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Bacterial blight, caused by Xanthomonas oryzae pv. oryzae (Xoo), is one of the major diseases that impact rice production in Asia. The bacteria use transcription activator-like effectors (TALEs) to hijack the host transcription machinery and activate key susceptibility (S) genes, specifically members of the SWEET sucrose uniporters through the recognition of effector-binding element (EBEs) in the promoter regions. However, natural variations in the EBEs that alter the binding affinity of TALEs usually prevent sufficient induction of SWEET genes, leading to resistance phenotypes. In this study, we identified candidate resistance alleles by mining a rice diversity panel for mutations in the promoter of OsSWEET13 and OsSWEET14, which are direct targets of three major TALEs PthXo2, PthXo3 and AvrXa7. We found natural variations at the EBE of both genes, which appeared to have emerged independently in at least three rice subspecies. For OsSWEET13, a 2-bp deletion at the 5th and 6th positions of the EBE, and a substitution at the 17th position appear to be sufficient to prevent activation by PthXo2. Similarly, a single nucleotide substitution at position 10 compromised the induction of OsSWEET14 by AvrXa7. These findings might increase our opportunities to reduce pathogen virulence by preventing the induction of SWEET transporters. Pyramiding variants along with other resistance genes may provide durable and broad-spectrum resistance to the disease.

Rice blast, caused by (teleomorph: Magnaporthe oryzae), is one of the most economically damaging diseases affecting rice worldwide. While the evolutionary origins and genetic structures of Asian and European P. oryzae populations are relatively well characterized, African isolates remain underexplored. This knowledge gap impedes the development of informed management strategies for rice blast in the region. The present study was conducted to characterize the genetic origins, population structure, admixture, demographic history, and effector gene diversity of P. oryzae isolates in SSA, and to elucidate their evolutionary trajectories and implications for disease management. A total of 180 genome sequences (45 from SSA, 135 from other regions) were analyzed using population genomic approaches. Phylogeographic reconstructions, demographic modeling, and genome-wide association studies were performed to trace migration events, quantify genetic diversity, and identify candidate adaptation genes. Effector gene repertoires were also examined for diversity and selection signatures. Our findings provide new dates for the divergence of SSA populations from Asian populations. The introduction of P. oryzae into Africa occurred mainly from China in the late 19th century, initially in West Africa (WA; Mali and Burkina Faso), and subsequently in Uganda and Madagascar during the early 20th century, before extending to the wider African region, with subsequent repeated introductions. Tajima's D and demographic modeling suggested complex population dynamics shaped by migration and asymmetric founder events, highlighting considerably shared genetic ancestry between Asia and East Africa (EA), in contrast with that between Asia and WA. Genome-wide association analysis identified a specific set of single nucleotide polymorphism markers, along with several candidate genes linked to adaptation. Effector analysis revealed that SSA isolates harbor fewer effectors and exhibit lower genetic diversity than Asian populations, with some effectors under positive selection, particularly in WA. P. oryzae populations in SSA are shaped by historical introductions, founder events, and region-specific adaptation processes. While WA populations have diverged significantly from their Asian ancestors, gene flow within SSA connects regional populations, and effector gene diversity reflects both conserved virulence strategies and adaptation to local hosts. Overall, this study improves the existing knowledge on P. oryzae populations in SSA and underscore the need for integrated management strategies that consider both historical and contemporary pathogen dynamics in Africa.

Sheath rot complex and seed discoloration in rice involve a number of pathogenic bacteria that cannot be associated with distinctive symptoms. These pathogens can easily travel on asymptomatic seeds and therefore represent a threat to rice cropping systems. Among the rice-infecting Pseudomonas, P. fuscovaginae has been associated with sheath brown rot disease in several rice growing areas around the world. The appearance of a similar Pseudomonas population, which here we named P. fuscovaginae-like, represents a perfect opportunity to understand common genomic features that can explain the infection mechanism in rice. We showed that the novel population is indeed closely related to P. fuscovaginae. A comparative genomics approach on eight rice-infecting Pseudomonas revealed heterogeneous genomes and a high number of strain-specific genes. The genomes of P. fuscovaginae-like harbor four secretion systems (Type I, II, III, and VI) and other important pathogenicity machinery that could probably facilitate rice colonization. We identified 123 core secreted proteins, most of which have strong signatures of positive selection suggesting functional adaptation. Transcript accumulation of putative pathogenicity-related genes during rice colonization revealed a concerted virulence mechanism. The study suggests that rice-infecting Pseudomonas causing sheath brown rot are intrinsically diverse and maintain a variable set of metabolic capabilities as a potential strategy to occupy a range of environments.

