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1.  Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication 
Nature biotechnology  2014;32(7):656-662.
The domestication of citrus, is poorly understood. Cultivated types are selections from, or hybrids of, wild progenitor species, whose identities and contributions remain controversial. By comparative analysis of a collection of citrus genomes, including a high quality haploid reference, we show that cultivated types were derived from two progenitor species. Though cultivated pummelos represent selections from a single progenitor species, C. maxima, cultivated mandarins are introgressions of C. maxima into the ancestral mandarin species, C. reticulata. The most widely cultivated citrus, sweet orange, is the offspring of previously admixed individuals, but sour orange is an F1 hybrid of pure C. maxima and C. reticulata parents, implying that wild mandarins were part of the early breeding germplasm. A wild “mandarin” from China exhibited substantial divergence from C. reticulata, suggesting the possibility of other unrecognized wild citrus species. Understanding citrus phylogeny through genome analysis clarifies taxonomic relationships and enables sequence-directed genetic improvement.
PMCID: PMC4113729  PMID: 24908277
2.  Positive selection of protective variants for type 2 diabetes from the Neolithic onward: a case study in Central Asia 
European Journal of Human Genetics  2013;21(10):1146-1151.
The high prevalence of type 2 diabetes and its uneven distribution among human populations is both a major public health concern and a puzzle in evolutionary biology. Why is this deleterious disease so common, while the associated genetic variants should be removed by natural selection? The ‘thrifty genotype' hypothesis proposed that the causal genetic variants were advantageous and selected for during the majority of human evolution. It remains, however, unclear whether genetic data support this scenario. In this study, we characterized patterns of selection at 10 variants associated with type 2 diabetes, contrasting one herder and one farmer population from Central Asia. We aimed at identifying which alleles (risk or protective) are under selection, dating the timing of selective events, and investigating the effect of lifestyle on selective patterns. We did not find any evidence of selection on risk variants, as predicted by the thrifty genotype hypothesis. Instead, we identified clear signatures of selection on protective variants, in both populations, dating from the beginning of the Neolithic, which suggests that this major transition was accompanied by a selective advantage for non-thrifty variants. Combining our results with worldwide data further suggests that East Asia was particularly prone to such recent selection of protective haplotypes. As much effort has been devoted so far to searching for thrifty variants, we argue that more attention should be paid to the evolution of non-thrifty variants.
PMCID: PMC3778335  PMID: 23340510
type 2 diabetes; genetic adaptation; Central Asia; thrifty genotype; human evolution
3.  The Streamlined Genome of Phytomonas spp. Relative to Human Pathogenic Kinetoplastids Reveals a Parasite Tailored for Plants 
PLoS Genetics  2014;10(2):e1004007.
Members of the family Trypanosomatidae infect many organisms, including animals, plants and humans. Plant-infecting trypanosomes are grouped under the single genus Phytomonas, failing to reflect the wide biological and pathological diversity of these protists. While some Phytomonas spp. multiply in the latex of plants, or in fruit or seeds without apparent pathogenicity, others colonize the phloem sap and afflict plants of substantial economic value, including the coffee tree, coconut and oil palms. Plant trypanosomes have not been studied extensively at the genome level, a major gap in understanding and controlling pathogenesis. We describe the genome sequences of two plant trypanosomatids, one pathogenic isolate from a Guianan coconut and one non-symptomatic isolate from Euphorbia collected in France. Although these parasites have extremely distinct pathogenic impacts, very few genes are unique to either, with the vast majority of genes shared by both isolates. Significantly, both Phytomonas spp. genomes consist essentially of single copy genes for the bulk of their metabolic enzymes, whereas other trypanosomatids e.g. Leishmania and Trypanosoma possess multiple paralogous genes or families. Indeed, comparison with other trypanosomatid genomes revealed a highly streamlined genome, encoding for a minimized metabolic system while conserving the major pathways, and with retention of a full complement of endomembrane organelles, but with no evidence for functional complexity. Identification of the metabolic genes of Phytomonas provides opportunities for establishing in vitro culturing of these fastidious parasites and new tools for the control of agricultural plant disease.
Author Summary
Some plant trypanosomes, single-celled organisms living in phloem sap, are responsible for important palm diseases, inducing frequent expensive and toxic insecticide treatments against their insect vectors. Other trypanosomes multiply in latex tubes without detriment to their host. Despite the wide range of behaviors and impacts, these trypanosomes have been rather unceremoniously lumped into a single genus: Phytomonas. A battery of molecular probes has been used for their characterization but no clear phylogeny or classification has been established. We have sequenced the genomes of a pathogenic phloem-specific Phytomonas from a diseased South American coconut palm and a latex-specific isolate collected from an apparently healthy wild euphorb in the south of France. Upon comparison with each other and with human pathogenic trypanosomes, both Phytomonas revealed distinctive compact genomes, consisting essentially of single-copy genes, with the vast majority of genes shared by both isolates irrespective of their effect on the host. A strong cohort of enzymes in the sugar metabolism pathways was consistent with the nutritional environments found in plants. The genetic nuances may reveal the basis for the behavioral differences between these two unique plant parasites, and indicate the direction of our future studies in search of effective treatment of the crop disease parasites.
PMCID: PMC3916237  PMID: 24516393
4.  Climate and Soil Type Together Explain the Distribution of Microendemic Species in a Biodiversity Hotspot 
PLoS ONE  2013;8(12):e80811.
