Publications by authors named "Etienne G J Danchin"

69 Publications

Author Correction: Horizontal Gene Transfer of Pectinases from Bacteria Preceded the Diversification of Stick and Leaf Insects.

Sci Rep 2021 Jul 26;11(1):15515. Epub 2021 Jul 26.

Department of Entomology, Max-Planck Institute für chemische Ökologie, Hans-Knöll-Str. 8, 07745, Jena, Germany.

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http://dx.doi.org/10.1038/s41598-021-94743-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8313565PMC
July 2021

Movements of transposable elements contribute to the genomic plasticity and species diversification in an asexually reproducing nematode pest.

Evol Appl 2021 Jul 15;14(7):1844-1866. Epub 2021 May 15.

Université Côte d'Azur INRAE CNRS ISA Sophia Antipolis France.

Despite reproducing without sexual recombination, is an adaptive and versatile phytoparasitic nematode. This species displays a global distribution, can parasitize a large range of plants, and can overcome plant resistance in a few generations. The mechanisms underlying this adaptability remain poorly known. At the whole-genome level, only a few single nucleotide variations have been observed across different geographical isolates with distinct ranges of compatible hosts. Exploring other factors possibly involved in genomic plasticity is thus important. Transposable elements (TEs), by their repetitive nature and mobility, can passively and actively impact the genome dynamics. This is particularly expected in polyploid hybrid genomes such as the one of . . Here, we have annotated the TE content of . , analyzed the statistical properties of this TE landscape, and used whole-genome pool-seq data to estimate the mobility of these TEs across twelve geographical isolates, presenting variations in ranges of compatible host plants. DNA transposons are more abundant than retrotransposons, and the high similarity of TE copies to their consensus sequences suggests they have been at least recently active. We have identified loci in the genome where the frequencies of presence of a TE showed substantial variations across the different isolates. Overall, variations in TE frequencies across isolates followed their phylogenetic divergence, suggesting TEs participate in the species diversification. Compared with the .  reference genome, we detected isolate and lineage-specific de novo insertion of some TEs, including within genic regions or in the upstream regulatory regions. We validated by PCR the insertion of some of these TEs inside genic regions, confirming TE movements have possible functional impacts. Overall, we show DNA transposons can drive genomic plasticity in .  and their role in genome evolution of other parthenogenetic animal deserves further investigation.
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http://dx.doi.org/10.1111/eva.13246DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8288018PMC
July 2021

Genome Expression Dynamics Reveal the Parasitism Regulatory Landscape of the Root-Knot Nematode and a Promoter Motif Associated with Effector Genes.

Genes (Basel) 2021 05 18;12(5). Epub 2021 May 18.

INRAE, Institut Sophia Agrobiotech, Université Côte d'Azur, CNRS, 06903 Sophia Antipolis, France.

Root-knot nematodes (genus ) are the major contributor to crop losses caused by nematodes. These nematodes secrete effector proteins into the plant, derived from two sets of pharyngeal gland cells, to manipulate host physiology and immunity. Successful completion of the life cycle, involving successive molts from egg to adult, covers morphologically and functionally distinct stages and will require precise control of gene expression, including effector genes. The details of how root-knot nematodes regulate transcription remain sparse. Here, we report a life stage-specific transcriptome of . Combined with an available annotated genome, we explore the spatio-temporal regulation of gene expression. We reveal gene expression clusters and predicted functions that accompany the major developmental transitions. Focusing on effectors, we identify a putative cis-regulatory motif associated with expression in the dorsal glands, providing an insight into effector regulation. We combine the presence of this motif with several other criteria to predict a novel set of putative dorsal gland effectors. Finally, we show this motif, and thereby its utility, is broadly conserved across the genus, and we name it Mel-DOG. Taken together, we provide the first genome-wide analysis of spatio-temporal gene expression in a root-knot nematode and identify a new set of candidate effector genes that will guide future functional analyses.
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http://dx.doi.org/10.3390/genes12050771DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8158474PMC
May 2021

Dissecting protein domain variability in the core RNA interference machinery of five insect orders.

RNA Biol 2020 Dec 31:1-29. Epub 2020 Dec 31.

Plant-Pest Molecular Interaction Laboratory (LIMPP), Brasilia, Brasília-DF, Brazil.

RNA interference (RNAi)-mediated gene silencing can be used to control specific insect pest populations. Unfortunately, the variable efficiency in the knockdown levels of target genes has narrowed the applicability of this technology to a few species. Here, we examine the current state of knowledge regarding the miRNA (micro RNA) and siRNA (small interfering RNA) pathways in insects and investigate the structural variability at key protein domains of the RNAi machinery. Our goal was to correlate domain variability with mechanisms affecting the gene silencing efficiency. To this end, the protein domains of 168 insect species, encompassing the orders Coleoptera, Diptera, Hemiptera, Hymenoptera, and Lepidoptera, were analysed using our pipeline, which takes advantage of meticulous structure-based sequence alignments. We used phylogenetic inference and the evolutionary rate coefficient () to outline the variability across domain regions and surfaces. Our results show that four domains, namely dsrm, Helicase, PAZ and Ribonuclease III, are the main contributors of protein variability in the RNAi machinery across different insect orders. We discuss the potential roles of these domains in regulating RNAi-mediated gene silencing and the role of loop regions in fine-tuning RNAi efficiency. Additionally, we identified several order-specific singularities which indicate that lepidopterans have evolved differently from other insect orders, possibly due to constant coevolution with plants and viruses. In conclusion, our results highlight several variability hotspots that deserve further investigation in order to improve the application of RNAi technology in the control of insect pests.
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http://dx.doi.org/10.1080/15476286.2020.1861816DOI Listing
December 2020

Comparative Genomics Reveals Novel Target Genes towards Specific Control of Plant-Parasitic Nematodes.