The impact of modern agriculture on the evolutionary trajectory of plant pathogens is a central question for crop sustainability. The Green Revolution replaced traditional rice landraces with high-yielding varieties, creating a uniform selection pressure that allows measuring the effect of such intervention. In this study, we analyzed a unique historical pathogen record to assess the impact of a major resistance gene, Xa4 , in the population structure of Xanthomonas oryzae pv. oryzae ( Xoo ) collected in the Philippines in a span of 40 years. After the deployment of Xa4 in the early 1960s, the emergence of virulent pathogen groups was associated with the increasing adoption of rice varieties carrying Xa4 , which reached 80% of the total planted area. Whole genomes analysis of a representative sample suggested six major pathogen groups with distinctive signatures of selection in genes related to secretion system, cell-wall degradation, lipopolysaccharide production, and detoxification of host defense components. Association genetics also suggested that each population might evolve different mechanisms to adapt to Xa4 . Interestingly, we found evidence of strong selective sweep affecting several populations in the mid-1980s, suggesting a major bottleneck that coincides with the peak of Xa4 deployment in the archipelago. Our study highlights how modern agricultural practices facilitate the adaptation of pathogens to overcome the effects of standard crop improvement efforts.

Understanding the processes that shaped contemporary pathogen populations in agricultural landscapes is quite important to define appropriate management strategies and to support crop improvement efforts. Here, we took advantage of an historical record to examine the adaptation pathway of the rice pathogen Xanthomonas oryzae pv. oryzae ( Xoo ) in a semi-isolated environment represented in the Philippine archipelago. By comparing genomes of key Xoo groups we showed that modern populations derived from three Asian lineages. We also showed that diversification of virulence factors occurred within each lineage, most likely driven by host adaptation, and it was essential to shape contemporary pathogen races. This finding is particularly important because it expands our understanding of pathogen adaptation to modern agriculture.

Abstract Rice blast caused by Magnaporthe oryzae is one of the most economically damaging diseases of rice worldwide. The disease originated in Asia but was detected for the first time in Sub-Saharan Africa (SSA) around 100 years ago. Despite its importance, the evolutionary processes involved in shaping the population structure of M. oryzae in SSA remain unclear. In this study, we investigate the population history of M. oryzae using a combined dataset of 180 genomes. Our results show that SSA populations are more diverse than earlier perceived, and harbor all genetic groups previously reported in Asia. While M. oryzae populations in SSA and Asia draw from the same genetic pools, both are experiencing different evolutionary trajectories resulting from unknown selection pressures or demographic processes. The distribution of rare alleles, measured as Tajima’s D values, show significant differences at the substructure level. Genome-wide analysis indicates potential events of population contraction strongly affecting M. oryzae in SSA. In addition, the distribution and haplotype diversity of effectors might suggest a process of local adaptation to SSA conditions. These findings provide additional clues about the evolutionary history of M. oryzae outside the center of origin and help to build customized disease management strategies. Competing Interest Statement The authors have declared no competing interest.

Understanding the factors that influence the outcome of crop interactions with microbes is key to managing crop diseases and improving yield. While the composition, structure and functional profile of crop microbial communities are shaped by complex interactions between the host, microbes and the environment, the relative contribution of each of these factors is mostly unknown. Here, we profiled the community composition of bacteria across leaves of 3,024 rice (Oryza sativa) accessions from field trials in China and the Philippines using metagenomics. Despite significant differences in diversity between environments, the structure and metabolic profiles of the microbiome appear to be conserved, suggesting that microbiomes converge onto core functions. Furthermore, co-occurrence analysis identified microbial hubs that regulate the network structure of the microbiome. We identified rice genomic regions controlling the abundance of these hubs, enriched for processes involved in stress responses and carbohydrate metabolism. We functionally validated the importance of these processes, finding that abundance of hub taxa was different in rice mutants with altered cellulose and salicylate accumulation, two major metabolites at the host-microbe interactions interface. By identifying key host genomic regions, host traits and hub microbes that govern microbiome composition, our study opens the door to designing future cropping systems.