The grasshopper genus Caledonula, endemic to New Caledonia, was studied to understand the evolution of species distributions in relation to climate and soil types. Based on a comprehensive sampling of 80 locations throughout the island, the genus was represented by five species, four of which are new to science, of which three are described here. All the species have limited distributions in New Caledonia. Bioclimatic niche modelling shows that all the species were found in association with a wet climate and reduced seasonality, explaining their restriction to the southern half of the island. The results suggest that the genus was ancestrally constrained by seasonality. A molecular phylogeny was reconstructed using two mitochondrial and two nuclear markers. The partially resolved tree showed monophyly of the species found on metalliferous soils, and molecular dating indicated a rather recent origin for the genus. Adaptation to metalliferous soils is suggested by both morphological changes and radiation on these soils. The genus Caledonula is therefore a good model to understand the origin of microendemism in the context of recent and mixed influences of climate and soil type.
PMCID: PMC3867321  PMID: 24367480
5.  Complete DNA Sequence of Kuraishia capsulata Illustrates Novel Genomic Features among Budding Yeasts (Saccharomycotina) 
Genome Biology and Evolution  2013;5(12):2524-2539.
The numerous yeast genome sequences presently available provide a rich source of information for functional as well as evolutionary genomics but unequally cover the large phylogenetic diversity of extant yeasts. We present here the complete sequence of the nuclear genome of the haploid-type strain of Kuraishia capsulata (CBS1993T), a nitrate-assimilating Saccharomycetales of uncertain taxonomy, isolated from tunnels of insect larvae underneath coniferous barks and characterized by its copious production of extracellular polysaccharides. The sequence is composed of seven scaffolds, one per chromosome, totaling 11.4 Mb and containing 6,029 protein-coding genes, ∼13.5% of which being interrupted by introns. This GC-rich yeast genome (45.7%) appears phylogenetically related with the few other nitrate-assimilating yeasts sequenced so far, Ogataea polymorpha, O. parapolymorpha, and Dekkera bruxellensis, with which it shares a very reduced number of tRNA genes, a novel tRNA sparing strategy, and a common nitrate assimilation cluster, three specific features to this group of yeasts. Centromeres were recognized in GC-poor troughs of each scaffold. The strain bears MAT alpha genes at a single MAT locus and presents a significant degree of conservation with Saccharomyces cerevisiae genes, suggesting that it can perform sexual cycles in nature, although genes involved in meiosis were not all recognized. The complete absence of conservation of synteny between K. capsulata and any other yeast genome described so far, including the three other nitrate-assimilating species, validates the interest of this species for long-range evolutionary genomic studies among Saccharomycotina yeasts.
PMCID: PMC3879985  PMID: 24317973
phylogeny; centromere; synteny; noncoding RNA; introgression
6.  Molecular evidence for an Asian origin of monitor lizards followed by Tertiary dispersals to Africa and Australasia 
Biology Letters  2012;8(5):853-855.
Monitor lizards are emblematic reptiles that are widely distributed in the Old World. Although relatively well studied in vertebrate research, their biogeographic history is still controversial. We constructed a molecular dataset for 54 anguimorph species, including representatives of all families with detailed sampling of the Varanidae (38 species). Our results are consistent with an Asian origin of the Varanidae followed by a dispersal to Africa 41 (49–33) Ma, possibly via an Iranian route. Another major event was the dispersal of monitors to Australia in the Late Eocene–Oligocene 32 (39–26) Ma. This divergence estimate adds to the suggestion that Australia was colonized by several squamate lineages prior to the collision of the Australian plate with the Asian plate starting 25 Ma.
PMCID: PMC3441001  PMID: 22809723
biogeography; squamates; Varanus; Cenozoic
7.  Comparative genomics of emerging pathogens in the Candida glabrata clade 
BMC Genomics  2013;14:623.
Candida glabrata follows C. albicans as the second or third most prevalent cause of candidemia worldwide. These two pathogenic yeasts are distantly related, C. glabrata being part of the Nakaseomyces, a group more closely related to Saccharomyces cerevisiae. Although C. glabrata was thought to be the only pathogenic Nakaseomyces, two new pathogens have recently been described within this group: C. nivariensis and C. bracarensis. To gain insight into the genomic changes underlying the emergence of virulence, we sequenced the genomes of these two, and three other non-pathogenic Nakaseomyces, and compared them to other sequenced yeasts.
Our results indicate that the two new pathogens are more closely related to the non-pathogenic N. delphensis than to C. glabrata. We uncover duplications and accelerated evolution that specifically affected genes in the lineage preceding the group containing N. delphensis and the three pathogens, which may provide clues to the higher propensity of this group to infect humans. Finally, the number of Epa-like adhesins is specifically enriched in the pathogens, particularly in C. glabrata.
Remarkably, some features thought to be the result of adaptation of C. glabrata to a pathogenic lifestyle, are present throughout the Nakaseomyces, indicating these are rather ancient adaptations to other environments. Phylogeny suggests that human pathogenesis evolved several times, independently within the clade. The expansion of the EPA gene family in pathogens establishes an evolutionary link between adhesion and virulence phenotypes. Our analyses thus shed light onto the relationships between virulence and the recent genomic changes that occurred within the Nakaseomyces.
Sequence Accession Numbers
Nakaseomyces delphensis: CAPT01000001 to CAPT01000179
Candida bracarensis: CAPU01000001 to CAPU01000251
Candida nivariensis: CAPV01000001 to CAPV01000123
Candida castellii: CAPW01000001 to CAPW01000101
Nakaseomyces bacillisporus: CAPX01000001 to CAPX01000186
PMCID: PMC3847288  PMID: 24034898
Candida glabrata; Fungal pathogens; Nakaseomyces; Yeast genomes; Yeast evolution
8.  Is the Species Flock Concept Operational? The Antarctic Shelf Case 
PLoS ONE  2013;8(8):e68787.