Genes (Basel) 2020 11 13;11(11). Epub 2020 Nov 13.

INRAE, Plant Health and Environment, University Côte d'Azur, CNRS, ISA, F-06903 Sophia-Antipolis CEDEX, France.

Plant-parasitic nematodes cause extensive annual yield losses to worldwide agricultural production. Most cultivated plants have no known resistance against nematodes and the few bearing a resistance gene can be overcome by certain species. Chemical methods that have been deployed to control nematodes have largely been banned from use due to their poor specificity and high toxicity. Hence, there is an urgent need for the development of cleaner and more specific control methods. Recent advances in nematode genomics, including in phytoparasitic species, provide an unprecedented opportunity to identify genes and functions specific to these pests. Using phylogenomics, we compared 61 nematode genomes, including 16 for plant-parasitic species and identified more than 24,000 protein families specific to these parasites. In the genome of , one of the most devastating plant parasites, we found ca. 10,000 proteins with orthologs restricted only to phytoparasitic species and no further homology in protein databases. Among these phytoparasite-specific proteins, ca. 1000 shared the same properties as known secreted effectors involved in essential parasitic functions. Of these, 68 were novel and showed strong expression during the endophytic phase of the nematode life cycle, based on both RNA-seq and RT-qPCR analyses. Besides effector candidates, transcription-related and neuro-perception functions were enriched in phytoparasite-specific proteins, revealing interesting targets for nematode control methods. This phylogenomics analysis constitutes a unique resource for the further understanding of the genetic basis of nematode adaptation to phytoparasitism and for the development of more efficient control methods.
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http://dx.doi.org/10.3390/genes11111347DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7696266PMC
November 2020

Recent Advances in Population Genomics of Plant-Parasitic Nematodes.

Phytopathology 2021 Jan 18;111(1):40-48. Epub 2020 Dec 18.

IGEPP, INRAE, Institut Agro, Univ Rennes, 35650, Le Rheu, France.

Plant-parasitic nematodes are a costly burden of crop production. Ubiquitous in nature, phytoparasitic nematodes are associated with nearly every important agricultural crop and represent a significant constraint on global food security. Population genetics is a key discipline in plant nematology to understand aspects of the life strategies of these parasites, in particular their modes of reproduction, geographic origins, evolutionary histories, and dispersion abilities. Advances in high-throughput sequencing technologies have enabled a recent but active effort in genomic analyses of plant-parasitic nematodes. Such genomic approaches applied to multiple populations are providing new insights into the molecular and evolutionary processes that underpin the establishment of these nematodes and into a better understanding of the genetic and mechanistic basis of their pathogenicity and adaptation to their host plants. In this review, we attempt to update information about genome resources and genotyping techniques useful for nematologists who are thinking about initiating population genomics or genome sequencing projects. This review is intended also to foster the development of population genomics in plant-parasitic nematodes through highlighting recent publications that illustrate the potential for this approach to identify novel molecular markers or genes of interest and improve our knowledge of the genome variability, pathogenicity, and evolutionary potential of plant-parasitic nematodes.
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http://dx.doi.org/10.1094/PHYTO-09-20-0418-RVWDOI Listing
January 2021

Genome structure and content of the rice root-knot nematode ().

Ecol Evol 2020 Oct 13;10(20):11006-11021. Epub 2020 Sep 13.

IRD-CIRAD-University of Montpellier UMR Interactions Plantes Microorganismes Environnement (IPME) Montpellier France.

Discovered in the 1960s, is a root-knot nematode species considered as a major threat to rice production. Yet, its origin, genomic structure, and intraspecific diversity are poorly understood. So far, such studies have been limited by the unavailability of a sufficiently complete and well-assembled genome. In this study, using a combination of Oxford Nanopore Technologies and Illumina sequencing data, we generated a highly contiguous reference genome (283 scaffolds with an N50 length of 294 kb, totaling 41.5 Mb). The completeness scores of our assembly are among the highest currently published for genomes. We predicted 10,284 protein-coding genes spanning 75.5% of the genome. Among them, 67 are identified as possibly originating from horizontal gene transfers (mostly from bacteria), which supposedly contribute to nematode infection, nutrient processing, and plant defense manipulation. Besides, we detected 575 canonical transposable elements (TEs) belonging to seven orders and spanning 2.61% of the genome. These TEs might promote genomic plasticity putatively related to the evolution of parasitism. This high-quality genome assembly constitutes a major improvement regarding previously available versions and represents a valuable molecular resource for future phylogenomic studies of species. In particular, this will foster comparative genomic studies to trace back the evolutionary history of .  and its closest relatives.
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http://dx.doi.org/10.1002/ece3.6680DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593179PMC
October 2020

Genome assembly and annotation of Meloidogyne enterolobii, an emerging parthenogenetic root-knot nematode.

Sci Data 2020 10 5;7(1):324. Epub 2020 Oct 5.

Université Côte d'Azur, INRAE, CNRS, Institut Sophia Agrobiotech, Sophia Antipolis, France.

Root-knot nematodes (genus Meloidogyne) are plant parasites causing huge economic loss in the agricultural industry and affecting severely numerous developing countries. Control methods against these plant pests are sparse, the preferred one being the deployment of plant cultivars bearing resistance genes against Meloidogyne species. However, M. enterolobii is not controlled by the resistance genes deployed in the crop plants cultivated in Europe. The recent identification of this species in Europe is thus a major concern. Here, we sequenced the genome of M. enterolobii using short and long-read technologies. The genome assembly spans 240 Mbp with contig N50 size of 143 kbp, enabling high-quality annotations of 59,773 coding genes, 4,068 non-coding genes, and 10,944 transposable elements (spanning 8.7% of the genome). We validated the genome size by flow cytometry and the structure, quality and completeness by bioinformatics metrics. This ensemble of resources will fuel future projects aiming at pinpointing the genome singularities, the origin, diversity, and adaptive potential of this emerging plant pest.
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http://dx.doi.org/10.1038/s41597-020-00666-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536185PMC
October 2020

Characterization of raffinose metabolism genes uncovers a wild Arachis galactinol synthase conferring tolerance to abiotic stresses.

