A survey of lineage-specific genes in Triticeae reveals de novo gene evolution from genomic raw material

Diploid plant genomes typically contain ~35,000 genes, almost all belonging to highly conserved gene families. Only a small fraction are lineage-specific, which are found in only one or few closely related species. Little is known about how genes arise de novo in plant genomes and how often this occurs; however, they are believed to be important for plants diversification and adaptation. We developed a pipeline to identify lineage-specific genes in Triticeae, using newly available genome assemblies of wheat, barley, and rye. Applying a set of stringent criteria, we identified 5942 candidate Triticeae-specific genes (TSGs), of which 2337 were validated as protein-coding genes in wheat. Differential gene expression analyses revealed that stress-induced wheat TSGs are strongly enriched in putative secreted proteins. Some were previously described to be involved in Triticeae non-host resistance and cold response. Additionally, we show that 1079 TSGs have sequence homology to transposable elements (TEs), ~68% of them deriving from regulatory non-coding regions of Gypsy retrotransposons. Most importantly, we demonstrate that these TSGs are enriched in transmembrane domains and are among the most highly expressed wheat genes overall. To summarize, we conclude that de novo gene formation is relatively rare and that Triticeae probably possess ~779 lineage-specific genes per haploid genome. TSGs, which respond to pathogen and environmental stresses, may be interesting candidates for future targeted resistance breeding in Triticeae. Finally, we propose that non-coding regions of TEs might provide important genetic raw material for the functional innovation of TM domains and the evolution of novel secreted proteins

Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat

Introgressions of chromosomal segments from related species into wheat are important sources of resistance against fungal diseases. The durability and effectiveness of introgressed resistance genes upon agricultural deployment is highly variable-a phenomenon that remains poorly understood, as the corresponding fungal avirulence genes are largely unknown. Until its breakdown, the Pm17 resistance gene introgressed from rye to wheat provided broad resistance against powdery mildew (Blumeria graminis). Here, we used quantitative trait locus (QTL) mapping to identify the corresponding wheat mildew avirulence effector AvrPm17. It is encoded by two paralogous genes that exhibit signatures of reoccurring gene conversion events and are members of a mildew sublineage specific effector cluster. Extensive haplovariant mining in wheat mildew and related sublineages identified several ancient virulent AvrPm17 variants that were present as standing genetic variation in wheat powdery mildew prior to the Pm17 introgression, thereby paving the way for the rapid breakdown of the Pm17 resistance. QTL mapping in mildew identified a second genetic component likely corresponding to an additional resistance gene present on the 1AL.1RS translocation carrying Pm17. This gene remained previously undetected due to suppressed recombination within the introgressed rye chromosomal segment. We conclude that the initial effectiveness of 1AL.1RS was based on simultaneous introgression of two genetically linked resistance genes. Our results demonstrate the relevance of pathogen-based genetic approaches to disentangling complex resistance loci in wheat. We propose that identification and monitoring of avirulence gene diversity in pathogen populations become an integral part of introgression breeding to ensure effective and durable resistance in wheat

A chromosome-scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

Blumeria graminis f. sp. tritici (B.g. tritici) is the causal agent of the wheat powdery mildew disease. The highly fragmented B.g. tritici genome available so far has prevented a systematic analysis of effector genes that are known to be involved in host adaptation. To study the diversity and evolution of effector genes we produced a chromosome‐scale assembly of the B.g. tritici genome. The genome assembly and annotation was achieved by combining long‐read sequencing with high‐density genetic mapping, bacterial artificial chromosome fingerprinting and transcriptomics. We found that the 166.6 Mb B.g. tritici genome encodes 844 candidate effector genes, over 40% more than previously reported. Candidate effector genes have characteristic local genomic organization such as gene clustering and enrichment for recombination‐active regions and certain transposable element families. A large group of 412 candidate effector genes shows high plasticity in terms of copy number variation in a global set of 36 isolates and of transcription levels. Our data suggest that copy number variation and transcriptional flexibility are the main drivers for adaptation in B.g. tritici. The high repeat content may play a role in providing a genomic environment that allows rapid evolution of effector genes with selection as the driving force

Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins

Crop breeding for resistance to pathogens largely relies on genes encoding receptors that confer race-specific immunity. Here, we report the identification of the wheat Pm4 race-specific resistance gene to powdery mildew. Pm4 encodes a putative chimeric protein of a serine/threonine kinase and multiple C2 domains and transmembrane regions, a unique domain architecture among known resistance proteins. Pm4 undergoes constitutive alternative splicing, generating two isoforms with different protein domain topologies that are both essential for resistance function. Both isoforms interact and localize to the endoplasmatic reticulum when co-expressed. Pm4 reveals additional diversity of immune receptor architecture to be explored for breeding and suggests an endoplasmatic reticulum-based molecular mechanism of Pm4-mediated race-specific resistance

Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species

Throughout the history of agriculture, many new crop species (polyploids or artificial hybrids) have been introduced to diversify products or to increase yield. However, little is known about how these new crops influence the evolution of new pathogens and diseases. Triticale is an artificial hybrid of wheat and rye, and it was resistant to the fungal pathogen powdery mildew (Blumeria graminis) until 2001 (refs. 1,2,3). We sequenced and compared the genomes of 46 powdery mildew isolates covering several formae speciales. We found that B. graminis f. sp. triticale, which grows on triticale and wheat, is a hybrid between wheat powdery mildew (B. graminis f. sp. tritici) and mildew specialized on rye (B. graminis f. sp. secalis). Our data show that the hybrid of the two mildews specialized on two different hosts can infect the hybrid plant species originating from those two hosts. We conclude that hybridization between mildews specialized on different species is a mechanism of adaptation to new crops introduced by agriculture

Chromosome-scale genome assembly provides insights into rye biology, evolution and agronomic potential

Rye (Secale cereale L.) is an exceptionally climate-resilient cereal crop, used extensively to produce improved wheat varieties via introgressive hybridization and possessing the entire repertoire of genes necessary to enable hybrid breeding. Rye is allogamous and only recently domesticated, thus giving cultivated ryes access to a diverse and exploitable wild gene pool. To further enhance the agronomic potential of rye, we produced a chromosome-scale annotated assembly of the 7.9-gigabase rye genome and extensively validated its quality by using a suite of molecular genetic resources. We demonstrate applications of this resource with a broad range of investigations. We present findings on cultivated rye's incomplete genetic isolation from wild relatives, mechanisms of genome structural evolution, pathogen resistance, low-temperature tolerance, fertility control systems for hybrid breeding and the yield benefits of rye-wheat introgressions.Peer reviewe

Cereal powdery mildew effectors: a complex toolbox for an obligate pathogen

Highlights • Cereal powdery mildews have evolved a large repertoire of candidate effector proteins. • These effectors are encoded within size variable and highly diversified gene families. • Mildew effectors can act as virulence factors, Avr genes and Avr suppressors. • Their mode of action provides a molecular basis for the Zig-Zag evolutionary model

A survey of lineage-specific genes in Triticeae reveals de novo gene evolution from genomic raw material

16 Pág.Diploid plant genomes typically contain ~35,000 genes, almost all belonging to highly conserved gene families. Only a small fraction are lineage-specific, which are found in only one or few closely related species. Little is known about how genes arise de novo in plant genomes and how often this occurs; however, they are believed to be important for plants diversification and adaptation. We developed a pipeline to identify lineage-specific genes in Triticeae, using newly available genome assemblies of wheat, barley, and rye. Applying a set of stringent criteria, we identified 5942 candidate Triticeae-specific genes (TSGs), of which 2337 were validated as protein-coding genes in wheat. Differential gene expression analyses revealed that stress-induced wheat TSGs are strongly enriched in putative secreted proteins. Some were previously described to be involved in Triticeae non-host resistance and cold response. Additionally, we show that 1079 TSGs have sequence homology to transposable elements (TEs), ~68% of them deriving from regulatory non-coding regions of Gypsy retrotransposons. Most importantly, we demonstrate that these TSGs are enriched in transmembrane domains and are among the most highly expressed wheat genes overall. To summarize, we conclude that de novo gene formation is relatively rare and that Triticeae probably possess ~779 lineage-specific genes per haploid genome. TSGs, which respond to pathogen and environmental stresses, may be interesting candidates for future targeted resistance breeding in Triticeae. Finally, we propose that non-coding regions of TEs might provide important genetic raw material for the functional innovation of TM domains and the evolution of novel secreted proteins.This work was supported by the Swiss National Foundation grant 31003A_163325.University of Zurich Research Priority Program, Grant/Award Number: U-702-21-01; Swiss National Foundation, Grant/Award Number: 31003A_163325Peer reviewe

Le Courrier

28 janvier 18331833/01/28 (N28)