There has been a significant body of literature on species flock definition but not so much about practical means to appraise them. We here apply the five criteria of Eastman and McCune for detecting species flocks in four taxonomic components of the benthic fauna of the Antarctic shelf: teleost fishes, crinoids (feather stars), echinoids (sea urchins) and crustacean arthropods. Practical limitations led us to prioritize the three historical criteria (endemicity, monophyly, species richness) over the two ecological ones (ecological diversity and habitat dominance). We propose a new protocol which includes an iterative fine-tuning of the monophyly and endemicity criteria in order to discover unsuspected flocks. As a result nine « full » species flocks (fulfilling the five criteria) are briefly described. Eight other flocks fit the three historical criteria but need to be further investigated from the ecological point of view (here called « core flocks »). The approach also shows that some candidate taxonomic components are no species flocks at all. The present study contradicts the paradigm that marine species flocks are rare. The hypothesis according to which the Antarctic shelf acts as a species flocks generator is supported, and the approach indicates paths for further ecological studies and may serve as a starting point to investigate the processes leading to flock-like patterning of biodiversity.
PMCID: PMC3732269  PMID: 23936311
9.  Integrative Biology of Idas iwaotakii (Habe, 1958), a ‘Model Species’ Associated with Sunken Organic Substrates 
PLoS ONE  2013;8(7):e69680.
The giant bathymodioline mussels from vents have been studied as models to understand the adaptation of organisms to deep-sea chemosynthetic environments. These mussels are closely related to minute mussels associated to organic remains decaying on the deep-sea floor. Whereas biological data accumulate for the giant mussels, the small mussels remain poorly studied. Despite this lack of data for species living on organic remains it has been hypothesized that during evolution, contrary to their relatives from vents or seeps, they did not acquire highly specialized biological features. We aim at testing this hypothesis by providing new biological data for species associated with organic falls. Within Bathymodiolinae a close phylogenetic relationship was revealed between the Bathymodiolus sensu stricto lineage (i.e. “thermophilus” lineage) which includes exclusively vent and seep species, and a diversified lineage of small mussels, attributed to the genus Idas, that includes mostly species from organic falls. We selected Idas iwaotakii (Habe, 1958) from this latter lineage to analyse population structure and to document biological features. Mitochondrial and nuclear markers reveal a north-south genetic structure at an oceanic scale in the Western Pacific but no structure was revealed at a regional scale or as correlated with the kind of substrate or depth. The morphology of larval shells suggests substantial dispersal abilities. Nutritional features were assessed by examining bacterial diversity coupled by a microscopic analysis of the digestive tract. Molecular data demonstrated the presence of sulphur-oxidizing bacteria resembling those identified in other Bathymodiolinae. In contrast with most Bathymodiolus s.s. species the digestive tract of I. iwaotakii is not reduced. Combining data from literature with the present data shows that most of the important biological features are shared between Bathymodiolus s.s. species and its sister-lineage. However Bathymodiolus s.s. species are ecologically more restricted and also display a lower species richness than Idas species.
PMCID: PMC3722101  PMID: 23894520
10.  Genomic insights into strategies used by Xanthomonas albilineans with its reduced artillery to spread within sugarcane xylem vessels 
BMC Genomics  2012;13:658.
Xanthomonas albilineans causes leaf scald, a lethal disease of sugarcane. X. albilineans exhibits distinctive pathogenic mechanisms, ecology and taxonomy compared to other species of Xanthomonas. For example, this species produces a potent DNA gyrase inhibitor called albicidin that is largely responsible for inducing disease symptoms; its habitat is limited to xylem; and the species exhibits large variability. A first manuscript on the complete genome sequence of the highly pathogenic X. albilineans strain GPE PC73 focused exclusively on distinctive genomic features shared with Xylella fastidiosa—another xylem-limited Xanthomonadaceae. The present manuscript on the same genome sequence aims to describe all other pathogenicity-related genomic features of X. albilineans, and to compare, using suppression subtractive hybridization (SSH), genomic features of two strains differing in pathogenicity.
Comparative genomic analyses showed that most of the known pathogenicity factors from other Xanthomonas species are conserved in X. albilineans, with the notable absence of two major determinants of the “artillery” of other plant pathogenic species of Xanthomonas: the xanthan gum biosynthesis gene cluster, and the type III secretion system Hrp (hypersensitive response and pathogenicity). Genomic features specific to X. albilineans that may contribute to specific adaptation of this pathogen to sugarcane xylem vessels were also revealed. SSH experiments led to the identification of 20 genes common to three highly pathogenic strains but missing in a less pathogenic strain. These 20 genes, which include four ABC transporter genes, a methyl-accepting chemotaxis protein gene and an oxidoreductase gene, could play a key role in pathogenicity. With the exception of hypothetical proteins revealed by our comparative genomic analyses and SSH experiments, no genes potentially involved in any offensive or counter-defensive mechanism specific to X. albilineans were identified, supposing that X. albilineans has a reduced artillery compared to other pathogenic Xanthomonas species. Particular attention has therefore been given to genomic features specific to X. albilineans making it more capable of evading sugarcane surveillance systems or resisting sugarcane defense systems.
This study confirms that X. albilineans is a highly distinctive species within the genus Xanthomonas, and opens new perpectives towards a greater understanding of the pathogenicity of this destructive sugarcane pathogen.
PMCID: PMC3542200  PMID: 23171051
11.  A Remarkable Case of Micro-Endemism in Laonastes aenigmamus (Diatomyidae, Rodentia) Revealed by Nuclear and Mitochondrial DNA Sequence Data 
PLoS ONE  2012;7(11):e48145.