Sci Rep 2020 09 17;10(1):15258. Epub 2020 Sep 17.

EMBRAPA Recursos Genéticos e Biotecnologia. Parque Estação Biológica, Final W5 Norte, Brasília, DF, CP 02372, Brazil.

Raffinose family oligosaccharides (RFOs) are implicated in plant regulatory mechanisms of abiotic stresses tolerance and, despite their antinutritional proprieties in grain legumes, little information is available about the enzymes involved in RFO metabolism in Fabaceae species. In the present study, the systematic survey of legume proteins belonging to five key enzymes involved in the metabolism of RFOs (galactinol synthase, raffinose synthase, stachyose synthase, alpha-galactosidase, and beta-fructofuranosidase) identified 28 coding-genes in Arachis duranensis and 31 in A. ipaënsis. Their phylogenetic relationships, gene structures, protein domains, and chromosome distribution patterns were also determined. Based on the expression profiling of these genes under water deficit treatments, a galactinol synthase candidate gene (AdGolS3) was identified in A. duranensis. Transgenic Arabidopsis plants overexpressing AdGolS3 exhibited increased levels of raffinose and reduced stress symptoms under drought, osmotic, and salt stresses. Metabolite and expression profiling suggested that AdGolS3 overexpression was associated with fewer metabolic perturbations under drought stress, together with better protection against oxidative damage. Overall, this study enabled the identification of a promising GolS candidate gene for metabolic engineering of sugars to improve abiotic stress tolerance in crops, whilst also contributing to the understanding of RFO metabolism in legume species.
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http://dx.doi.org/10.1038/s41598-020-72191-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7498584PMC
September 2020

Evolutionarily conserved plant genes responsive to root-knot nematodes identified by comparative genomics.

Mol Genet Genomics 2020 Jul 24;295(4):1063-1078. Epub 2020 Apr 24.

EMBRAPA Recursos Genéticos e Biotecnologia, Brasília-DF, Brazil.

Root-knot nematodes (RKNs, genus Meloidogyne) affect a large number of crops causing severe yield losses worldwide, more specifically in tropical and sub-tropical regions. Several plant species display high resistance levels to Meloidogyne, but a general view of the plant immune molecular responses underlying resistance to RKNs is still lacking. Combining comparative genomics with differential gene expression analysis may allow the identification of widely conserved plant genes involved in RKN resistance. To identify genes that are evolutionary conserved across plant species, we used OrthoFinder to compared the predicted proteome of 22 plant species, including important crops, spanning 214 Myr of plant evolution. Overall, we identified 35,238 protein orthogroups, of which 6,132 were evolutionarily conserved and universal to all the 22 plant species (PLAnts Common Orthogroups-PLACO). To identify host genes responsive to RKN infection, we analyzed the RNA-seq transcriptome data from RKN-resistant genotypes of a peanut wild relative (Arachis stenosperma), coffee (Coffea arabica L.), soybean (Glycine max L.), and African rice (Oryza glaberrima Steud.) challenged by Meloidogyne spp. using EdgeR and DESeq tools, and we found 2,597 (O. glaberrima), 743 (C. arabica), 665 (A. stenosperma), and 653 (G. max) differentially expressed genes (DEGs) during the resistance response to the nematode. DEGs' classification into the previously characterized 35,238 protein orthogroups allowed identifying 17 orthogroups containing at least one DEG of each resistant Arachis, coffee, soybean, and rice genotype analyzed. Orthogroups contain 364 DEGs related to signaling, secondary metabolite production, cell wall-related functions, peptide transport, transcription regulation, and plant defense, thus revealing evolutionarily conserved RKN-responsive genes. Interestingly, the 17 DEGs-containing orthogroups (belonging to the PLACO) were also universal to the 22 plant species studied, suggesting that these core genes may be involved in ancestrally conserved immune responses triggered by RKN infection. The comparative genomic approach that we used here represents a promising predictive tool for the identification of other core plant defense-related genes of broad interest that are involved in different plant-pathogen interactions.
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http://dx.doi.org/10.1007/s00438-020-01677-7DOI Listing
July 2020

Genome sequence of the root-knot nematode .

J Nematol 2020 ;52:1-5

Agricultural Institute of Slovenia, Plant Protection Department, Ljubljana, Slovenia.

Root-knot nematodes from the genus are polyphagous plant endoparasites and agricultural pests of global importance. Here, we report the high-quality genome sequence of population SI-Smartno V13. The resulting genome assembly of SI-Smartno V13 consists of 327 contigs, with an N50 contig length of 1,711,905 bp and a total assembly length of 209.16 Mb.

Root-knot nematodes from the genus are polyphagous plant endoparasites and agricultural pests of global importance. Here, we report the high-quality genome sequence of population SI-Smartno V13. The resulting genome assembly of SI-Smartno V13 consists of 327 contigs, with an N50 contig length of 1,711,905 bp and a total assembly length of 209.16 Mb.
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http://dx.doi.org/10.21307/jofnem-2020-025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7266024PMC
January 2020

Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest.

Evol Appl 2020 Feb 6;13(2):442-457. Epub 2019 Nov 6.

INRA Université Côte d'Azur CNRS ISA Sophia Antipolis France.

