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Oryza sativa (rice) plays an essential food security role for more than half of the world's population. Obtaining crops with high levels of disease resistance is a major challenge for breeders, especially today, given the urgent need for agriculture to be more sustainable. Plant resistance genes are mainly encoded by three large leucine-rich repeat (LRR)-containing receptor (LRR-CR) families: the LRR-receptor-like kinase (LRR-RLK), LRR-receptor-like protein (LRR-RLP) and nucleotide-binding LRR receptor (NLR). Using lrrprofiler, a pipeline that we developed to annotate and classify these proteins, we compared three publicly available annotations of the rice Nipponbare reference genome. The extended discrepancies that we observed for LRR-CR gene models led us to perform an in-depth manual curation of their annotations while paying special attention to nonsense mutations. We then transferred this manually curated annotation to Kitaake, a cultivar that is closely related to Nipponbare, using an optimized strategy. Here, we discuss the breakthrough achieved by manual curation when comparing genomes and, in addition to 'functional' and 'structural' annotations, we propose that the community adopts this approach, which we call 'comprehensive' annotation. The resulting data are crucial for further studies on the natural variability and evolution of LRR-CR genes in order to promote their use in breeding future resilient varieties.

Oryza sativa (rice) plays an essential food security role for more than half of the world's population. Obtaining crops with high levels of disease resistance is a major challenge for breeders, especially today, given the urgent need for agriculture to be more sustainable. Plant resistance genes are mainly encoded by three large leucine-rich repeat (LRR)-containing receptor (LRR-CR) families: the LRR-receptor-like kinase (LRR-RLK), LRR-receptor-like protein (LRR-RLP) and nucleotide-binding LRR receptor (NLR). Using lrrprofiler, a pipeline that we developed to annotate and classify these proteins, we compared three publicly available annotations of the rice Nipponbare reference genome. The extended discrepancies that we observed for LRR-CR gene models led us to perform an in-depth manual curation of their annotations while paying special attention to nonsense mutations. We then transferred this manually curated annotation to Kitaake, a cultivar that is closely related to Nipponbare, using an optimized strategy. Here, we discuss the breakthrough achieved by manual curation when comparing genomes and, in addition to 'functional' and 'structural' annotations, we propose that the community adopts this approach, which we call 'comprehensive' annotation. The resulting data are crucial for further studies on the natural variability and evolution of LRR-CR genes in order to promote their use in breeding future resilient varieties.

Because of their high level of diversity and complex evolutionary histories, most studies on plant receptor-like kinase subfamilies have focused on their kinase domains. With the large amount of genome sequence data available today, particularly on basal land plants and Charophyta, more attention should be paid to primary events that shaped the diversity of the RLK gene family. We thus focus on the motifs and domains found in association with kinase domains to illustrate their origin, organization, and evolutionary dynamics. We discuss when these different domain associations first occurred and how they evolved, based on a literature review complemented by some of our unpublished results.

Because of their high level of diversity and complex evolutionary histories, most studies on plant receptor-like kinase subfamilies have focused on their kinase domains. With the large amount of genome sequence data available today, particularly on basal land plants and Charophyta, more attention should be paid to primary events that shaped the diversity of the RLK gene family. We thus focus on the motifs and domains found in association with kinase domains to illustrate their origin, organization, and evolutionary dynamics. We discuss when these different domain associations first occurred and how they evolved, based on a literature review complemented by some of our unpublished results.

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes' but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times(2). With 450 species spread throughout Asia, Europe and America(3), oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical(4) and modelling(5) approaches have shown that intra-organismal genetic heterogeneity can be selected for(6) and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes(7). However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes' but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times(2). With 450 species spread throughout Asia, Europe and America(3), oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical(4) and modelling(5) approaches have shown that intra-organismal genetic heterogeneity can be selected for(6) and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes(7). However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes' but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times(2). With 450 species spread throughout Asia, Europe and America(3), oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical(4) and modelling(5) approaches have shown that intra-organismal genetic heterogeneity can be selected for(6) and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes(7). However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.

