Evolutionary Dynamics of the Genomic Region around the Blast Resistance Gene Pi-Ta in AA Genome Oryza Species

By Lee, Seonghee; Costanzo, Stefano et al. | Genetics, December 2009 | Go to article overview

Evolutionary Dynamics of the Genomic Region around the Blast Resistance Gene Pi-Ta in AA Genome Oryza Species


Lee, Seonghee, Costanzo, Stefano, Jia, Yulin, Olsen, Kenneth M., Caicedo, Ana L., Genetics


ABSTRACT

The race-specific resistance gene Pi-ta has been effectively used to control blast disease, one of the most destructive plant diseases worldwide. A single amino acid change at the 918 position of the Pi-ta protein was known to determine resistance specificity. To understand the evolutionary dynamics present, we examined sequences of the Pi-ta locus and its flanking regions in 159 accessions composed of seven AA genome Oryza species: O. sativa, O. rufipogon, O. nivara, O. meridionalis, O. glaberrima, O. barthii, and O. glumaepatula. A 3364-bp fragment encoding a predicted transposon was found in the proximity of the Pi-ta promoter region associated with the resistance phenotype. Haplotype network analysis with 33 newly identified Pi-ta haplotypes and 18 newly identified Pi-ta protein variants demonstrated the evolutionary relationships of Pi-ta haplotypes between O. sativa and O. rufipogon. In O. rufipogon, the recent directional selection was found in the Pi-ta region, while significant deviation from neutral evolution was not found in all O. sativa groups. Results of sequence variation in flanking regions around Pi-ta in O. sativa suggest that the size of the resistant Pi-ta introgressed block was at least 5.4 Mb in all elite resistant cultivars but not in the cultivars without Pi-ta. These findings demonstrate that the Pi-ta region with transposon and additional plant modifiers has evolved under an extensive selection pressure during crop breeding.

(ProQuest: ... denotes formulae omitted.)

PLANT resistance (R) genes have evolved to fight against a wide range of pathogens in a race-specific manner where a particular R gene in a plant recognizes the corresponding avirulence (AVR) gene in a pathogen race (Flor 1971). Thus far, a number of R genes have been identified and characterized from diverse plant species. Most characterized R genes to date encode putative proteins with nucleotide binding sites (NBS) and leucine-rich repeats (LRR) (Hulbert et al. 2001). Most R genes are highly polymorphic and diversified, which is consistent with the ability to interact with diverse random molecules encoded by diverse pathogen AVR genes (Meyers et al. 2003; Bakker et al. 2006; Shen et al. 2006).

Blast disease, caused by the filamentous ascomycete Magnaporthe oryzae B.C. Couch [formerly M. grisea (T. T. Hebert) M. E. Barr] (Rossman et al. 1990; Couch and Kohn 2002), has been one of the major constraints to stable crop production. Currently, Oryza sativa and M. oryzae have been an excellent model pathosystem for uncovering the molecular coevolution mechanisms of host-pathogen (Valent et al. 1991; Talbot 2003). At least 80 race-specific R genes that confer resistance to specific pathogen races have been described in rice germplasm (Ballini et al. 2008). Eleven blast R genes (Pi-ta, Pib, Pi2/Piz-t, Pi5, Pi9, Pi21, Pi36, Pi37, Pi-d2, Pikm, and Pit) have been cloned, and most of them, except Pi21 and Pi-d2, were also predicted to encode receptor proteins with NBS (Chen et al. 2006; Fukuoka et al. 2009; Jia et al. 2009b). In most cases, blast R genes are members of small gene families with a single family member required for resistance. Pikm and Pi5 are exceptions that require two members of the same gene family for Pikm- and Pi5-mediated resistance, respectively (Ashikawa et al. 2008; Lee et al. 2009). Recently, a retrotransposon was predicted to be involved in the Pit resistance (Hayashi and Yoshida 2009).

The evolutionary dynamics and mechanisms of resistance mediated by Pi-ta is one of the best-studied Rgenes. Pi-ta has been effectively deployed in the United States and around the globe for controlling blast disease (Bryan et al. 2000; Jia et al. 2000; Jia 2003; Jia et al. 2004a,b;Huang et al. 2008; Jia andMartin 2008;Wang et al. 2008; Jia et al. 2009a). Pi-ta encodes a predicted cytoplasmic protein with a centrally located NBS and a highly interrupted LRR domain (referred to as the LRD) at the carboxyl terminus that recognizes the corresponding avirulence gene AVR-Pita, triggering race-specific resistance. …

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Evolutionary Dynamics of the Genomic Region around the Blast Resistance Gene Pi-Ta in AA Genome Oryza Species
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