The root-knot nematodes are the most devastating worms to worldwide agriculture with being the most widely distributed and damaging species. This parasitic and ecological success seems surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been suspected based on cytological observations but, so far, never confirmed by population genomics data. As a species, is highly polyphagous with thousands of host plants. However, different isolates present distinct and overlapping patterns of host compatibilities. Historically, four "host races" had been defined as a function of ranges of compatible and incompatible plants. In this study, we used population genomics to assess whether (a) reproduction is actually clonal in this species, (b) the host races follow an underlying phylogenetic signal or, rather represent multiple independent transitions, and (c) how genome variations associate with other important biological traits such as the affected crops and geographical distribution. We sequenced the genomes of 11 isolates across Brazil that covered the four host races in replicates. By aligning the genomic reads of these isolates to the reference genome assembly, we identified point variations. Analysis of linkage disequilibrium and 4-gametes test showed no evidence for recombination, corroborating the clonal reproduction of . The few point variations between the isolates showed no significant association with the host races, the geographical origin of the samples, or the crop on which they have been collected. Addition of isolates from other locations around the world confirmed this lack of underlying phylogenetic signal. This suggests multiple gains and losses of parasitic abilities and adaptations to different environments account for the broad host spectrum and wide geographical distribution of and thus to its high economic impact. This surprising adaptability without sex poses both evolutionary and agro-economic challenges.
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http://dx.doi.org/10.1111/eva.12881DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976969PMC
February 2020

Signatures of the Evolution of Parthenogenesis and Cryptobiosis in the Genomes of Panagrolaimid Nematodes.

iScience 2019 Nov 24;21:587-602. Epub 2019 Oct 24.

Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh EH9 3FL, UK; Edinburgh Genomics, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK.

Most animal species reproduce sexually and fully parthenogenetic lineages are usually short lived in evolution. Still, parthenogenesis may be advantageous as it avoids the cost of sex and permits colonization by single individuals. Panagrolaimid nematodes have colonized environments ranging from arid deserts to Arctic and Antarctic biomes. Many are obligatory meiotic parthenogens, and most have cryptobiotic abilities, being able to survive repeated cycles of complete desiccation and freezing. To identify systems that may contribute to these striking abilities, we sequenced and compared the genomes and transcriptomes of parthenogenetic and outcrossing panagrolaimid species, including cryptobionts and non-cryptobionts. The parthenogens are triploids, most likely originating through hybridization. Adaptation to cryptobiosis shaped the genomes of panagrolaimid nematodes and is associated with the expansion of gene families and signatures of selection on genes involved in cryptobiosis. All panagrolaimids have acquired genes through horizontal gene transfer, some of which are likely to contribute to cryptobiosis.
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http://dx.doi.org/10.1016/j.isci.2019.10.039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6889759PMC
November 2019

A Chemosensory GPCR as a Potential Target to Control the Root-Knot Nematode Parasitism in Plants.

Molecules 2019 Oct 22;24(20). Epub 2019 Oct 22.

EMBRAPA Genetic Resources and Biotechnology, Brasilia 70770-917, DF, Brazil.

Root-knot nematodes (RKN), from the genus, have a worldwide distribution and cause severe economic damage to many life-sustaining crops. Because of their lack of specificity and danger to the environment, most chemical nematicides have been banned from use. Thus, there is a great need for new and safe compounds to control RKN. Such research involves identifying beforehand the nematode proteins essential to the invasion. Since G protein-coupled receptors GPCRs are the target of a large number of drugs, we have focused our research on the identification of putative nematode GPCRs such as those capable of controlling the movement of the parasite towards (or within) its host. A datamining procedure applied to the genome of allowed us to identify a GPCR, belonging to the neuropeptide GPCR family that can serve as a target to carry out a virtual screening campaign. We reconstructed a 3D model of this receptor by homology modeling and validated it through extensive molecular dynamics simulations. This model was used for large scale molecular dockings which produced a filtered limited set of putative antagonists for this GPCR. Preliminary experiments using these selected molecules allowed the identification of an active compound, namely C260-2124, from the ChemDiv provider, which can serve as a starting point for further investigations.
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http://dx.doi.org/10.3390/molecules24203798DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6832152PMC
October 2019

Cross-Kingdom Analysis of Diversity, Evolutionary History, and Site Selection within the Eukaryotic Macrophage Migration Inhibitory Factor Superfamily.

Genes (Basel) 2019 09 24;10(10). Epub 2019 Sep 24.

Institut Sophia Agrobiotech, Université Côte d'Azur, INRA, CNRS, 400 Route des Chappes, F-06903 Sophia Antipolis, France.

Macrophage migration inhibitory factors (MIF) are multifunctional proteins regulating major processes in mammals, including activation of innate immune responses. MIF proteins also play a role in innate immunity of invertebrate organisms or serve as virulence factors in parasitic organisms, raising the question of their evolutionary history. We performed a broad survey of MIF presence or absence and evolutionary relationships across 803 species of plants, fungi, protists, and animals, and explored a potential relation with the taxonomic status, the ecology, and the lifestyle of individual species. We show that MIF evolutionary history in eukaryotes is complex, involving probable ancestral duplications, multiple gene losses and recent clade-specific re-duplications. Intriguingly, MIFs seem to be essential and highly conserved with many sites under purifying selection in some kingdoms (e.g., plants), while in other kingdoms they appear more dispensable (e.g., in fungi) or present in several diverged variants (e.g., insects, nematodes), suggesting potential neofunctionalizations within the protein superfamily.
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http://dx.doi.org/10.3390/genes10100740DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6826473PMC
September 2019

Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles.

BMC Evol Biol 2019 05 10;19(1):100. Epub 2019 May 10.

Entomology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745, Jena, Germany.