Sorghum bicolor is the fifth cereal worldwide for grain production, constituting the staple food for a round 500 million people. The release of its genome sequence, its phylogenetic proximity with other important C4 species (maize, switchgrass, sugarcane) and its low genome complexity contribute to its interest on a more fundamental level. Sorghum bicolor wild relatives (ssp. verticilliflorum) and domesticated (ssp. bicolor) pools are inter-fertile and intense gene flow occurs. However, a clear domestication syndrome is visible (plant architecture, shattering, dormancy and seed weight). ln spite of its agronomical Importance, the evolutionary dynamics of sorghum domestication and the genetic bases of adaptations to natural and anthropogenic pressures are not well understood. Here we leverage transcriptomic and genomic resources to improve our knowledge on the evolutionary history of S. bicolor, with a particular focus on the consequences of the domestication process. As a first step, gene expression and nucleotide variability of the expressed genes were analyzed in 11 cultivated and 9 wild accessions selected to maximize the genetic coverage of these two pools. The cultivated compartment harbors 30% lower genetic diversity than the wild pool, which supports the occurrence of a genetic bottleneck in the domestication history of sorghum. More than 900 genes are significantly differentially expressed between the two compartments. Among them, genes involved in photosynthesis and in reduction-oxidation processing of seed storage proteins are over-represented. Further analyses revealed that domestication reduced significantly the variability of the isoform expression balance (expression ratio of the alternative proteins coded by a single gene) in cultivated sorghum. Scans for local adaptation and positive selection on large cultivated and wild panels genotyped with genotyping by sequencing approaches are ongoing. Overall, these analyses pave the way towards the identifica

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes' but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times(2). With 450 species spread throughout Asia, Europe and America(3), oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical(4) and modelling(5) approaches have shown that intra-organismal genetic heterogeneity can be selected for(6) and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes(7). However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.

Sorghum bicolor is the fifth cereal worldwide for grain production, constituting the staple food for a round 500 million people. The release of its genome sequence, its phylogenetic proximity with other important C4 species (maize, switchgrass, sugarcane) and its low genome complexity contribute to its interest on a more fundamental level. Sorghum bicolor wild relatives (ssp. verticilliflorum) and domesticated (ssp. bicolor) pools are inter-fertile and intense gene flow occurs. However, a clear domestication syndrome is visible (plant architecture, shattering, dormancy and seed weight). ln spite of its agronomical Importance, the evolutionary dynamics of sorghum domestication and the genetic bases of adaptations to natural and anthropogenic pressures are not well understood. Here we leverage transcriptomic and genomic resources to improve our knowledge on the evolutionary history of S. bicolor, with a particular focus on the consequences of the domestication process. As a first step, gene expression and nucleotide variability of the expressed genes were analyzed in 11 cultivated and 9 wild accessions selected to maximize the genetic coverage of these two pools. The cultivated compartment harbors 30% lower genetic diversity than the wild pool, which supports the occurrence of a genetic bottleneck in the domestication history of sorghum. More than 900 genes are significantly differentially expressed between the two compartments. Among them, genes involved in photosynthesis and in reduction-oxidation processing of seed storage proteins are over-represented. Further analyses revealed that domestication reduced significantly the variability of the isoform expression balance (expression ratio of the alternative proteins coded by a single gene) in cultivated sorghum. Scans for local adaptation and positive selection on large cultivated and wild panels genotyped with genotyping by sequencing approaches are ongoing. Overall, these analyses pave the way towards the identifica

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes' but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times(2). With 450 species spread throughout Asia, Europe and America(3), oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical(4) and modelling(5) approaches have shown that intra-organismal genetic heterogeneity can be selected for(6) and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes(7). However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.