L. aenigmamus is endemic to the limestone formations of the Khammuan Province (Lao PDR), and is strongly specialized ecologically. From the survey of 137 individuals collected from 38 localities, we studied the phylogeography of this species using one mitochondrial (Cyt b) and two nuclear genes (BFIBR and GHR). Cyt b analyses reveal a strong mtDNA phylogeographical structure: 8 major geographical clades differing by 5–14% sequence divergence were identified, most of them corresponding to distinct karst areas. Nuclear markers display congruent results but with a less genetic structuring. Together, the data strongly suggest an inland insular model for Laonastes population structure. With 8 to 16 evolutionary significant units in a small area (about 200×50 km) this represents an exceptional example of micro-endemism. Our results suggest that L. aenigmamus may represent a complex of species and/or sub-species. The common ancestor of all Laonastes may have been widely distributed within the limestone formations of the Khammuan Province at the end of Miocene/beginning of the Pliocene. Parallel events of karst fragmentation and population isolation would have occurred during the Pleistocene or/and the end of the Pliocene. The limited gene flow detected between populations from different karst blocks restrains the likelihood of survival of Laonastes. This work increases the necessity for a strict protection of this rare animal and its habitat and provides exclusive information, essential to the organization of its protection.
PMCID: PMC3498270  PMID: 23155377
12.  Secondary Sympatry Caused by Range Expansion Informs on the Dynamics of Microendemism in a Biodiversity Hotspot 
PLoS ONE  2012;7(11):e48047.
Islands are bounded areas where high endemism is explained either by allopatric speciation through the fragmentation of the limited amount of space available, or by sympatric speciation and accumulation of daughter species. Most empirical evidence point out the dominant action of allopatric speciation. We evaluate this general view by looking at a case study where sympatric speciation is suspected. We analyse the mode, tempo and geography of speciation in Agnotecous, a cricket genus endemic to New Caledonia showing a generalized pattern of sympatry between species making sympatric speciation plausible. We obtained five mitochondrial and five nuclear markers (6.8 kb) from 37 taxa corresponding to 17 of the 21 known extant species of Agnotecous, and including several localities per species, and we conducted phylogenetic and dating analyses. Our results suggest that the diversification of Agnotecous occurred mostly through allopatric speciation in the last 10 Myr. Highly microendemic species are the most recent ones (<2 Myr) and current sympatry is due to secondary range expansion after allopatric speciation. Species distribution should then be viewed as a highly dynamic process and extreme microendemism only as a temporary situation. We discuss these results considering the influence of climatic changes combined with intricate soil diversity and mountain topography. A complex interplay between these factors could have permitted repeated speciation events and range expansion.
PMCID: PMC3490955  PMID: 23139758
13.  An Extreme Case of Plant–Insect Codiversification: Figs and Fig-Pollinating Wasps 
Systematic Biology  2012;61(6):1029-1047.
It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant–insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant–insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.]
PMCID: PMC3478567  PMID: 22848088
14.  Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage 
Genome Biology  2012;13(8):R74.
Bathycoccus prasinos is an extremely small cosmopolitan marine green alga whose cells are covered with intricate spider's web patterned scales that develop within the Golgi cisternae before their transport to the cell surface. The objective of this work is to sequence and analyze its genome, and to present a comparative analysis with other known genomes of the green lineage.
Its small genome of 15 Mb consists of 19 chromosomes and lacks transposons. Although 70% of all B. prasinos genes share similarities with other Viridiplantae genes, up to 428 genes were probably acquired by horizontal gene transfer, mainly from other eukaryotes. Two chromosomes, one big and one small, are atypical, an unusual synapomorphic feature within the Mamiellales. Genes on these atypical outlier chromosomes show lower GC content and a significant fraction of putative horizontal gene transfer genes. Whereas the small outlier chromosome lacks colinearity with other Mamiellales and contains many unknown genes without homologs in other species, the big outlier shows a higher intron content, increased expression levels and a unique clustering pattern of housekeeping functionalities. Four gene families are highly expanded in B. prasinos, including sialyltransferases, sialidases, ankyrin repeats and zinc ion-binding genes, and we hypothesize that these genes are associated with the process of scale biogenesis.
The minimal genomes of the Mamiellophyceae provide a baseline for evolutionary and functional analyses of metabolic processes in green plants.
PMCID: PMC3491373  PMID: 22925495
15.  Reviving the African Wolf Canis lupus lupaster in North and West Africa: A Mitochondrial Lineage Ranging More than 6,000 km Wide 
PLoS ONE  2012;7(8):e42740.
The recent discovery of a lineage of gray wolf in North-East Africa suggests the presence of a cryptic canid on the continent, the African wolf Canis lupus lupaster. We analyzed the mtDNA diversity (cytochrome b and control region) of a series of African Canis including wolf-like animals from North and West Africa. Our objectives were to assess the actual range of C. l. lupaster, to further estimate the genetic characteristics and demographic history of its lineage, and to question its taxonomic delineation from the golden jackal C. aureus, with which it has been considered synonymous. We confirmed the existence of four distinct lineages within the gray wolf, including C. lupus/familiaris (Holarctic wolves and dogs), C. l. pallipes, C. l. chanco and C. l. lupaster. Taxonomic assignment procedures identified wolf-like individuals from Algeria, Mali and Senegal, as belonging to C. l. lupaster, expanding its known distribution c. 6,000 km to the west. We estimated that the African wolf lineage (i) had the highest level of genetic diversity within C. lupus, (ii) coalesced during the Late Pleistocene, contemporaneously with Holarctic wolves and dogs, and (iii) had an effective population size of c. 80,000 females. Our results suggest that the African wolf is a relatively ancient gray wolf lineage with a fairly large, past effective population size, as also suggested by the Pleistocene fossil record. Unique field observations in Senegal allowed us to provide a morphological and behavioral diagnosis of the African wolf that clearly distinguished it from the sympatric golden jackal. However, the detection of C. l. lupaster mtDNA haplotypes in C. aureus from Senegal brings the delineation between the African wolf and the golden jackal into question. In terms of conservation, it appears urgent to further characterize the status of the African wolf with regard to the African golden jackal.
