Seonghee Lee

Host Versus Nonhost Resistance: Distinct Wars with Similar Arsenals

Plants face several challenges by bacterial, fungal, oomycete, and viral pathogens during their life cycle. In order to defend against these biotic stresses, plants possess a dynamic, innate, natural immune system that efficiently detects potential pathogens and initiates a resistance response in the form of basal resistance and/or resistance (R)-gene-mediated defense, which is often associated with a hypersensitive response. Depending upon the nature of plant-pathogen interactions, plants generally have two main defense mechanisms, host resistance and nonhost resistance. Host resistance is generally controlled by single R genes and less durable compared with nonhost resistance. In contrast, nonhost resistance is believed to be a multi-gene trait and more durable. In this review, we describe the mechanisms of host and nonhost resistance against fungal and bacterial plant pathogens. In addition, we also attempt to compare host and nonhost resistance responses to identify similarities and differences, and their practical applications in crop improvement.

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

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.

Arabidopsis Heterotrimeric G-Proteins Play a Critical Role in Host and Nonhost Resistance against Pseudomonas syringae Pathogens

Heterotrimeric G-proteins have been proposed to be involved in many aspects of plant disease resistance but their precise role in mediating nonhost disease resistance is not well understood. We evaluated the roles of specific subunits of heterotrimeric G-proteins using knock-out mutants of Arabidopsis Gα, Gβ and Gγ subunits in response to host and nonhost Pseudomonas pathogens. Plants lacking functional Gα, Gβ and Gγ1Gγ2 proteins displayed enhanced bacterial growth and disease susceptibility in response to host and nonhost pathogens. Mutations of single Gγ subunits Gγ1, Gγ2 and Gγ3 did not alter bacterial disease resistance. Some specificity of subunit usage was observed when comparing host pathogen versus nonhost pathogen. Overexpression of both Gα and Gβ led to reduced bacterial multiplication of nonhost pathogen P. syringae pv. tabaci whereas overexpression of Gβ, but not of Gα, resulted in reduced bacterial growth of host pathogen P. syringae pv. maculicola, compared to wild-type Col-0. Moreover, the regulation of stomatal aperture by bacterial pathogens was altered in Gα and Gβ mutants but not in any of the single or double Gγ mutants. Taken together, these data substantiate the critical role of heterotrimeric G-proteins in plant innate immunity and stomatal modulation in response to P. syringae.

Molecular Evolution of the Rice Blast Resistance Gene Pi-ta in Invasive Weedy Rice in the USA

The Pi-ta gene in rice has been effectively used to control rice blast disease caused by Magnaporthe oryzae worldwide. Despite a number of studies that reported the Pi-ta gene in domesticated rice and wild species, little is known about how the Pi-ta gene has evolved in US weedy rice, a major weed of rice. To investigate the genome organization of the Pi-ta gene in weedy rice and its relationship to gene flow between cultivated and weedy rice in the US, we analyzed nucleotide sequence variation at the Pi-ta gene and its surrounding 2 Mb region in 156 weedy, domesticated and wild rice relatives. We found that the region at and around the Pi-ta gene shows very low genetic diversity in US weedy rice. The patterns of molecular diversity in weeds are more similar to cultivated rice (indica and aus), which have never been cultivated in the US, rather than the wild rice species, Oryza rufipogon. In addition, the resistant Pi-ta allele (Pi-ta) found in the majority of US weedy rice belongs to the weedy group strawhull awnless (SH), suggesting a single source of origin for Pi-ta. Weeds with Pi-ta were resistant to two M. oryzae races, IC17 and IB49, except for three accessions, suggesting that component(s) required for the Pi-ta mediated resistance may be missing in these accessions. Signatures of flanking sequences of the Pi-ta gene and SSR markers on chromosome 12 suggest that the susceptible pi-ta allele (pi-ta), not Pi-ta, has been introgressed from cultivated to weedy rice by out-crossing.

Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by nonhost bacterial pathogens

Pseudomonas syringae is the most widespread bacterial pathogen in plants. Several strains of P. syringae produce a phytotoxin, coronatine (COR), which acts as a jasmonic acid mimic and inhibits plant defense responses and contributes to disease symptom development. In this study, we found that COR inhibits early defense responses during nonhost disease resistance. Stomatal closure induced by a nonhost pathogen, P. syringae pv. tabaci, was disrupted by COR in tomato epidermal peels. In addition, nonhost HR cell death triggered by P. syringae pv. tabaci on tomato was remarkably delayed when COR was supplemented along with P. syringae pv. tabaci inoculation. Using isochorismate synthase (ICS)-silenced tomato plants and transcript profiles of genes in SA- and JA-related defense pathways, we show that COR suppresses SA-mediated defense during nonhost resistance.

Identification of two major resistance genes against race IE-1k of Magnaporthe oryzae in the indica rice cultivar Zhe733

The race IE-1k of Magnaporthe oryzae recovered from the Southern US overcomes the resistance (R) gene Pita. The objectives of the present study were to identify and tag R genes to IE-1k for rice breeding. TM2, S1, 94071, and B isolates of the race IE-1k were used to identify and map R genes from a resistant indica rice cultivar Zhe733 using a recombinant inbred line population from a cross of the genetic stock KBNTlpa1-1 and Zhe733. The ratio of 3 resistant:1 susceptible in 162 RIL of an F10-11 KBNTlpa1-1/Zhe733 (K/Z) population indicated that two major R genes in Zhe733 confer resistance to IE-1k. A total of 118 polymorphic simple sequence repeat markers were analyzed in 162 F10-11 individuals of the K/Z population to determine chromosomal locations of the loci conferring resistance to race IE-1k using composite interval mapping. Two major R genes temporarily designated as Pi42(t) and Pi43(t) each providing complete resistance to IE-1k were identified on chromosomes 8 and 11, respectively. RILs containing Pi42(t) and Pi43(t) were also resistant to other US races IB-1, IB-45, IB-49, IB-54, IC-17, IE-1, IG-1, and IH-1. The Pi42(t) gene was mapped between RM310 and RM72, and the location of Pi43(t) was closely associated with two flanking SSR markers RM1233 and RM224 on chromosome 11 in a chromosomal region carrying the resistance gene Pi1. Two molecular markers RM72 and RM1233 identified in this study should be useful for fine mapping and for facilitating incorporation of Pi42(t) and Pi43(t) into advanced breeding lines by marker-assisted selection.

Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana

BackgroundPseudomonas syringae pv. tabaci (Pstab) is the causal agent of wildfire disease in tobacco plants. Several pathovars of Pseudomonas syringae produce a phytotoxic extracellular metabolite called coronatine (COR). COR has been shown to suppress plant defense responses. Interestingly, Pstab does not produce COR but still actively suppresses early plant defense responses. It is not clear if Pstab produces any extracellular metabolites that actively suppress early defense during bacterial pathogenesis.ResultsWe found that the Pstab extracellular metabolite extracts (Pstab extracts) remarkably suppressed stomatal closure and nonhost hypersensitive response (HR) cell death induced by a nonhost pathogen, P. syringae pv. tomato T1 (Pst T1), in Nicotiana benthamiana. We also found that the accumulation of nonhost pathogens, Pst T1 and P. syringae pv. glycinea (Psgly), was increased in N. benthamiana plants upon treatment with Pstab extracts . The HR cell death induced by Pathogen-Associated Molecular Pattern (INF1), gene-for-gene interaction (Pto/AvrPto and Cf-9/AvrCf-9) and ethanol was not delayed or suppressed by Pstab extracts. We performed metabolite profiling to investigate the extracellular metabolites from Pstab using UPLC-qTOF-MS and identified 49 extracellular metabolites from the Pstab supernatant culture. The results from gene expression profiling of PR-1, PR-2, PR-5, PDF1.2, ABA1, COI1, and HSR203J suggest that Pstab extracellular metabolites may interfere with SA-mediated defense pathways.ConclusionsIn this study, we found that Pstab extracts suppress plant defense responses such as stomatal closure and nonhost HR cell death induced by the nonhost bacterial pathogen Pst T1 in N. benthamiana.

Coevolutionary Dynamics of Rice Blast Resistance Gene Pi-ta and Magnaporthe oryzae Avirulence Gene AVR-Pita 1.

The Pi-ta gene in rice is effective in preventing infections by Magnaporthe oryzae strains that contain the corresponding avirulence gene, AVR-Pita1. Diverse haplotypes of AVR-Pita1 have been identified from isolates of M. oryzae from rice production areas in the United States and worldwide. DNA sequencing and mapping studies have revealed that AVR-Pita1 is highly unstable, while expression analysis and quantitative resistance loci mapping of the Pi-ta locus revealed complex evolutionary mechanisms of Pi-ta-mediated resistance. Among these studies, several Pi-ta transcripts were identified, most of which are probably derived from alternative splicing and exon skipping, which could produce functional resistance proteins that support a new concept of coevolution of Pi-ta and AVR-Pita1. User-friendly DNA markers for Pi-ta have been developed to support marker-assisted selection, and development of new rice varieties with the Pi-ta markers. Genome-wide association studies revealed a link between Pi-ta-mediated resistance and yield components suggesting that rice has evolved a complicated defense mechanism against the blast fungus. In this review, we detail the current understanding of Pi-ta allelic variation, its linkage with rice productivity, AVR-Pita allelic variation, and the coevolution of Pi-ta and AVR-Pita in Oryza species and M. oryzae populations, respectively. We also review the genetic and molecular basis of Pi-ta and AVR-Pita interaction, and its value in marker-assisted selection and engineering resistance.

Understanding the Co-evolution of the Rice Blast Resistance Gene PI-TA and Magnaporthe oryzae Avirulence Gene AVR-PITA

The Pi-ta gene in rice effectively prevents infection by races of Magnaporthe oryzae that contain the corresponding AVR gene, AVR-Pita. Pi-ta is a putative cytoplasmic protein with a centrally located nucleotide binding sites (NBS) and a leucine rich domain (LRD) at the carboxyl terminus. The Pi-ta gene has been deployed effectively in preventing rice blast in the southern US since 1990. AVR-Pita encodes a predicted metalloprotease, and its processed form, AVR-Pita176

General control non-repressible-4 (GCN4) degrades 14-3-3 and RIN4 complex to regulate stomatal aperture with implications on nonhost resistance and drought tolerance

, was shown to directly bind with the Pi-ta protein in triggering effective defense responses. Variants of AVR-Pita were identified in many contemporary M. oryzae races and in isolates collected during the last 30 years in the US. Sequence analysis of these AVR-Pita variants revealed that the AVR-Pita protein might be under diversified selection. Most recently, sequence analysis of the Pi-ta variants in six Oryza species (O. sativa, O. glaberrima, O. officialis, O. rufipogon, O. barthii and O. nivara) revealed that functional nucleotide polymorphism at the position of 918 (FNP918) is present among all these Oryzae species, and Pi-ta may be under balanced selection. Our results suggest that Pi-ta co-evolves with AVR-Pita, and that rice engages trench warfare with M. oryzae during the host and pathogen co-evolution.