We produced a unique large data set of reference transcriptomes to obtain new knowledge about the evolution of plant genomes and crop domestication. For this purpose, we validated a RNA-Seq data assembly protocol to perform comparative population genomics. For the validation, we assessed and compared the quality of de novo Illumina short-read assemblies using data from two crops for which an annotated reference genome was available, namely grapevine and sorghum. We used the same protocol for the release of 26 new transcriptomes of crop plants and wild relatives, including still understudied crops such as yam, pearl millet and fonio. The species list has a wide taxonomic representation with the inclusion of 15 monocots and 11 eudicots. All contigs were annotated using BLAST, prot4EST and Blast2GO. A strong originality of the data set is that each crop is associated with close relative species, which will permit whole-genome comparative evolutionary studies between crops and their wild-related species. This large resource will thus serve research communities working on both crops and model organisms. All the data are available at http://arcad-bioinformatics.southgreen.fr. (Résumé d'auteur)

Domestication is known to strongly reduce genomic diversity through population bottlenecks. The resulting loss of polymorphism has been thoroughly documented in numerous cultivated species. Here we investigate the impact of domestication on the diversity of alternative transcript expressions using RNAseq data obtained on cultivated and wild sorghum accessions (ten accessions for each pool). In that aim, we focus on genes expressing two isoforms in sorghum and estimate the ratio between expression levels of those isoforms in each accession. Noticeably, for a given gene, one isoform can either be overexpressed or underexpressed in some wild accessions, whereas in the cultivated accessions, the balance between the two isoforms of the same gene appears to be much more homogenous. Indeed, we observe in sorghum significantly more variation in isoform expression balance among wild accessions than among domesticated accessions. The possibility exists that the loss of nucleotide diversity due to domestication could affect regulatory elements, controlling transcription or degradation of these isoforms. Impact on the isoform expression balance is discussed. As far as we know, this is the first time that the impact of domestication on transcript isoform balance has been studied at the genomic scale. This could pave the way towards the identification of key domestication genes with finely tuned isoform expressions in domesticated accessions while being highly variable in their wild relatives.

Leucine-Rich Repeats Receptor-Like Kinase (LRR-RLK) genes represent a large and complex gene family in plants, mainly involved in development and stress responses. These receptors are composed of an LRR-containing extracellular domain (ECD), a transmembrane domain (TM) and an intracellular kinase domain (KD). To provide new perspectives on functional analyses of these genes in model and non-model plant species, we performed a phylogenetic analysis on 8,360 LRR-RLK receptors in 31 angiosperm genomes (8 monocots and 23 dicots). We identified 101 orthologous groups (OGs) of genes being conserved among almost all monocot and dicot species analyzed. We observed that more than 10% of these OGs are absent in the Brassicaceae species studied. We show that the ECD structural features are not always conserved among orthologs, suggesting that functions may have diverged in some OG sets. Moreover, we looked at targets of positive selection footprints in 12 pairs of OGs and noticed that depending on the subgroups, positive selection occurred more frequently either in the ECDs or in the KDs.

Domestication is known to strongly reduce genomic diversity through population bottlenecks. The resulting loss of polymorphism has been thoroughly documented in numerous cultivated species. Here we investigate the impact of domestication on the diversity of alternative transcript expressions using RNAseq data obtained on cultivated and wild sorghum accessions (ten accessions for each pool). In that aim, we focus on genes expressing two isoforms in sorghum and estimate the ratio between expression levels of those isoforms in each accession. Noticeably, for a given gene, one isoform can either be overexpressed or underexpressed in some wild accessions, whereas in the cultivated accessions, the balance between the two isoforms of the same gene appears to be much more homogenous. Indeed, we observe in sorghum significantly more variation in isoform expression balance among wild accessions than among domesticated accessions. The possibility exists that the loss of nucleotide diversity due to domestication could affect regulatory elements, controlling transcription or degradation of these isoforms. Impact on the isoform expression balance is discussed. As far as we know, this is the first time that the impact of domestication on transcript isoform balance has been studied at the genomic scale. This could pave the way towards the identification of key domestication genes with finely tuned isoform expressions in domesticated accessions while being highly variable in their wild relatives.