PMCID: PMC3416759  PMID: 22900047
16.  The Medicago Genome Provides Insight into the Evolution of Rhizobial Symbioses 
Young, Nevin D. | Debellé, Frédéric | Oldroyd, Giles E. D. | Geurts, Rene | Cannon, Steven B. | Udvardi, Michael K. | Benedito, Vagner A. | Mayer, Klaus F. X. | Gouzy, Jérôme | Schoof, Heiko | Van de Peer, Yves | Proost, Sebastian | Cook, Douglas R. | Meyers, Blake C. | Spannagl, Manuel | Cheung, Foo | De Mita, Stéphane | Krishnakumar, Vivek | Gundlach, Heidrun | Zhou, Shiguo | Mudge, Joann | Bharti, Arvind K. | Murray, Jeremy D. | Naoumkina, Marina A. | Rosen, Benjamin | Silverstein, Kevin A. T. | Tang, Haibao | Rombauts, Stephane | Zhao, Patrick X. | Zhou, Peng | Barbe, Valérie | Bardou, Philippe | Bechner, Michael | Bellec, Arnaud | Berger, Anne | Bergès, Hélène | Bidwell, Shelby | Bisseling, Ton | Choisne, Nathalie | Couloux, Arnaud | Denny, Roxanne | Deshpande, Shweta | Dai, Xinbin | Doyle, Jeff | Dudez, Anne-Marie | Farmer, Andrew D. | Fouteau, Stéphanie | Franken, Carolien | Gibelin, Chrystel | Gish, John | Goldstein, Steven | González, Alvaro J. | Green, Pamela J. | Hallab, Asis | Hartog, Marijke | Hua, Axin | Humphray, Sean | Jeong, Dong-Hoon | Jing, Yi | Jöcker, Anika | Kenton, Steve M. | Kim, Dong-Jin | Klee, Kathrin | Lai, Hongshing | Lang, Chunting | Lin, Shaoping | Macmil, Simone L | Magdelenat, Ghislaine | Matthews, Lucy | McCorrison, Jamison | Monaghan, Erin L. | Mun, Jeong-Hwan | Najar, Fares Z. | Nicholson, Christine | Noirot, Céline | O’Bleness, Majesta | Paule, Charles R. | Poulain, Julie | Prion, Florent | Qin, Baifang | Qu, Chunmei | Retzel, Ernest F. | Riddle, Claire | Sallet, Erika | Samain, Sylvie | Samson, Nicolas | Sanders, Iryna | Saurat, Olivier | Scarpelli, Claude | Schiex, Thomas | Segurens, Béatrice | Severin, Andrew J. | Sherrier, D. Janine | Shi, Ruihua | Sims, Sarah | Singer, Susan R. | Sinharoy, Senjuti | Sterck, Lieven | Viollet, Agnès | Wang, Bing-Bing | Wang, Keqin | Wang, Mingyi | Wang, Xiaohong | Warfsmann, Jens | Weissenbach, Jean | White, Doug D. | White, Jim D. | Wiley, Graham B. | Wincker, Patrick | Xing, Yanbo | Yang, Limei | Yao, Ziyun | Ying, Fu | Zhai, Jixian | Zhou, Liping | Zuber, Antoine | Dénarié, Jean | Dixon, Richard A. | May, Gregory D. | Schwartz, David C. | Rogers, Jane | Quétier, Francis | Town, Christopher D. | Roe, Bruce A.
Nature  2011;480(7378):520-524.
Legumes (Fabaceae or Leguminosae) are unique among cultivated plants for their ability to carry out endosymbiotic nitrogen fixation with rhizobial bacteria, a process that takes place in a specialized structure known as the nodule. Legumes belong to one of the two main groups of eurosids, the Fabidae, which includes most species capable of endosymbiotic nitrogen fixation 1. Legumes comprise several evolutionary lineages derived from a common ancestor 60 million years ago (Mya). Papilionoids are the largest clade, dating nearly to the origin of legumes and containing most cultivated species 2. Medicago truncatula (Mt) is a long-established model for the study of legume biology. Here we describe the draft sequence of the Mt euchromatin based on a recently completed BAC-assembly supplemented with Illumina-shotgun sequence, together capturing ~94% of all Mt genes. A whole-genome duplication (WGD) approximately 58 Mya played a major role in shaping the Mt genome and thereby contributed to the evolution of endosymbiotic nitrogen fixation. Subsequent to the WGD, the Mt genome experienced higher levels of rearrangement than two other sequenced legumes, Glycine max (Gm) and Lotus japonicus (Lj). Mt is a close relative of alfalfa (M. sativa), a widely cultivated crop with limited genomics tools and complex autotetraploid genetics. As such, the Mt genome sequence provides significant opportunities to expand alfalfa’s genomic toolbox.
PMCID: PMC3272368  PMID: 22089132
17.  Deep-Sea Origin and In-Situ Diversification of Chrysogorgiid Octocorals 
PLoS ONE  2012;7(6):e38357.
