Abstract
Bacterial blight, caused by Xanthomonas oryzae pv. oryzae (Xoo), is the most important bacterial disease in rice (Oryza sativa L.). Our previous studies have revealed that the bacterial blight resistance gene Xa23 from wild rice O. rufipogon Griff. confers the broadest-spectrum resistance against all the naturally occurring Xoo races. As a novel executor R gene, Xa23 is transcriptionally activated by the bacterial avirulence (Avr) protein AvrXa23 via binding to a 28-bp DNA element (EBEAvrXa23) in the promoter region. So far, the evolutionary mechanism of Xa23 remains to be illustrated. Here, a rice germplasm collection of 97 accessions, including 29 rice cultivars (indica and japonica) and 68 wild relatives, was used to analyze the evolution, phylogeographic relationship and association of Xa23 alleles with bacterial blight resistance. All the ~ 473 bp DNA fragments consisting of promoter and coding regions of Xa23 alleles in the germplasm accessions were PCR-amplified and sequenced, and nine single nucleotide polymorphisms (SNPs) were detected in the promoter regions (~131 bp sequence upstream from the start codon ATG) of Xa23/xa23 alleles while only two SNPs were found in the coding regions. The SNPs in the promoter regions formed 5 haplotypes (Pro-A, B, C, D, E) which showed no significant difference in geographic distribution among these 97 rice accessions. However, haplotype association analysis indicated that Pro-A is the most favored haplotype for bacterial blight resistance. Moreover, SNP changes among the 5 haplotypes mostly located in the EBE/ebe regions (EBEAvrXa23 and corresponding ebes located in promoters of xa23 alleles), confirming that the EBE region is the key factor to confer bacterial blight resistance by altering gene expression. Polymorphism analysis and neutral test implied that Xa23 had undergone a bottleneck effect, and selection process of Xa23 was not detected in cultivated rice. In addition, the Xa23 coding region was found highly conserved in the Oryza genus but absent in other plant species by searching the plant database, suggesting that Xa23 originated along with the diversification of the Oryza genus from the grass family during evolution. This research offers a potential for flexible use of novel Xa23 alleles in rice breeding programs and provide a model for evolution analysis of other executor R genes.
Highlights
Plants could co-evolve in response to changes of pathogens [1]
Our previous work indicated that Xa23 is a single copy gene in the rice variety CBB23 and the 28-bp EBEAvrXa23 localized in the Xa23 promoter is the core element for interaction with the pathogen effector AvrXa23
In Oryza, the coding regions of Xa23 alleles ranged from 327 bp to 492 bp in length and the nucleotide sequence identity compared with Xa23 in CBB23 ranged from 88% to 100%
Summary
Plants could co-evolve in response to changes of pathogens [1]. Plants have evolved resistance (R) genes to interact with their cognate avr genes and activate host immune responses [3, 4]. Intensive diversifying selection allowed the pathogen to diversify its effector genes and escape recognition by the plant resistance gene, resulting in loss of the R gene-mediated resistance [1]. The constant interactions between hosts and pathogens are thought to play an important role in the evolution of R genes in plants and avr genes in pathogens. An in-depth study of the molecular evolution of R genes will be of significance for identifying novel or “hidden” resistant alleles and unravelling the role of pathogen-imposed selection of R genes [5,6,7,8]
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