Leucine-Rich Repeats Receptor-Like Kinase (LRR-RLK) genes represent a large and complex gene family in plants, mainly involved in development and stress responses. These receptors are composed of an LRR-containing extracellular domain (ECD), a transmembrane domain (TM) and an intracellular kinase domain (KD). To provide new perspectives on functional analyses of these genes in model and non-model plant species, we performed a phylogenetic analysis on 8,360 LRR-RLK receptors in 31 angiosperm genomes (8 monocots and 23 dicots). We identified 101 orthologous groups (OGs) of genes being conserved among almost all monocot and dicot species analyzed. We observed that more than 10% of these OGs are absent in the Brassicaceae species studied. We show that the ECD structural features are not always conserved among orthologs, suggesting that functions may have diverged in some OG sets. Moreover, we looked at targets of positive selection footprints in 12 pairs of OGs and noticed that depending on the subgroups, positive selection occurred more frequently either in the ECDs or in the KDs.

Gene duplications are an important factor in plant evolution and lineage specific expanded (LSE) genes are of particular interest. Receptor-like kinases (RLK) expanded massively in land plants and Leucine-Rich Repeat (LRR)-RLKs constitute the largest RLK family. Based on the phylogeny of 7,554 LRR-RLK genes from 31 fully sequenced flowering plant genomes, the complex evolutionary dynamics of this family was characterized in depth. We studied the involvement of selection during the expansion of this family among angiosperms. LRR-RLK subgroups harbor extremely contrasted rates of duplication, retention or loss and LSE copies are predominantly found in subgroups involved in environmental interactions. Expansion rates also differ significantly depending on the time when rounds of expansion or loss occurred on the angiosperm phylogenetic tree. Finally, using a dN/dS-based test in a phylogenetic framework, we searched for selection footprints on LSE and single-copy LRR-RLK genes. Selective constraint appeared to be globally relaxed at LSE genes and codons under positive selection were detected in 50% of them. Moreover, the LRR domains - and specifically four amino acids in them - were found to be the main targets of positive selection. Here, we provide an extensive overview of the expansion and evolution of this very large gene family.

Gene duplications are an important factor in plant evolution and lineage specific expanded (LSE) genes are of particular interest. Receptor-like kinases (RLK) expanded massively in land plants and Leucine-Rich Repeat (LRR)-RLKs constitute the largest RLK family. Based on the phylogeny of 7,554 LRR-RLK genes from 31 fully sequenced flowering plant genomes, the complex evolutionary dynamics of this family was characterized in depth. We studied the involvement of selection during the expansion of this family among angiosperms. LRR-RLK subgroups harbor extremely contrasted rates of duplication, retention or loss and LSE copies are predominantly found in subgroups involved in environmental interactions. Expansion rates also differ significantly depending on the time when rounds of expansion or loss occurred on the angiosperm phylogenetic tree. Finally, using a dN/dS-based test in a phylogenetic framework, we searched for selection footprints on LSE and single-copy LRR-RLK genes. Selective constraint appeared to be globally relaxed at LSE genes and codons under positive selection were detected in 50% of them. Moreover, the LRR domains - and specifically four amino acids in them - were found to be the main targets of positive selection. Here, we provide an extensive overview of the expansion and evolution of this very large gene family.

Background Recurrent gene duplication and retention played an important role in angiosperm genome evolution. It has been hypothesized that these processes contribute significantly to plant adaptation but so far this hypothesis has not been tested at the genome scale. Results We studied available sequenced angiosperm genomes to assess the frequency of positive selection footprints in lineage specific expanded (LSE) gene families compared to single-copy genes using a dN/dS-based test in a phylogenetic framework. We found 5.38% of alignments in LSE genes with codons under positive selection. In contrast, we found no evidence for codons under positive selection in the single-copy reference set. An analysis at the branch level shows that purifying selection acted more strongly on single-copy genes than on LSE gene clusters. Moreover we detect significantly more branches indicating evolution under positive selection and/or relaxed constraint in LSE genes than in single-copy genes. Conclusions In this - to our knowledge -first genome-scale study we provide strong empirical support for the hypothesis that LSE genes fuel adaptation in angiosperms. Our conservative approach for detecting selection footprints as well as our results can be of interest for further studies on (plant) gene family evolution.

