flowers. Despite
advances inmolecular systematics, some hypotheses of relationships
remain weakly resolved. Inferring deep phylogenies with bouts of
rapid diversification can be problematic; however, genome-scale
data should significantly increase the number of informative characters
for analyses. Recent phylogenomic reconstructions focused on
the major divergences of plants have resulted in promising but inconsistent
results. One limitation is sparse taxon sampling, likely
resulting from the difficulty and cost of data generation. To address
this limitation, transcriptome data for 92 streptophyte taxa were
generated and analyzed along with 11 published plant genome
sequences. Phylogenetic reconstructions were conducted using up
to 852 nuclear genes and 1,701,170 aligned sites. Sixty-nine analyses
were performed to test the robustness of phylogenetic inferences to
permutations of the datamatrix or to phylogeneticmethod, including
supermatrix, supertree, and coalescent-based approaches, maximumlikelihood
and Bayesian methods, partitioned and unpartitioned analyses,
and amino acid versus DNA alignments. Among other
results, we find robust support for a sister-group relationship
between land plants and one group of streptophyte green algae,
the Zygnematophyceae. Strong and robust support for a
clade comprising liverworts and mosses is inconsistent with a
widely accepted view of early land plant evolution, and suggests
that phylogenetic hypotheses used to understand the evolution of
fundamental plant traits should be reevaluated.
Full-text · Article · Oct 2014 · Proceedings of the National Academy of Sciences
[Show abstract][Hide abstract] ABSTRACT: Movement of RNAs between cells of a single plant is well documented, but cross-species RNA transfer is largely unexplored.
Cuscuta pentagona (dodder) is a parasitic plant that forms symplastic connections with its hosts and takes up host messenger RNAs (mRNAs).
We sequenced transcriptomes of Cuscuta growing on Arabidopsis and tomato hosts to characterize mRNA transfer between species and found that mRNAs move in high numbers and in a bidirectional
manner. The mobile transcripts represented thousands of different genes, and nearly half the expressed transcriptome of Arabidopsis was identified in Cuscuta. These findings demonstrate that parasitic plants can exchange large proportions of their transcriptomes with hosts, providing
potential mechanisms for RNA-based interactions between species and horizontal gene transfer.
[Show abstract][Hide abstract] ABSTRACT: Petunia possesses self-incompatibility, by which pistils reject self-pollen but accept non-self-pollen for fertilization. Self-/non-self-recognition between pollen and pistil is regulated by the pistil-specific S-RNase gene and by multiple pollen-specific S-locus F-box (SLF) genes. To date, 10 SLF genes have been identified by various methods, and seven have been shown to be involved in pollen specificity. For a given S-haplotype, each SLF interacts with a subset of its non-self S-RNases, and an as yet unknown number of SLFs are thought to collectively mediate ubiquitination and degradation of all non-self S-RNases to allow cross-compatible pollination. To identify a complete suite of SLF genes of P. inflata, we used a de novo RNA-seq approach to analyze the pollen transcriptomes of S2-haplotype and S3-haplotype, as well as the leaf transcriptome of the S3S3 genotype. We searched for genes that fit several criteria established from the properties of the known SLF genes and identified the same seven new SLF genes in S2-haplotype and S3-haplotype, suggesting that a total of 17 SLF genes constitute pollen specificity in each S-haplotype. This finding lays the foundation for understanding how multiple SLF genes evolved and the biochemical basis for differential interactions between SLF proteins and S-RNases.
[Show abstract][Hide abstract] ABSTRACT: Pectins are acidic sugar-containing polysaccharides that are universally conserved components of the primary cell walls of plants and modulate both tip and diffuse cell growth. However, many of their specific functions and the evolution of the genes responsible for producing and modifying them are incompletely understood. The moss Physcomitrella patens is emerging as a powerful model system for the study of plant cell walls. To identify deeply conserved pectin-related genes in Physcomitrella, we generated phylogenetic trees for 16 pectin-related gene families using sequences from ten plant genomes and analyzed the evolutionary relationships within these families.
Contrary to our initial hypothesis that a single ancestral gene was present for each pectin-related gene family in the common ancestor of land plants, five of the 16 gene families, including homogalacturonan galacturonosyltransferases, polygalacturonases, pectin methylesterases, homogalacturonan methyltransferases, and pectate lyase-like proteins, show evidence of multiple members in the early land plant that gave rise to the mosses and vascular plants. Seven of the gene families, the UDP-rhamnose synthases, UDP-glucuronic acid epimerases, homogalacturonan galacturonosyltransferase-like proteins, beta-1,4-galactan beta-1,4-galactosyltransferases, rhamnogalacturonan-II xylosyltransferases, and pectin acetylesterases appear to have had a single member in the common ancestor of land plants. We detected no Physcomitrella members in the xylogalacturonan xylosyltransferase, rhamnogalacturonan-I arabinosyltransferase, pectin methylesterase inhibitor, or polygalacturonase inhibitor protein families.
Several gene families related to the production and modification of pectins in plants appear to have multiple members that are conserved as far back as the common ancestor of mosses and vascular plants. The presence of multiple members of these families even before the divergence of other important cell wall-related genes, such as cellulose synthases, suggests a more complex role than previously suspected for pectins in the evolution of land plants. The presence of relatively small pectin-related gene families in Physcomitrella as compared to Arabidopsis makes it an attractive target for analysis of the role of pectins in cell walls. In contrast, the absence of genes in Physcomitrella for some families suggests that certain pectin modifications, such as homogalacturonan xylosylation, arose later during land plant evolution.
Full-text · Article · Mar 2014 · BMC Plant Biology