The diversity, ubiquity and prevalence in deep waters of the octocoral family Chrysogorgiidae Verrill, 1883 make it noteworthy as a model system to study radiation and diversification in the deep sea. Here we provide the first comprehensive phylogenetic analysis of the Chrysogorgiidae, and compare phylogeny and depth distribution. Phylogenetic relationships among 10 of 14 currently-described Chrysogorgiidae genera were inferred based on mitochondrial (mtMutS, cox1) and nuclear (18S) markers. Bathymetric distribution was estimated from multiple sources, including museum records, a literature review, and our own sampling records (985 stations, 2345 specimens). Genetic analyses suggest that the Chrysogorgiidae as currently described is a polyphyletic family. Shallow-water genera, and two of eight deep-water genera, appear more closely related to other octocoral families than to the remainder of the monophyletic, deep-water chrysogorgiid genera. Monophyletic chrysogorgiids are composed of strictly (Iridogorgia Verrill, 1883, Metallogorgia Versluys, 1902, Radicipes Stearns, 1883, Pseudochrysogorgia Pante & France, 2010) and predominantly (Chrysogorgia Duchassaing & Michelotti, 1864) deep-sea genera that diversified in situ. This group is sister to gold corals (Primnoidae Milne Edwards, 1857) and deep-sea bamboo corals (Keratoisidinae Gray, 1870), whose diversity also peaks in the deep sea. Nine species of Chrysogorgia that were described from depths shallower than 200 m, and mtMutS haplotypes sequenced from specimens sampled as shallow as 101 m, suggest a shallow-water emergence of some Chrysogorgia species.
PMCID: PMC3377635  PMID: 22723855
18.  Evolution of oil-producing trichomes in Sisyrinchium (Iridaceae): insights from the first comprehensive phylogenetic analysis of the genus 
Annals of Botany  2011;107(8):1287-1312.
Background and Aims
Sisyrinchium (Iridaceae: Iridoideae: Sisyrinchieae) is one of the largest, most widespread and most taxonomically complex genera in Iridaceae, with all species except one native to the American continent. Phylogenetic relationships within the genus were investigated and the evolution of oil-producing structures related to specialized oil-bee pollination examined.
Phylogenetic analyses based on eight molecular markers obtained from 101 Sisyrinchium accessions representing 85 species were conducted in the first extensive phylogenetic analysis of the genus. Total evidence analyses confirmed the monophyly of the genus and retrieved nine major clades weakly connected to the subdivisions previously recognized. The resulting phylogenetic hypothesis was used to reconstruct biogeographical patterns, and to trace the evolutionary origin of glandular trichomes present in the flowers of several species.
Key Results and Conclusions
Glandular trichomes evolved three times independently in the genus. In two cases, these glandular trichomes are oil-secreting, suggesting that the corresponding flowers might be pollinated by oil-bees. Biogeographical patterns indicate expansions from Central America and the northern Andes to the subandean ranges between Chile and Argentina and to the extended area of the Paraná river basin. The distribution of oil-flower species across the phylogenetic trees suggests that oil-producing trichomes may have played a key role in the diversification of the genus, a hypothesis that requires future testing.
PMCID: PMC3101146  PMID: 21527419
Oil-bee pollination; glandular trichomes; elaiophores; lipids; phylogeography; Sisyrinchieae; Olsynium; Solenomelus
19.  Complete Genome Sequence of the Clinical Streptococcus salivarius Strain CCHSS3 ▿  
Journal of Bacteriology  2011;193(18):5041-5042.
Streptococcus salivarius is a commensal species commonly found in the human oral cavity and digestive tract, although it is also associated with human infections such as meningitis, endocarditis, and bacteremia. Here, we report the complete sequence of S. salivarius strain CCHSS3, isolated from human blood.
PMCID: PMC3165645  PMID: 21742894
20.  Complete Genome Sequence of the Commensal Streptococcus salivarius Strain JIM8777 ▿  
Journal of Bacteriology  2011;193(18):5024-5025.
The commensal bacterium Streptococcus salivarius is a prevalent species of the human oropharyngeal tract with an important role in oral ecology. Here, we report the complete 2.2-Mb genome sequence and annotation of strain JIM8777, which was recently isolated from the oral cavity of a healthy, dentate infant.
PMCID: PMC3165664  PMID: 21742871
21.  Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea 
Amselem, Joelle | Cuomo, Christina A. | van Kan, Jan A. L. | Viaud, Muriel | Benito, Ernesto P. | Couloux, Arnaud | Coutinho, Pedro M. | de Vries, Ronald P. | Dyer, Paul S. | Fillinger, Sabine | Fournier, Elisabeth | Gout, Lilian | Hahn, Matthias | Kohn, Linda | Lapalu, Nicolas | Plummer, Kim M. | Pradier, Jean-Marc | Quévillon, Emmanuel | Sharon, Amir | Simon, Adeline | ten Have, Arjen | Tudzynski, Bettina | Tudzynski, Paul | Wincker, Patrick | Andrew, Marion | Anthouard, Véronique | Beever, Ross E. | Beffa, Rolland | Benoit, Isabelle | Bouzid, Ourdia | Brault, Baptiste | Chen, Zehua | Choquer, Mathias | Collémare, Jérome | Cotton, Pascale | Danchin, Etienne G. | Da Silva, Corinne | Gautier, Angélique | Giraud, Corinne | Giraud, Tatiana | Gonzalez, Celedonio | Grossetete, Sandrine | Güldener, Ulrich | Henrissat, Bernard | Howlett, Barbara J. | Kodira, Chinnappa | Kretschmer, Matthias | Lappartient, Anne | Leroch, Michaela | Levis, Caroline | Mauceli, Evan | Neuvéglise, Cécile | Oeser, Birgitt | Pearson, Matthew | Poulain, Julie | Poussereau, Nathalie | Quesneville, Hadi | Rascle, Christine | Schumacher, Julia | Ségurens, Béatrice | Sexton, Adrienne | Silva, Evelyn | Sirven, Catherine | Soanes, Darren M. | Talbot, Nicholas J. | Templeton, Matt | Yandava, Chandri | Yarden, Oded | Zeng, Qiandong | Rollins, Jeffrey A. | Lebrun, Marc-Henri | Dickman, Marty
PLoS Genetics  2011;7(8):e1002230.