Background Recurrent gene duplication and retention played an important role in angiosperm genome evolution. It has been hypothesized that these processes contribute significantly to plant adaptation but so far this hypothesis has not been tested at the genome scale. Results We studied available sequenced angiosperm genomes to assess the frequency of positive selection footprints in lineage specific expanded (LSE) gene families compared to single-copy genes using a dN/dS-based test in a phylogenetic framework. We found 5.38% of alignments in LSE genes with codons under positive selection. In contrast, we found no evidence for codons under positive selection in the single-copy reference set. An analysis at the branch level shows that purifying selection acted more strongly on single-copy genes than on LSE gene clusters. Moreover we detect significantly more branches indicating evolution under positive selection and/or relaxed constraint in LSE genes than in single-copy genes. Conclusions In this - to our knowledge -first genome-scale study we provide strong empirical support for the hypothesis that LSE genes fuel adaptation in angiosperms. Our conservative approach for detecting selection footprints as well as our results can be of interest for further studies on (plant) gene family evolution.

L'analyse de la liaison statistique entre allèles à 2 locus, ou déséquilibre de liaison (DL), a été abordée simultanément chez le riz, le sorgho, le blé, l'hévéa et Medicago truncatula en utilisant des échantillons tirés de collections de ressources génétiques. Des stratégies utilisant des BACs ont permis de développer des marqueurs dans des zones localisées. L'utilisation des séquences terminales des BACs ciblés a été efficace pour définir des marqueurs microsatellites. Par ailleurs, des amorces ont été développées pour séquencer directement des fragments géniques. Le haut niveau de polymorphisme des marqueurs microsatellites a pu nécessiter des adaptations pour le calcul du DL. La structure génétique observée sur les plantes cultivées génère un fort bruit de fond de DL, tandis que dans les collections d'espèces sauvages autogames, le DL reste faible même à courte distance, décroissant rapidement au delà de 20 kb. A l'intérieur des groupes définis pour les espèces cultivées, le DL est plus faible et décroît assez rapidement, parfois de manière différente selon les groupes, de 100 kb environ pour le riz à 500 kb pour le sorgho. Une bonne connaissance de la diversité de l'espèce apparaît donc nécessaire avant de réaliser des études d'associations qui paraissent dès lors réalisables en utilisant les accessions contenues dans les collections de ressources génétiques.

L'analyse de la liaison statistique entre allèles à 2 locus, ou déséquilibre de liaison (DL), a été abordée simultanément chez le riz, le sorgho, le blé, l'hévéa et Medicago truncatula en utilisant des échantillons tirés de collections de ressources génétiques. Des stratégies utilisant des BACs ont permis de développer des marqueurs dans des zones localisées. L'utilisation des séquences terminales des BACs ciblés a été efficace pour définir des marqueurs microsatellites. Par ailleurs, des amorces ont été développées pour séquencer directement des fragments géniques. Le haut niveau de polymorphisme des marqueurs microsatellites a pu nécessiter des adaptations pour le calcul du DL. La structure génétique observée sur les plantes cultivées génère un fort bruit de fond de DL, tandis que dans les collections d'espèces sauvages autogames, le DL reste faible même à courte distance, décroissant rapidement au delà de 20 kb. A l'intérieur des groupes définis pour les espèces cultivées, le DL est plus faible et décroît assez rapidement, parfois de manière différente selon les groupes, de 100 kb environ pour le riz à 500 kb pour le sorgho. Une bonne connaissance de la diversité de l'espèce apparaît donc nécessaire avant de réaliser des études d'associations qui paraissent dès lors réalisables en utilisant les accessions contenues dans les collections de ressources génétiques.