Background: Cellulose, a major polysaccharide of the plant cell wall, consists of β-1,4-linked glucose moieties forming a molecular network recalcitrant to enzymatic breakdown. Although cellulose is potentially a rich source of energy, the ability to degrade it is rare in animals and was believed to be present only in cellulolytic microbes. Recently, it has become clear that some animals encode endogenous cellulases belonging to several glycoside hydrolase families (GHs), including GH45. GH45s are distributed patchily among the Metazoa and, in insects, are encoded only by the genomes of Phytophaga beetles. This study aims to understand both the enzymatic functions and the evolutionary history of GH45s in these beetles.

Results: To this end, we biochemically assessed the enzymatic activities of 37 GH45s derived from five species of Phytophaga beetles and discovered that beetle-derived GH45s degrade three different substrates: amorphous cellulose, xyloglucan and glucomannan. Our phylogenetic and gene structure analyses indicate that at least one gene encoding a putative cellulolytic GH45 was present in the last common ancestor of the Phytophaga, and that GH45 xyloglucanases evolved several times independently in these beetles. The most closely related clade to Phytophaga GH45s was composed of fungal sequences, suggesting this GH family was acquired by horizontal gene transfer from fungi. Besides the insects, other arthropod GH45s do not share a common origin and appear to have emerged at least three times independently.

Conclusion: The rise of functional innovation from gene duplication events has been a fundamental process in the evolution of GH45s in Phytophaga beetles. Both, enzymatic activity and ancestral origin suggest that GH45s were likely an essential prerequisite for the adaptation allowing Phytophaga beetles to feed on plants.
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http://dx.doi.org/10.1186/s12862-019-1429-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6509783PMC
May 2019

Contrasting Effects of Wild Dehydrin Under Abiotic and Biotic Stresses.

Front Plant Sci 2019 18;10:497. Epub 2019 Apr 18.

EMBRAPA Recursos Genéticos e Biotecnologia, Brasília, Brazil.

Plant dehydrins (DNHs) belong to the LEA (Late Embryogenesis Abundant) protein family and are involved in responses to multiple abiotic stresses. DHNs are classified into five subclasses according to the organization of three conserved motifs (K-; Y-; and S-segments). In the present study, the DHN protein family was characterized by molecular phylogeny, exon/intron organization, protein structure, and tissue-specificity expression in eight Fabaceae species. We identified 20 DHN genes, encompassing three (YSK, SK, and K) subclasses sharing similar gene organization and protein structure. Two additional low conserved DHN Φ-segments specific to the legume SK-type of proteins were also found. The expression patterns of DHN genes in four legume species (, and ) revealed that their tissue-specific regulation is associated with the presence or absence of the Y-segment. Indeed, DHN genes containing a Y-segment are mainly expressed in seeds, whereas those without the Y-segment are ubiquitously expressed. Further qRT-PCR analysis revealed that, amongst stress responsive dehydrins, a SK-type DHN gene from () showed opposite response to biotic and abiotic stress with a positive regulation under water deficit and negative regulation upon nematode infection. Furthermore, transgenic lines overexpressing (OE) displayed improved tolerance to multiple abiotic stresses (freezing and drought) but increased susceptibility to the biotrophic root-knot nematode (RKN) . This contradictory role of in responses to abiotic and biotic stresses was further investigated by qRT-PCR analysis of transgenic plants using a set of stress-responsive genes involved in the abscisic acid (ABA) and jasmonic acid (JA) signaling pathways and suggested an involvement of DHN overexpression in these stress-signaling pathways.
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http://dx.doi.org/10.3389/fpls.2019.00497DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6482428PMC
April 2019

Gene copy number variations as signatures of adaptive evolution in the parthenogenetic, plant-parasitic nematode Meloidogyne incognita.

Mol Ecol 2019 05 29;28(10):2559-2572. Epub 2019 Apr 29.

INRA, Université Côte d'Azur, CNRS, ISA, Sophia Antipolis, France.

Adaptation to changing environmental conditions represents a challenge to parthenogenetic organisms, and until now, how phenotypic variants are generated in clones in response to the selection pressure of their environment remains poorly known. The obligatory parthenogenetic root-knot nematode species Meloidogyne incognita has a worldwide distribution and is the most devastating plant-parasitic nematode. Despite its asexual reproduction, this species exhibits an unexpected capacity of adaptation to environmental constraints, for example, resistant hosts. Here, we used a genomewide comparative hybridization strategy to evaluate variations in gene copy numbers between genotypes of M. incognita resulting from two parallel experimental evolution assays on a susceptible vs. resistant host plant. We detected gene copy number variations (CNVs) associated with the ability of the nematodes to overcome resistance of the host plant, and this genetic variation may reflect an adaptive response to host resistance in this parthenogenetic species. The CNV distribution throughout the nematode genome is not random and suggests the occurrence of genomic regions more prone to undergo duplications and losses in response to the selection pressure of the host resistance. Furthermore, our analysis revealed an outstanding level of gene loss events in nematode genotypes that have overcome the resistance. Overall, our results support the view that gene loss could be a common class of adaptive genetic mechanism in response to a challenging new biotic environment in clonal animals.
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http://dx.doi.org/10.1111/mec.15095DOI Listing
May 2019

Comparative root transcriptome of wild Arachis reveals NBS-LRR genes related to nematode resistance.

BMC Plant Biol 2018 Aug 6;18(1):159. Epub 2018 Aug 6.

EMBRAPA Genetic Resources and Biotechnology, Brasilia, DF, Brazil.

Background: The Root-Knot Nematode (RKN), Meloidogyne arenaria, significantly reduces peanut grain quality and yield worldwide. Whilst the cultivated species has low levels of resistance to RKN and other pests and diseases, peanut wild relatives (Arachis spp.) show rich genetic diversity and harbor high levels of resistance to many pathogens and environmental constraints. Comparative transcriptome analysis can be applied to identify candidate resistance genes.

