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      • The bacterial type III-secreted protein AvrRps4 is a bipartite effector

        Halane, Morgan K.,Kim, Sang Hee,Spears, Benjamin J.,Garner, Christopher M.,Rogan, Conner J.,Okafor, Elizabeth C.,Su, Jianbin,Bhattacharjee, Saikat,Gassmann, Walter Public Library of Science 2018 PLoS pathogens Vol.14 No.3

        <▼1><P>Bacterial effector proteins secreted into host plant cells manipulate those cells to the benefit of the pathogen, but effector-triggered immunity (ETI) occurs when effectors are recognized by host resistance proteins. The RPS4/RRS1 pair recognizes the <I>Pseudomonas syringae</I> pv. pisi effector AvrRps4. AvrRps4 is processed <I>in planta</I> into AvrRps4<SUP>N</SUP> (133 amino acids), homologous to the N-termini of other effectors including the native <I>P</I>. <I>syringae</I> pv. tomato strain DC3000 effector HopK1, and AvrRps4<SUP>C</SUP> (88 amino acids). Previous data suggested that AvrRps4<SUP>C</SUP> alone is necessary and sufficient for resistance when overexpressed in heterologous systems. We show that delivering AvrRps4<SUP>C</SUP> from DC3000, but not from a DC3000 <I>hopK1</I><SUP><I>-</I></SUP> strain, triggers resistance in the Arabidopsis accession Col-0. Delivering AvrRps4<SUP>C</SUP> in tandem with AvrRps4<SUP>N</SUP>, or as a chimera with HopK1<SUP>N</SUP>, fully complements AvrRps4-triggered immunity. AvrRps4<SUP>N</SUP> in the absence of AvrRps4<SUP>C</SUP> enhances virulence in Col-0. In addition, AvrRps4<SUP>N</SUP> triggers a hypersensitive response in lettuce that is attenuated by coexpression of AvrRps4<SUP>C</SUP>, further supporting the role of AvrRps4<SUP>N</SUP> as a bona fide effector domain. Based on these results we propose that evolutionarily, fusion of AvrRps4<SUP>C</SUP> to AvrRps4<SUP>N</SUP> may have counteracted recognition of AvrRps4<SUP>N</SUP>, and that the plant <I>RPS4/RRS1</I> resistance gene pair was selected as a countermeasure. We conclude that AvrRps4 represents an unusual chimeric effector, with recognition in Arabidopsis by RPS4/RRS1 requiring the presence of both processed effector moieties.</P></▼1><▼2><P><B>Author summary</B></P><P>An important component of the plant immune system relies on the detection of pathogen-derived effectors by immune receptors called resistance proteins. Bacterial pathogens inject effectors into the host cell via a dedicated secretion system to suppress defenses and to manipulate the physiology of the host cell to the pathogen's advantage. Usually, a single resistance protein recognizes a single effector, but an increasing number of exceptions and elaborations on this one-to-one relationship are known. The plant Arabidopsis uses a pair of resistance proteins, RRS1 and RPS4, to detect the effector AvrRps4. After injection into the cell, AvrRps4 is cleaved into two protein parts, and it had been assumed that only the C-terminal part needs to be present to trigger RPS4/RRS1. We show here that both AvrRps4 parts are required for triggering resistance in Arabidopsis, and that the N-terminal part, which previously had been assumed to only function in effector secretion into the host cell, in fact on its own has some functions of an effector. This conclusion is supported by the observation that the N-terminal part of AvrRps4 is sufficient to trigger resistance in lettuce. The fusion of the two AvrRps4 parts may have arisen to counteract plant defenses.</P></▼2>

      • KCI등재

        Pi5 and Pii Paired NLRs Are Functionally Exchangeable and Confer Similar Disease Resistance Specificity

        Vo, Kieu Thi Xuan,Lee, Sang-Kyu,Halane, Morgan K.,Song, Min-Young,Hoang, Trung Viet,Kim, Chi-Yeol,Park, Sook-Young,Jeon, Junhyun,Kim, Sun Tae,Sohn, Kee Hoon,Jeon, Jong-Seong Korean Society for Molecular and Cellular Biology 2019 Molecules and cells Vol.42 No.9

        Effector-triggered immunity (ETI) is an effective layer of plant defense initiated upon recognition of avirulence (Avr) effectors from pathogens by cognate plant disease resistance (R) proteins. In rice, a large number of R genes have been characterized from various cultivars and have greatly contributed to breeding programs to improve resistance against the rice blast pathogen Magnaporthe oryzae. The extreme diversity of R gene repertoires is thought to be a result of co-evolutionary history between rice and its pathogens including M. oryzae. Here we show that Pii is an allele of Pi5 by DNA sequence characterization and complementation analysis. Pii-1 and Pii-2 cDNAs were cloned by reverse transcription polymerase chain reaction from the Pii-carrying cultivar Fujisaka5. The complementation test in susceptible rice cultivar Dongjin demonstrated that the rice blast resistance mediated by Pii, similar to Pi5, requires the presence of two nucleotide-binding leucine-rich repeat genes, Pii-1 and Pii-2. Consistent with our hypothesis that Pi5 and Pii are functionally indistinguishable, the replacement of Pii-1 by Pi5-1 and Pii-2 by Pi5-2, respectively, does not change the level of disease resistance to M. oryzae carrying AVR-Pii. Surprisingly, Exo70F3, required for Pii-mediated resistance, is dispensable for Pi5-mediated resistance. Based on our results, despite similarities observed between Pi5 and Pii, we hypothesize that Pi5 and Pii pairs require partially distinct mechanisms to function.

      • KCI등재

        Pi5 and Pii Paired NLRs Are Functionally Exchangeable and Confer Similar Disease Resistance Specificity

        VO THI XUAN KIEU,이상규,Morgan K. Halane,송민영,Trung Viet Hoang,김치열,박숙영,전준현,김선태,손기훈,전종성 한국분자세포생물학회 2019 Molecules and cells Vol.42 No.9

        Effector-triggered immunity (ETI) is an effective layer of plant defense initiated upon recognition of avirulence (Avr) effectors from pathogens by cognate plant disease resistance (R) proteins. In rice, a large number of R genes have been characterized from various cultivars and have greatly contributed to breeding programs to improve resistance against the rice blast pathogen Magnaporthe oryzae. The extreme diversity of R gene repertoires is thought to be a result of co-evolutionary history between rice and its pathogens including M. oryzae. Here we show that Pii is an allele of Pi5 by DNA sequence characterization and complementation analysis. Pii-1 and Pii-2 cDNAs were cloned by reverse transcription polymerase chain reaction from the Pii-carrying cultivar Fujisaka5. The complementation test in susceptible rice cultivar Dongjin demonstrated that the rice blast resistance mediated by Pii, similar to Pi5, requires the presence of two nucleotide-binding leucine-rich repeat genes, Pii-1 and Pii-2. Consistent with our hypothesis that Pi5 and Pii are functionally indistinguishable, the replacement of Pii-1 by Pi5-1 and Pii-2 by Pi5-2, respectively, does not change the level of disease resistance to M. oryzae carrying AVR-Pii. Surprisingly, Exo70F3, required for Pii-mediated resistance, is dispensable for Pi5-mediated resistance. Based on our results, despite similarities observed between Pi5 and Pii, we hypothesize that Pi5 and Pii pairs require partially distinct mechanisms to function.

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