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Multiple Alleles Encoding Atypical NLRs with Unique Central Tandem Repeats in Rice Confer Resistance to Xanthomonas oryzae pv. oryzae.

ABSTRACT: Plants have developed various mechanisms for avoiding pathogen invasion, including resistance (R) genes. Most R genes encode nucleotide-binding domain and leucine-rich repeat containing proteins (NLRs). Here, we report the isolation of three new bacterial blight R genes in rice, Xa1-2, Xa14, and Xa31(t), which were allelic to Xa1 and encoded atypical NLRs with unique central tandem repeats (CTRs). We also found that Xa31(t) was the same gene as Xa1-2. Although Xa1-2 and Xa14 conferred different resistance spectra, their performance could be attenuated by iTALEs, as has previously been reported for Xa1. XA1, XA1-2, XA14, and non-resistant RGAF differed mainly in the substructure of the leucine-rich repeat domain. They all contained unique CTRs and belonged to the CTR-NLRs, which existed only in Gramineae. We also found that interactions among these genes led to differing resistance performance. In conclusion, our results uncover a unique locus in rice consisting of at least three multiple alleles (Xa1, Xa1-2, and Xa14) that encode CTR-NLRs and confer resistance to Xanthomonas oryzae pv. oryzae (Xoo).

SUBMITTER: Zhang B

PROVIDER: S-EPMC7748011 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Multiple Alleles Encoding Atypical NLRs with Unique Central Tandem Repeats in Rice Confer Resistance to Xanthomonas oryzae pv. oryzae.

Zhang Biaoming B Zhang Haitao H Li Fang F Ouyang Yidan Y Yuan Meng M Li Xianghua X Xiao Jinghua J Wang Shiping S

Plant communications 20200620 4

Plants have developed various mechanisms for avoiding pathogen invasion, including resistance (R) genes. Most R genes encode nucleotide-binding domain and leucine-rich repeat containing proteins (NLRs). Here, we report the isolation of three new bacterial blight R genes in rice, Xa1-2, Xa14, and Xa31(t), which were allelic to Xa1 and encoded atypical NLRs with unique central tandem repeats (CTRs). We also found that Xa31(t< ...[more]

PMID: 33367251

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Project description:BackgroundXanthomonas oryzae pv oryzae is a devastating pathogen of rice and has been extensively studied as a model pathogen of monocotyledons. Expressional studies in both the contenders have been undertaken in past to understand the molecular mechanism underlying the compatible and incompatible interactions in the pathosystem. Continuous update on database and gene annotations necessitates constant updating on the roles of the new entities as well as reinterpretation of regulations of the previous ones. Moreover the past endeavors have addressed the middle or late defense responses of the rice plant whereas in the present study an attempt has been made to investigate the early defense responses taking place immediately after inoculation.ResultsMicroarray was used to study the transcriptional modulations in eighteen days old rice seedling leaves of both susceptible and resistant genotypes one hour after inoculation. In resistant plants as compared to susceptible ones 274 genes were found to be differentially expressed. Annotations could be assigned to 112 up- and 73 down-regulated transcripts and gene interaction maps were generated for 86 transcripts. Expressional data and interaction maps were used to develop a hypothetical scheme of the molecular events taking place during early defense response. Network analysis with the differential transcripts showed up-regulation of major clusters of cell signaling proteins and transcription factors while growth and basal metabolic components were largely found to be down-regulated.ConclusionsThis study provides an understanding of the early defense signaling in rice cells. Components of the calcium and lipid signaling as well as MAPK cascade were modulated, by signals from surface receptors and cytosolic R-proteins, to arouse jasmonic acid and ethylene signaling and suppress auxin signaling through various transcription factors. Abscisic acid modulation was also evident through the expression regulation of transcription factors involved with its functions. Moreover adjustments in expression levels of components of primary as well as secondary metabolism, protein trafficking and turnout were apparent, highlighting the complexity of defense response.

Project description:BackgroundPathogenic Gram-negative bacteria interact with their eukaryotic hosts by deploying the type III translocon to inject effector proteins into the cytosol of eukaryotic cells. The translocon compositions, the number and biochemical characteristics of type III translocators in animal-pathogenic bacteria have been well elucidated, but information is lacking for plant-pathogenic bacteria. With extensive studies on biological functions of the Hpa1 protein secreted by the type III secretion system in Xanthomonas oryzae pv. oryzae (Xoo), we show here that Hpa1 is a type III translocator based on measurements of two proteins categorized as transcription activator-like (TAL) effector.ResultsHpa1 was functionally associated with the TAL effector PthXo1 or AvrXa10 by genetic analysis of the wild-type Xoo strain and related mutants or recombinant strains. Inoculation experiments suggested that Hpa1 is required not only for the virulent role of PthXo1 in the susceptible rice variety Nipponbare, but also for the avirulent function of AvrXa10 on the resistant rice variety IRBB10. Hpa1 is unrelated to the secretion of PthXo1 and AvrXa10 out of bacterial cells. However, Hpa1 is critical for both TAL effectors to be translocated from bacterial cells into the cytosol of rice cells based on replicate experiments performed on the susceptible and resistant varieties, respectively. Hpa1-mediated translocation of PthXo1 is coincident with induced expression of rice SWEET11 gene, which is the regulatory target of PthXo1, resulting in the occurrence of the bacterial blight disease in the susceptible rice variety. By contrast, the immune hypersensitive response is induced in agreement with induced expression of rice Xa10 gene, which is the target of AvrXa10, only when AvrXa10 is translocated from bacteria into cells of the resistant rice variety. All the virulent or avirulent performances of the TAL effectors are nullified by directed mutation that removes the α-helix motif from the Hpa1 sequence.ConclusionsThe genetic and biochemical data demonstrate that Hap1 is a type III translocator at least for TAL effectors PthXo1 and AvrXa10. The effect of the directed mutation suggests that Hpa1 depends on its α-helical motif to fulfil the translocator function.

Dataset Information

Multiple Alleles Encoding Atypical NLRs with Unique Central Tandem Repeats in Rice Confer Resistance to Xanthomonas oryzae pv. oryzae.

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Multiple Alleles Encoding Atypical NLRs with Unique Central Tandem Repeats in Rice Confer Resistance to <i>Xanthomonas oryzae</i> pv. <i>oryzae</i>.

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