Sclerotinia sclerotiorum and Botrytis cinerea are closely related necrotrophic plant pathogenic fungi notable for their wide host ranges and environmental persistence. These attributes have made these species models for understanding the complexity of necrotrophic, broad host-range pathogenicity. Despite their similarities, the two species differ in mating behaviour and the ability to produce asexual spores. We have sequenced the genomes of one strain of S. sclerotiorum and two strains of B. cinerea. The comparative analysis of these genomes relative to one another and to other sequenced fungal genomes is provided here. Their 38–39 Mb genomes include 11,860–14,270 predicted genes, which share 83% amino acid identity on average between the two species. We have mapped the S. sclerotiorum assembly to 16 chromosomes and found large-scale co-linearity with the B. cinerea genomes. Seven percent of the S. sclerotiorum genome comprises transposable elements compared to <1% of B. cinerea. The arsenal of genes associated with necrotrophic processes is similar between the species, including genes involved in plant cell wall degradation and oxalic acid production. Analysis of secondary metabolism gene clusters revealed an expansion in number and diversity of B. cinerea–specific secondary metabolites relative to S. sclerotiorum. The potential diversity in secondary metabolism might be involved in adaptation to specific ecological niches. Comparative genome analysis revealed the basis of differing sexual mating compatibility systems between S. sclerotiorum and B. cinerea. The organization of the mating-type loci differs, and their structures provide evidence for the evolution of heterothallism from homothallism. These data shed light on the evolutionary and mechanistic bases of the genetically complex traits of necrotrophic pathogenicity and sexual mating. This resource should facilitate the functional studies designed to better understand what makes these fungi such successful and persistent pathogens of agronomic crops.
Author Summary
Sclerotinia sclerotiorum and Botrytis cinerea are notorious plant pathogenic fungi with very wide host ranges. They cause vast economic damage during crop cultivation as well as in harvested produce. These fungi are typical examples of necrotrophs: they first kill host plant cells and then colonize the dead tissue. The genome sequences of the two fungi were determined in order to examine commonalities in structure and content and in order to find unique features that may distinguish them from other pathogenic fungi and from saprotrophic fungi. The genomes show high sequence identity and a similar arrangement of genes. S. sclerotiorum and B. cinerea differ in their regulation of sexual reproduction, and the genetic basis and its evolution could be explained from the genome sequence. The genome sequence revealed a striking difference in the number and diversity of secondary metabolism gene clusters, which may be involved in the adaptation to different ecological niches. Altogether, there were no unique features in the genomes of S. sclerotiorum and B. cinerea that could be identified as “silver bullets,” which distinguish these aggressive pathogens from other pathogenic and non-pathogenic fungi. These findings reinforce the quantitative, multigenic nature of necrotrophic pathogenesis.
PMCID: PMC3158057  PMID: 21876677
22.  Multiple colonizations from Madagascar and converged acquisition of dioecy in the Mascarene Dombeyoideae (Malvaceae) as inferred from chloroplast and nuclear DNA sequence analyses 
Annals of Botany  2010;106(2):343-357.
Background and Aims
In the Mascarenes, a young oceanic archipelago composed of three main islands, the Dombeyoideae (Malvaceae) have diversified extensively with a high endemism rate. With the exception of the genus Trochetia, Mascarene Dombeyoideae are described as dioecious whereas Malagasy and African species are considered to be monocline, species with individuals bearing hermaphrodite/perfect flowers. In this study, the phylogenetic relationships were reconstructed to clarify the taxonomy, understand the phylogeographic pattern of relationships and infer the evolution of the breeding systems for the Mascarenes Dombeyoideae.
Parsimony and Bayesian analysis of four DNA markers (ITS, rpl16 intron and two intergenic spacers trnQ-rsp16 and psbM-trnD) was used. The molecular matrix comprised 2985 characters and 48 taxa. The Bayesian phylogeny was used to infer phylogeographical hypotheses and the evolution of breeding systems.
Key Results
Parsimony and Bayesian trees produced similar results. The Dombeyoideae from the Mascarenes are polyphyletic and distributed among four clades. Species of Dombeya, Trochetia and Ruizia are nested in the same clade, which implies the paraphyly of Dombeya. Additionally, it is shown that each of the four clades has an independent Malagasy origin. Two adaptive radiation events have occurred within two endemic lineages of the Mascarenes. The polyphyly of the Mascarene Dombeyoideae suggests at least three independent acquisitions of dioecy.
This molecular phylogeny highlights the taxonomic issues within the Dombeyoideae. Indeed, the limits and distinctions of the genera Dombeya, Trochetia and Ruizia should be reconsidered. The close phylogeographic relationships between the flora of the Mascarenes and Madagascar are confirmed. Despite their independent origins and a distinct evolutionary history, each endemic clade has developed a different breeding systems (dioecy) compared with the Malagasy Dombeyoideae. Sex separation appears as an evolutionary convergence and may be the consequence of selective pressures particular to insular environments.
PMCID: PMC2908169  PMID: 20562131
Dombeyoideae; Mascarene archipelago; Dombeya; Ruizia; Trochetia; dioecy; Indian Ocean; biogeography; ITS; rpl16 intron; psbM-trnD; trnQ-rps16
23.  Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite 
Genome Biology  2011;12(3):R29.
Blastocystis is a highly prevalent anaerobic eukaryotic parasite of humans and animals that is associated with various gastrointestinal and extraintestinal disorders. Epidemiological studies have identified different subtypes but no one subtype has been definitively correlated with disease.