Sheath rot complex and seed discoloration in rice involve a number of pathogenic bacteria that cannot be associated with distinctive symptoms. These pathogens can easily travel on asymptomatic seeds and therefore represent a threat to rice cropping systems. Among the rice-infecting Pseudomonas, P. fuscovaginae has been associated with sheath brown rot disease in several rice growing areas around the world. The appearance of a similar Pseudomonas population, which here we named P. fuscovaginae-like, represents a perfect opportunity to understand common genomic features that can explain the infection mechanism in rice. We showed that the novel population is indeed closely related to P. fuscovaginae. A comparative genomics approach on eight rice-infecting Pseudomonas revealed heterogeneous genomes and a high number of strain-specific genes. The genomes of P. fuscovaginae-like harbor four secretion systems (Type I, II, III, and VI) and other important pathogenicity machinery that could probably facilitate rice colonization. We identified 123 core secreted proteins, most of which have strong signatures of positive selection suggesting functional adaptation. Transcript accumulation of putative pathogenicity-related genes during rice colonization revealed a concerted virulence mechanism. The study suggests that rice-infecting Pseudomonas causing sheath brown rot are intrinsically diverse and maintain a variable set of metabolic capabilities as a potential strategy to occupy a range of environments.

African rice (Oryza glaberrima) was independently domesticated in West Africa around 3000 years ago, and has long been intertwined in the history of the region. The gradual replacement of African rice by Asian rice (Oryza sativa), which was introduced when European settlers arrived, has since dominated rice cultivation in Africa. Domesticated rice species are affected by bacterial leaf blight (BLB), which is caused by the pathogen Xanthomonas oryzae pv. oryzae (Xoo). Here we provide evidence that the bacterial leaf blight pathogen in Africa (AfXoo) belongs to a distinct phylogroup from the one circulating in Asia (AsXoo), and has a different evolutionary history. Analysis of 88 AfXoo genomes identified five groups, one of which is a highly diverse population that might have probably given rise to three independent clonal populations based on multiple genetic tests. Tip-dating analysis revealed that the emergence and expansion of AfXoo coincided with the rise and fall of African rice nearly a thousand years ago, and O. sativa served as a bottleneck in the evolution of AfXoo over time. Although the type III effectors (T3E), proteins that are secreted by the pathogen to evade host resistance or seize control of host nutrients, are highly conserved in AfXoo, we observed some variation in effector families. Different evolutionary modifications in the transcription activator-like effectors (TALEs), especially in repeat variable di-residues (RVDs), likely enabled adaptation to both host species. Previous analyses carried out on samples collected in Burkina Faso have shown that there could be more than one TALE repertoire combination in the field, and genome sequencing data revealed potential TALE evolutionary mechanisms that could happen. Our research provides a comprehensive genetic history of bacterial blight in West Africa, and its past and present impact on rice cultivation in the region.Competing Interest StatementThe authors have declared no competing interest.

Background: The crop microbial communities are shaped by interactions between the host, microbes and the environment, however, their relative contribution is beginning to be understood. Here, we explore these interactions in the leaf bacterial community across 3,024 rice accessions. Findings: By using unmapped DNA sequencing reads as microbial reads, we characterized the structure of the rice bacterial microbiome. We identified central bacteria taxa that emerge as microbial “hubs” and may have an influence on the network of host-microbe interactions. We found regions in the rice genome that might control the assembly of these microbial hubs. To our knowledge this is one of the first studies that uses raw data from plant genome sequencing projects to characterize the leaf bacterial communities. Conclusion: We showed, that the structure of the rice leaf microbiome is modulated by multiple interactions among host, microbes, and environment. Our data provide insight into the factors influencing microbial assemblage in the rice leaf and also opens the door for future initiatives to modulate rice consortia for crop improvement efforts.