Results: Transcriptome analysis during the early stages of RKN infection of two peanut wild relatives, the highly RKN resistant Arachis stenosperma and the moderately susceptible A. duranensis, revealed genes related to plant immunity with contrasting expression profiles. These included genes involved in hormone signaling and secondary metabolites production and also members of the NBS-LRR class of plant disease resistance (R) genes. From 345 NBS-LRRs identified in A.duranensis reference genome, 52 were differentially expressed between inoculated and control samples, with the majority occurring in physical clusters unevenly distributed on eight chromosomes with preferential tandem duplication. The majority of these NBS-LRR genes showed contrasting expression behaviour between A. duranensis and A. stenosperma, particularly at 6 days after nematode inoculation, coinciding with the onset of the Hypersensitive Response in the resistant species. The physical clustering of some of these NBS-LRR genes correlated with their expression patterns in the contrasting genotypes. Four NBS-LRR genes exclusively expressed in A. stenosperma are located within clusters on chromosome Aradu. A09, which harbors a QTL for RKN resistance, suggesting a functional role for their physical arrangement and their potential involvement in this defense response.

Conclusion: The identification of functional novel R genes in wild Arachis species responsible for triggering effective defense cascades can contribute to the crop genetic improvement and enhance peanut resilience to RKN.
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http://dx.doi.org/10.1186/s12870-018-1373-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080386PMC
August 2018

Genome-wide expert annotation of the epigenetic machinery of the plant-parasitic nematodes Meloidogyne spp., with a focus on the asexually reproducing species.

BMC Genomics 2018 May 3;19(1):321. Epub 2018 May 3.

Université Côte d'Azur, INRA, ISA, Sophia Antipolis, France.

Background: The renewed interest in epigenetics has led to the understanding that both the environment and individual lifestyle can directly interact with the epigenome to influence its dynamics. Epigenetic phenomena are mediated by DNA methylation, stable chromatin modifications and non-coding RNA-associated gene silencing involving specific proteins called epigenetic factors. Multiple organisms, ranging from plants to yeast and mammals, have been used as model systems to study epigenetics. The interactions between parasites and their hosts are models of choice to study these mechanisms because the selective pressures are strong and the evolution is fast. The asexually reproducing root-knot nematodes (RKN) offer different advantages to study the processes and mechanisms involved in epigenetic regulation. RKN genomes sequencing and annotation have identified numerous genes, however, which of those are involved in the adaption to an environment and potentially relevant to the evolution of plant-parasitism is yet to be discovered.

Results: Here, we used a functional comparative annotation strategy combining orthology data, mining of curated genomics as well as protein domain databases and phylogenetic reconstructions. Overall, we show that (i) neither RKN, nor the model nematode Caenorhabditis elegans possess any DNA methyltransferases (DNMT) (ii) RKN do not possess the complete machinery for DNA methylation on the 6th position of adenine (6mA) (iii) histone (de)acetylation and (de)methylation pathways are conserved between C. elegans and RKN, and the corresponding genes are amplified in asexually reproducing RKN (iv) some specific non-coding RNA families found in plant-parasitic nematodes are dissimilar from those in C. elegans. In the asexually reproducing RKN Meloidogyne incognita, expression data from various developmental stages supported the putative role of these proteins in epigenetic regulations.

Conclusions: Our results refine previous predictions on the epigenetic machinery of model species and constitute the most comprehensive description of epigenetic factors relevant to the plant-parasitic lifestyle and/or asexual mode of reproduction of RKN. Providing an atlas of epigenetic factors in RKN is an informative resource that will enable researchers to explore their potential role in adaptation of these parasites to their environment.
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http://dx.doi.org/10.1186/s12864-018-4686-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5934874PMC
May 2018

The Transcriptomes of Xiphinema index and Longidorus elongatus Suggest Independent Acquisition of Some Plant Parasitism Genes by Horizontal Gene Transfer in Early-Branching Nematodes.

Genes (Basel) 2017 Oct 23;8(10). Epub 2017 Oct 23.

Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK.

Nematodes have evolved the ability to parasitize plants on at least four independent occasions, with plant parasites present in Clades 1, 2, 10 and 12 of the phylum. In the case of Clades 10 and 12, horizontal gene transfer of plant cell wall degrading enzymes from bacteria and fungi has been implicated in the evolution of plant parasitism. We have used ribonucleic acid sequencing (RNAseq) to generate reference transcriptomes for two economically important nematode species, and , representative of two genera within the early-branching Clade 2 of the phylum Nematoda. We used a transcriptome-wide analysis to identify putative horizontal gene transfer events. This represents the first in-depth transcriptome analysis from any plant-parasitic nematode of this clade. For each species, we assembled ~30 million Illumina reads into a reference transcriptome. We identified 62 and 104 transcripts, from and , respectively, that were putatively acquired via horizontal gene transfer. By cross-referencing horizontal gene transfer prediction with a phylum-wide analysis of Pfam domains, we identified Clade 2-specific events. Of these, a GH12 cellulase from was analysed phylogenetically and biochemically, revealing a likely bacterial origin and canonical enzymatic function. Horizontal gene transfer was previously shown to be a phenomenon that has contributed to the evolution of plant parasitism among nematodes. Our findings underline the importance and the extensiveness of this phenomenon in the evolution of plant-parasitic life styles in this speciose and widespread animal phylum.
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http://dx.doi.org/10.3390/genes8100287DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5664137PMC
October 2017

Alienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life.

Genes (Basel) 2017 Sep 29;8(10). Epub 2017 Sep 29.

INRA, CNRS, ISA, Université Côte d'Azur, 06903 Sophia Antipolis Cedex, France.