Here we report the 18.8 Mb genome sequence of a Blastocystis subtype 7 isolate, which is the smallest stramenopile genome sequenced to date. The genome is highly compact and contains intriguing rearrangements. Comparisons with other available stramenopile genomes (plant pathogenic oomycete and diatom genomes) revealed effector proteins potentially involved in the adaptation to the intestinal environment, which were likely acquired via horizontal gene transfer. Moreover, Blastocystis living in anaerobic conditions harbors mitochondria-like organelles. An incomplete oxidative phosphorylation chain, a partial Krebs cycle, amino acid and fatty acid metabolisms and an iron-sulfur cluster assembly are all predicted to occur in these organelles. Predicted secretory proteins possess putative activities that may alter host physiology, such as proteases, protease-inhibitors, immunophilins and glycosyltransferases. This parasite also possesses the enzymatic machinery to tolerate oxidative bursts resulting from its own metabolism or induced by the host immune system.
This study provides insights into the genome architecture of this unusual stramenopile. It also proposes candidate genes with which to study the physiopathology of this parasite and thus may lead to further investigations into Blastocystis-host interactions.
PMCID: PMC3129679  PMID: 21439036
24.  Haplowebs as a graphical tool for delimiting species: a revival of Doyle's "field for recombination" approach and its application to the coral genus Pocillopora in Clipperton 
Usual methods for inferring species boundaries from molecular sequence data rely either on gene trees or on population genetic analyses. Another way of delimiting species, based on a view of species as "fields for recombination" (FFRs) characterized by mutual allelic exclusivity, was suggested in 1995 by Doyle. Here we propose to use haplowebs (haplotype networks with additional connections between haplotypes found co-occurring in heterozygous individuals) to visualize and delineate single-locus FFRs (sl-FFRs). Furthermore, we introduce a method to quantify the reliability of putative species boundaries according to the number of independent markers that support them, and illustrate this approach with a case study of taxonomically difficult corals of the genus Pocillopora collected around Clipperton Island (far eastern Pacific).
One haploweb built from intron sequences of the ATP synthase β subunit gene revealed the presence of two sl-FFRs among our 74 coral samples, whereas a second one built from ITS sequences turned out to be composed of four sl-FFRs. As a third independent marker, we performed a combined analysis of two regions of the mitochondrial genome: since haplowebs are not suited to analyze non-recombining markers, individuals were sorted into four haplogroups according to their mitochondrial sequences. Among all possible bipartitions of our set of samples, thirteen were supported by at least one molecular dataset, none by two and only one by all three datasets: this congruent pattern obtained from independent nuclear and mitochondrial markers indicates that two species of Pocillopora are present in Clipperton.
Our approach builds on Doyle's method and extends it by introducing an intuitive, user-friendly graphical representation and by proposing a conceptual framework to analyze and quantify the congruence between sl-FFRs obtained from several independent markers. Like delineation methods based on population-level statistical approaches, our method can distinguish closely-related species that have not yet reached reciprocal monophyly at most or all of their loci; like tree-based approaches, it can yield meaningful conclusions using a number of independent markers as low as three. Future efforts will aim to develop programs that speed up the construction of haplowebs from FASTA sequence alignments and help perform the congruence analysis outlined in this article.
PMCID: PMC3022603  PMID: 21118572
25.  Bioinformatic analysis of ESTs collected by Sanger and pyrosequencing methods for a keystone forest tree species: oak 
BMC Genomics  2010;11:650.
The Fagaceae family comprises about 1,000 woody species worldwide. About half belong to the Quercus family. These oaks are often a source of raw material for biomass wood and fiber. Pedunculate and sessile oaks, are among the most important deciduous forest tree species in Europe. Despite their ecological and economical importance, very few genomic resources have yet been generated for these species. Here, we describe the development of an EST catalogue that will support ecosystem genomics studies, where geneticists, ecophysiologists, molecular biologists and ecologists join their efforts for understanding, monitoring and predicting functional genetic diversity.
We generated 145,827 sequence reads from 20 cDNA libraries using the Sanger method. Unexploitable chromatograms and quality checking lead us to eliminate 19,941 sequences. Finally a total of 125,925 ESTs were retained from 111,361 cDNA clones. Pyrosequencing was also conducted for 14 libraries, generating 1,948,579 reads, from which 370,566 sequences (19.0%) were eliminated, resulting in 1,578,192 sequences. Following clustering and assembly using TGICL pipeline, 1,704,117 EST sequences collapsed into 69,154 tentative contigs and 153,517 singletons, providing 222,671 non-redundant sequences (including alternative transcripts). We also assembled the sequences using MIRA and PartiGene software and compared the three unigene sets. Gene ontology annotation was then assigned to 29,303 unigene elements. Blast search against the SWISS-PROT database revealed putative homologs for 32,810 (14.7%) unigene elements, but more extensive search with Pfam, Refseq_protein, Refseq_RNA and eight gene indices revealed homology for 67.4% of them. The EST catalogue was examined for putative homologs of candidate genes involved in bud phenology, cuticle formation, phenylpropanoids biosynthesis and cell wall formation. Our results suggest a good coverage of genes involved in these traits. Comparative orthologous sequences (COS) with other plant gene models were identified and allow to unravel the oak paleo-history. Simple sequence repeats (SSRs) and single nucleotide polymorphisms (SNPs) were searched, resulting in 52,834 SSRs and 36,411 SNPs. All of these are available through the Oak Contig Browser
This genomic resource provides a unique tool to discover genes of interest, study the oak transcriptome, and develop new markers to investigate functional diversity in natural populations.
PMCID: PMC3017864  PMID: 21092232

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