Disease resistance and sexual reproductive development are generally considered as separate biological processes, regulated by different sets of genes. Here we show that xa13, a recessive allele conferring disease resistance against bacterial blight, one of the most devastating rice diseases worldwide, plays a key role in both disease resistance and pollen development. The dominant allele, Xa13, is required for both bacterial growth and pollen development. Promoter mutations in Xa13 cause down-regulation of expression during host–pathogen interaction, resulting in the fully recessive xa13 that confers race-specific resistance. The recessive xa13 allele represents a new type of plant disease resistance.

WebIn both laboratory and field studies, engineering translational control of immune mediator production in Arabidopsis and rice confers disease resistance, without compromising plant fitness. It is well established that plants elicit immune responses by reprogramming their transcriptional response. Controlling this for agricultural purposes without reducing the plant's fitness has been a challenge. Xinnian Dong and colleagues have engineered translational control into Arabidopsis and rice to promote production of immune mediators and show, in laboratory and field studies, that this confers disease resistance without compromising plant fitness. This was achieved using insights from a related paper published in this issue, in which Xinnian Dong and colleagues uncover new regulators of plant immune responses. Through global translatome analysis, they observe that plants modify their translational output independently of the changes in the transcriptional output to establish pathogen-triggered immunity. Controlling plant disease has been a struggle for humankind since the advent of agriculture. Studies of plant immune mechanisms have led to strategies of engineering resistant crops through ectopic transcription of plants’ own defence genes, such as the master immune regulatory gene NPR1 (ref. 1). However, enhanced resistance obtained through such strategies is often associated with substantial penalties to fitness2, making the resulting products undesirable for agricultural applications. To remedy this problem, we sought more stringent mechanisms of expressing defence proteins. On the basis of our latest finding that translation of key immune regulators, such as TBF1 (ref. 3), is rapidly and transiently induced upon pathogen challenge (see accompanying paper4), we developed a ‘TBF1-cassette’ consisting of not only the immune-inducible promoter but also two pathogen-responsive upstream open reading frames (uORFsTBF1) of the TBF1 gene. Here we demonstrate that inclusion of uORFsTBF1-mediated translational control over the production of snc1-1 (an autoactivated immune receptor) in Arabidopsis thaliana and AtNPR1 in rice enables us to engineer broad-spectrum disease resistance without compromising plant fitness in the laboratory or in the field. This broadly applicable strategy may lead to decreased pesticide use and reduce the selective pressure for resistant pathogens.

Pathogen effectors are virulence factors causing plant diseases. How the host targets of these effectors facilitate pathogen infection is largely unknown. An effector of Xanthomonas oryzae pv oryzae (Xoo) transcriptionally activates rice (Oryza sativa) susceptibility gene Xa13 to cause bacterial blight disease. Xa13 encodes an indispensable plasma membrane protein of the MtN3/saliva family, which is prevalent in eukaryotes with unknown biochemical function. We show that the XA13 protein cooperates with two other proteins, COPT1 and COPT5, to promote removal of copper from xylem vessels, where Xoo multiplies and spreads to cause disease. Copper, an essential micronutrient of plants and an important element for a number of pesticides in agriculture, suppresses Xoo growth. Xoo strain PXO99 is more sensitive to copper than other strains; its infection of rice is associated with activation of XA13, COPT1, and COPT5, which modulate copper redistribution in rice. The involvement of XA13 in copper redistribution has led us to propose a mechanism of bacterial virulence.

The MtN3/saliva/SWEET-type genes, existing either alone or in a family group, are found in diverse organisms, from monocellular protozoa to higher eukaryotes, indicating their importance in cellular organisms. These genes encode polytopic membrane proteins that feature an MtN3/saliva domain, also known as a PQ loop repeat. The rice MtN3/saliva/SWEET gene family consists of 21 members and is among the largest families in sequenced organisms. Accumulating data suggest that these genes are involved in multiple physiological processes, including reproductive development, senescence, environmental adaptation, and host-pathogen interaction, in different species. In rice, some members of the family, including Xa13/Os8N3/OsSWEET11, which is essential for reproductive development, are used by the pathogenic bacterium Xanthomonas oryzae pv. oryzae to invade its host. Emerging data have also revealed that at least some MtN3/saliva/SWEET-type proteins may regulate different physiological processes by facilitating ion transport via interaction with ion transporters or as sugar transporters. The accumulating knowledge about MtN3/saliva/SWEET-type genes will help to elucidate the molecular bases of their function in different organisms.

Intensive rice breeding over the past 50 y has dramatically increased productivity especially in the indica subspecies, but our knowledge of the genomic changes associated with such improvement has been limited. In this study, we analyzed low-coverage sequencing data of 1,479 rice accessions from 73 countries, including landraces and modern cultivars. We identified two major subpopulations, indica I (IndI) and indica II (IndII), in the indica subspecies, which corresponded to the two putative heterotic groups resulting from independent breeding efforts. We detected 200 regions spanning 7.8% of the rice genome that had been differentially selected between IndI and IndII, and thus referred to as breeding signatures. These regions included large numbers of known functional genes and loci associated with important agronomic traits revealed by genome-wide association studies. Grain yield was positively correlated with the number of breeding signatures in a variety, suggesting that the number of breeding signatures in a line may be useful for predicting agronomic potential and the selected loci may provide targets for rice improvement. Significance Intensive rice breeding over the past 50 y has produced many high-performing cultivars, but our knowledge of the genomic changes associated with such improvement remains limited. By analyzing sequences of 1,479 rice accessions, this study identified genomic changes associated with breeding efforts, referred to as breeding signatures, involving 7.8% of the rice genome. Accumulation of selected regions is positively correlated with yield improvement. The number of selected regions in a line may be used for predicting agronomic potential, and the selected loci may provide useful targets for rice improvement.

Approximately one third of the identified 34 rice major disease resistance (R) genes conferring race‐specific resistance to different strains of Xanthomonas oryzae pv. oryzae (Xoo), which causes rice bacterial blight disease, are recessive genes. However, only two of the recessive resistance genes have been characterized thus far. Here we report the characterization of another recessive resistance gene, xa25, for Xoo resistance. The xa25, localized in the centromeric region of chromosome 12, mediates race‐specific resistance to Xoo strain PXO339 at both seedling and adult stages by inhibiting Xoo growth. It encodes a protein of the MtN3/saliva family, which is prevalent in eukaryotes, including mammals. Transformation of the dominant Xa25 into a resistant rice line carrying the recessive xa25 abolished its resistance to PXO339. The encoding proteins of recessive xa25 and its dominant allele Xa25 have eight amino acid differences. The expression of dominant Xa25 but not recessive xa25 was rapidly induced by PXO339 but not other Xoo strain infections. The nature of xa25‐encoding protein and its expression pattern in comparison with its susceptible allele in rice–Xoo interaction indicate that the mechanism of xa25‐mediated resistance appears to be different from that conferred by most of the characterized R proteins.