Horizontal gene transfer (HGT) is the transmission of genes between organisms by other means than parental to offspring inheritance. While it is prevalent in prokaryotes, HGT is less frequent in eukaryotes and particularly in Metazoa. Here, we propose Alienness, a taxonomy-aware web application available at http://alienness.sophia.inra.fr. Alienness parses BLAST results against public libraries to rapidly identify candidate HGT in any genome of interest. Alienness takes as input the result of a BLAST of a whole proteome of interest against any National Center for Biotechnology Information (NCBI) protein library. The user defines recipient (e.g., Metazoa) and donor (e.g., bacteria, fungi) branches of interest in the NCBI taxonomy. Based on the best BLAST E-values of candidate donor and recipient taxa, Alienness calculates an Alien Index (AI) for each query protein. An AI > 0 indicates a better hit to candidate donor than recipient taxa and a possible HGT. Higher AI represent higher gap of E-values between candidate donor and recipient and a more likely HGT. We confirmed the accuracy of Alienness on phylogenetically confirmed HGT of non-metazoan origin in plant-parasitic nematodes. Alienness scans whole proteomes to rapidly identify possible HGT in any species of interest and thus fosters exploration of HGT more easily and largely across the tree of life.
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http://dx.doi.org/10.3390/genes8100248DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5664098PMC
September 2017

Prospects of herbivore egg-killing plant defenses for sustainable crop protection.

Ecol Evol 2016 10 7;6(19):6906-6918. Epub 2016 Sep 7.

Department of Agricultural and Forest Sciences University of Palermo Viale delle Scienze edificio 5 90128 Palermo Italy.

Due to a growing demand of food production worldwide, new strategies are suggested to allow for sustainable production of food with minimal effects on natural resources. A promising alternative to the application of chemical pesticides is the implementation of crops resistant to insect pests. Plants produce compounds that are harmful to a wide range of attackers, including insect pests; thus, exploitation of their natural defense system can be the key for the development of pest-resistant crops. Interestingly, some plants possess a unique first line of defense that eliminates the enemy before it becomes destructive: egg-killing. Insect eggs can trigger (1) direct defenses, mostly including plant cell tissue growth or cell death that lead to eggs desiccating, being crushed or falling off the plant or (2) indirect defenses, plant chemical cues recruiting natural enemies that kill the egg or hatching larvae (parasitoids). The consequences of plant responses to eggs are that insect larvae do not hatch or that they are impeded in development, and damage to the plant is reduced. Here, we provide an overview on the ubiquity and evolutionary history of egg-killing traits within the plant kingdom including crops. Up to now, little is known on the mechanisms and on the genetic basis of egg-killing traits. Making use of egg-killing defense traits in crops is a promising new way to sustainably reduce losses of crop yield. We provide suggestions for new breeding strategies to grow egg-killing crops and improve biological control.
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http://dx.doi.org/10.1002/ece3.2365DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513223PMC
October 2016

Hybridization and polyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes.

PLoS Genet 2017 06 8;13(6):e1006777. Epub 2017 Jun 8.

INRA, Université Côte d'Azur, CNRS, ISA, France.

Root-knot nematodes (genus Meloidogyne) exhibit a diversity of reproductive modes ranging from obligatory sexual to fully asexual reproduction. Intriguingly, the most widespread and devastating species to global agriculture are those that reproduce asexually, without meiosis. To disentangle this surprising parasitic success despite the absence of sex and genetic exchanges, we have sequenced and assembled the genomes of three obligatory ameiotic and asexual Meloidogyne. We have compared them to those of relatives able to perform meiosis and sexual reproduction. We show that the genomes of ameiotic asexual Meloidogyne are large, polyploid and made of duplicated regions with a high within-species average nucleotide divergence of ~8%. Phylogenomic analysis of the genes present in these duplicated regions suggests that they originated from multiple hybridization events and are thus homoeologs. We found that up to 22% of homoeologous gene pairs were under positive selection and these genes covered a wide spectrum of predicted functional categories. To biologically assess functional divergence, we compared expression patterns of homoeologous gene pairs across developmental life stages using an RNAseq approach in the most economically important asexually-reproducing nematode. We showed that >60% of homoeologous gene pairs display diverged expression patterns. These results suggest a substantial functional impact of the genome structure. Contrasting with high within-species nuclear genome divergence, mitochondrial genome divergence between the three ameiotic asexuals was very low, signifying that these putative hybrids share a recent common maternal ancestor. Transposable elements (TE) cover a ~1.7 times higher proportion of the genomes of the ameiotic asexual Meloidogyne compared to the sexual relative and might also participate in their plasticity. The intriguing parasitic success of asexually-reproducing Meloidogyne species could be partly explained by their TE-rich composite genomes, resulting from allopolyploidization events, and promoting plasticity and functional divergence between gene copies in the absence of sex and meiosis.
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http://dx.doi.org/10.1371/journal.pgen.1006777DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5465968PMC
June 2017

Genome-wide analysis of expansin superfamily in wild Arachis discloses a stress-responsive expansin-like B gene.

Plant Mol Biol 2017 May 27;94(1-2):79-96. Epub 2017 Feb 27.

Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, Final W5 Norte, Brasília, DF, CP 02372, Brazil.

