Genome-Wide Associations and Transcriptional Profiling Reveal ROS Regulation as One Underlying Mechanism of Sheath Blight Resistance in Rice.

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.

The Green Revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae.

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.

Natural variations in the promoter of OsSWEET13 and OsSWEET14 expand the range of resistance against Xanthomonas oryzae pv. oryzae.

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.

Immunity and starvation: new opportunities to elevate disease resistance in crops.

Plants use multiple mechanisms to defend themselves against invading microbes. Besides using their immune system to surveil and eliminate pathogens, plants actively block the pathogens' access to nutrients as an alternative way to prevent colonization. In this review, we focus on immunity and starvation as major obstacles for pathogens' adaptation. We summarize the key mechanisms employed by pathogens to modulate host immunity and to guarantee sugar uptake. In contrast to genes that deal with the immune system and show high levels of plasticity, pathogen genes involved in sugar acquisition are highly conserved, and may not have adapted to co-evolving interactions with the host. We propose a model to assess the durability of different control strategies based on the ability of pathogens to deal with host immunity or starvation. This analysis opens new opportunities to elevate disease resistance in crops by reducing the likelihood of pathogen adaptation.

Effector Diversification Contributes to Xanthomonas oryzae pv. oryzae Phenotypic Adaptation in a Semi-Isolated Environment.

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.

Rice-Infecting Pseudomonas Genomes Are Highly Accessorized and Harbor Multiple Putative Virulence Mechanisms to Cause Sheath Brown Rot.

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.