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.

Rice sheath blight, caused by the necrotrophic fungus Rhizoctonia solani Kühn, continues to be an important and challenging rice disease worldwide. Here, we used genome-wide association studies over a high-density rice array to facilitate the identification of potential novel genes and quantitative trait loci related to sheath blight resistance. We identified multiple regions that significantly associated with independent disease components in chromosomes 1, 4, and 11 under controlled condition. In particular, we investigated qLN1128, a quantitative trait locus enriched with defense-related genes that reduce disease lesions in a near-isogenic line. RNA profiling of the line carrying qLN1128 showed a number of differentially expressed genes related to the reactive oxygen species (ROS)-redox pathway. Histochemical staining revealed less ROS accumulation on the resistant line, suggesting efficient ROS deregulation that delays pathogen colonization. The detection of genomic regions controlling multiple mechanisms of resistance to sheath blight will provide tools to design effective breeding interventions in rice.

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.

Bacterial blight (X. oryzae pv. oryzae) is a serious disease in rice across the world. To better control the disease, it is important to understand its epidemiology and how key aspects of this (e.g. infection efficiency, and spatial spread) change according to environment (e.g. local site conditions and season), management, and in particular, variety resistance. To explore this, we analysed data on the disease progress on resistant and susceptible varieties of rice grown at four sites in the Philippines across five seasons using a combination of mechanistic modelling and statistical analysis. Disease incidence was generally lower in the resistant variety. However, we found no evidence that the primary infection efficiency was lower in resistant varieties, suggesting that differences were largely due to reduced secondary spread. Despite secondary spread being attributed to splash dispersal which is exacerbated by wind and rain, the wetter sites of Pila and Victoria in south Luzon tended to have lower infection rates than the drier sites in central Luzon. Likewise, we found spread in the dry season can be substantial and should therefore not be ignored. In fact, we found site to be a greater determinant of the number of infection attempts suggesting that other environmental and management factors had greater effect on the disease than climate. Primary infection was characterised by spatially-random observations of disease incidence. As the season progressed, we observed an emerging short-range (1.6 m–4 m) spatial structure suggesting secondary spread was predominantly short-range, particularly where the resistant variety was grown.