Expansins are plant cell wall-loosening proteins involved in adaptive responses to environmental stimuli and various developmental processes. The first genome-wide analysis of the expansin superfamily in the Arachis genus identified 40 members in A. duranensis and 44 in A. ipaënsis, the wild progenitors of cultivated peanut (A. hypogaea). These expansins were further characterized regarding their subfamily classification, distribution along the genomes, duplication events, molecular structure, and phylogeny. A RNA-seq expression analysis in different Arachis species showed that the majority of these expansins are modulated in response to diverse stresses such as water deficit, root-knot nematode (RKN) infection, and UV exposure, with an expansin-like B gene (AraEXLB8) displaying a highly distinct stress-responsive expression profile. Further analysis of the AraEXLB8 coding sequences showed high conservation across the Arachis genotypes, with eight haplotypes identified. The modulation of AraEXLB8 expression in response to the aforementioned stresses was confirmed by qRT-PCR analysis in distinct Arachis genotypes, whilst in situ hybridization revealed transcripts in different root tissues according to the stress imposed. The overexpression of AraEXLB8 in soybean (Glycine max) composite plants remarkably decreased the number of galls in transformed hairy roots inoculated with RKN. This study improves the current understanding of the molecular evolution, divergence, and gene expression of expansins in Arachis, and provides molecular and functional insights into the role of expansin-like B, the less-studied plant expansin subfamily.
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http://dx.doi.org/10.1007/s11103-017-0594-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5437183PMC
May 2017

Lateral gene transfer in eukaryotes: tip of the iceberg or of the ice cube?

BMC Biol 2016 11 18;14(1):101. Epub 2016 Nov 18.

Institut Sophia Agrobiotech, INRA, University of Nice Sophia Antipolis, CNRS, 06903, Sophia Antipolis, France.

Lateral gene transfer (LGT) is the transmission of genes, sometimes across species barriers, outwith the classic vertical inheritance from parent to offspring. LGT is recognized as an important phenomenon that has shaped the genomes and biology of prokaryotes. Whether LGT in eukaryotes is important and widespread remains controversial. A study in BMC Biology concludes that LGT in eukaryotes is neither continuous nor prevalent and suggests a rule of thumb for judging when apparent LGT may reflect contamination.See research article: http://bmcbiol.biomedcentral.com/articles/10.1186/s12915-016-0315-9 .
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http://dx.doi.org/10.1186/s12915-016-0330-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5116166PMC
November 2016

Nod Factor Effects on Root Hair-Specific Transcriptome of Medicago truncatula: Focus on Plasma Membrane Transport Systems and Reactive Oxygen Species Networks.

Front Plant Sci 2016 7;7:794. Epub 2016 Jun 7.

Biochimie and Physiologie Moléculaire des Plantes, UMR 5004 Centre National de la Recherche Scientifique/386 Institut National de la Recherche Agronomique/SupAgro Montpellier/Université de Montpellier, Campus SupAgro-Institut National de la Recherche Agronomique Montpellier, France.

Root hairs are involved in water and nutrient uptake, and thereby in plant autotrophy. In legumes, they also play a crucial role in establishment of rhizobial symbiosis. To obtain a holistic view of Medicago truncatula genes expressed in root hairs and of their regulation during the first hours of the engagement in rhizobial symbiotic interaction, a high throughput RNA sequencing on isolated root hairs from roots challenged or not with lipochitooligosaccharides Nod factors (NF) for 4 or 20 h was carried out. This provided a repertoire of genes displaying expression in root hairs, responding or not to NF, and specific or not to legumes. In analyzing the transcriptome dataset, special attention was paid to pumps, transporters, or channels active at the plasma membrane, to other proteins likely to play a role in nutrient ion uptake, NF electrical and calcium signaling, control of the redox status or the dynamic reprogramming of root hair transcriptome induced by NF treatment, and to the identification of papilionoid legume-specific genes expressed in root hairs. About 10% of the root hair expressed genes were significantly up- or down-regulated by NF treatment, suggesting their involvement in remodeling plant functions to allow establishment of the symbiotic relationship. For instance, NF-induced changes in expression of genes encoding plasma membrane transport systems or disease response proteins indicate that root hairs reduce their involvement in nutrient ion absorption and adapt their immune system in order to engage in the symbiotic interaction. It also appears that the redox status of root hair cells is tuned in response to NF perception. In addition, 1176 genes that could be considered as "papilionoid legume-specific" were identified in the M. truncatula root hair transcriptome, from which 141 were found to possess an ortholog in every of the six legume genomes that we considered, suggesting their involvement in essential functions specific to legumes. This transcriptome provides a valuable resource to investigate root hair biology in legumes and the roles that these cells play in rhizobial symbiosis establishment. These results could also contribute to the long-term objective of transferring this symbiotic capacity to non-legume plants.
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http://dx.doi.org/10.3389/fpls.2016.00794DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4894911PMC
July 2016

The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence.

Genome Biol 2016 Jun 10;17(1):124. Epub 2016 Jun 10.

USDA-ARS Horticultural Crops Research Laboratory, Corvallis, OR, USA.

Background: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes.

Results: We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative 'effector islands' in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking.

Conclusions: These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action.
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http://dx.doi.org/10.1186/s13059-016-0985-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4901422PMC
June 2016

Horizontal Gene Transfer of Pectinases from Bacteria Preceded the Diversification of Stick and Leaf Insects.

Sci Rep 2016 05 23;6:26388. Epub 2016 May 23.

Department of Entomology, Max-Planck Institute für chemische Ökologie, Hans-Knöll-Str. 8, 07745 Jena Germany.

Genes acquired by horizontal transfer are increasingly being found in animal genomes. Understanding their origin and evolution requires knowledge about the phylogenetic relationships from both source and recipient organisms. We used RNASeq data and respective assembled transcript libraries to trace the evolutionary history of polygalacturonase (pectinase) genes in stick insects (Phasmatodea). By mapping the distribution of pectinase genes on a Polyneoptera phylogeny, we identified the transfer of pectinase genes from known phasmatodean gut microbes into the genome of an early euphasmatodean ancestor that took place between 60 and 100 million years ago. This transfer preceded the rapid diversification of the suborder, enabling symbiont-free pectinase production that would increase the insects' digestive efficiency and reduce dependence on microbes. Bacteria-to-insect gene transfer was thought to be uncommon, however the increasing availability of large-scale genomic data may change this prevailing notion.
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http://dx.doi.org/10.1038/srep26388DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4876471PMC
May 2016
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