The <scp>NB</scp>‐<scp>LRR</scp> proteins <scp>RGA</scp>4 and <scp>RGA</scp>5 interact functionally and physically to confer disease resistance

Césari, Stella; Kanzaki, Hiromitsu; Fujiwara, Tadashi; Bernoux, Maud; Chalvon, Véronique; Kawano, Yoji; Shimamoto, Ko; Dodds, Peter N.; Terauchi, Ryohei; Kroj, Thomas

doi:10.15252/embj.201487923

Cited by 293 publications

(188 citation statements)

References 79 publications

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“…Self-interaction was detected for the rice Resistance Gene Analog 5 (RGA5) CC and L6-TIR domain, the positive controls in this experiment ( Fig. S4) (7,17).…”

Section: Resultsmentioning

confidence: 73%

“…Consistent with previous reports, MLA10 :HA and MLA10 :CFP also induced a strong cell-death response. A positive control protein, the rice autoactive CC-NLR RGA4, produced a strong cell-death response, but its inactive T 500 M/Y 501 H/G 502 D mutant (rga4 TYG/MHD ) did not (16,17). Expression of the CC-NB fragments of Sr33 (residues 1-225), Sr50 (1-228), and MLA10 (1-225) also triggered a cell-death response (Fig.…”

Section: Resultsmentioning

confidence: 94%

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Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Césari¹,

Moore²,

Chen³

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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103

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Plants possess intracellular immune receptors designated “nucleotide-binding domain and leucine-rich repeat” (NLR) proteins that translate pathogen-specific recognition into disease-resistance signaling. The wheat immune receptors Sr33 and Sr50 belong to the class of coiled-coil (CC) NLRs. They confer resistance against a broad spectrum of field isolates of Puccinia graminis f. sp. tritici, including the Ug99 lineage, and are homologs of the barley powdery mildew-resistance protein MLA10. Here, we show that, similarly to MLA10, the Sr33 and Sr50 CC domains are sufficient to induce cell death in Nicotiana benthamiana. Autoactive CC domains and full-length Sr33 and Sr50 proteins self-associate in planta. In contrast, truncated CC domains equivalent in size to an MLA10 fragment for which a crystal structure was previously determined fail to induce cell death and do not self-associate. Mutations in the truncated region also abolish self-association and cell-death signaling. Analysis of Sr33 and Sr50 CC domains fused to YFP and either nuclear localization or nuclear export signals in N. benthamiana showed that cell-death induction occurs in the cytosol. In stable transgenic wheat plants, full-length Sr33 proteins targeted to the cytosol provided rust resistance, whereas nuclear-targeted Sr33 was not functional. These data are consistent with CC-mediated induction of both cell-death signaling and stem rust resistance in the cytosolic compartment, whereas previous research had suggested that MLA10-mediated cell-death and disease resistance signaling occur independently, in the cytosol and nucleus, respectively.

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“…Self-interaction was detected for the rice Resistance Gene Analog 5 (RGA5) CC and L6-TIR domain, the positive controls in this experiment ( Fig. S4) (7,17).…”

Section: Resultsmentioning

confidence: 73%

Section: Resultsmentioning

confidence: 94%

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Césari¹,

Moore²,

Chen³

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

103

116

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“…By combing the metabolome and transcriptome findings, 23 novel genes were found playing roles in both metabolic processes and expression regulation. (Fig 3a,b) that have high homology to rice NBS-LRR genes Os11gRGA4 and Os11gRGA5, which were shown to interact functionally and physically to mediate resistance to the fungal pathogen Magnaporthe oryzae (Okuyama et al 2011;Césari et al 2014). Recent studies have verified that inducing plant immunity impacts flavonoid biosynthesis (Ali et al 2011;Serrano et al 2012), and that flavonoid compounds significantly contribute to plant resistance (Treutter 2005;Treutter 2006).…”

Section: Maize Pan-transcriptome Plays An Important Role In Regulatinmentioning

confidence: 99%

Maize pan-transcriptome provides novel insights into genome complexity and quantitative trait variation

Jin

Liu

et al. 2015

Preprint

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Variation in gene expression contributes to the diversity of phenotype. The construction of the pan-transcriptome is especially necessary for species with complex genomes, such as maize. However, knowledge of the regulation mechanisms and functional consequences of the pan-transcriptome is limited. In this study, we identified 13,382 nuclear expression presence and absence variation candidates (ePAVs, expressed in 5%~95% lines; based on the reference genome) by re-analyzing the RNA sequencing data from the kernels (15 days after pollination) of 368 maize diverse inbreds. It was estimated that only ~1% of the ePAVs are explained by DNA sequence presence and absence variations (PAV). The ePAV genes tend to be regulated by distant eQTLs when compared with non-ePAV genes (called here core expression genes, expressed in more than 95% lines). When the expression presence/absence status was used as the "genotype" to perform genome-wide association study, 56 (0.42%) ePAVs were significantly associated with 15 agronomic traits and 1,967 (14.74%) with 526 metabolic traits, measured from the mature kernels. While the above was majorly based on the reference genome, by using a modified 'assemble-then-align' strategy, 2,355 high confidence novel sequences with a total length of 1.9Mb were found absent in the current B73 reference genome (v2). Ten randomly selected novel sequences were validated with genomic PCR. A simulation analysis suggested that the pan-transcriptome of the maize whole kernel is approaching a maximum value of 63,000 genes. Two novel validated sequences annotated as NBS_LRR like genes were found to associate with flavonoid content and their homologs in rice were also found to affect flavonoids and disease-resistance. Novel sequences absent in the present reference genome might be functionally important and deserve more attentions. This study provides novel perspectives and resources to discover maize quantitative trait variations and help us to better understand the kernel regulation networks, thus enhancing maize breeding.

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“…The two genes are both required for the recognition and the defence response of the M. oryzae effector AVR-Pia. Further study showed that RGA5 directly binds to RGA4 to repress an RGA4-triggered effector-independent cell-death response (Cé sari et al, 2014). RGA5 seems to play a central role in the recognition because of its direct interaction with both AVR-Pia and RGA4.…”

Section: Introductionmentioning

confidence: 98%

Expression, purification, crystallization and preliminary X-ray diffraction analysis of the effector-interaction domain of the resistance protein RGA5-A fromOryza sativaL.japonica

et al. 2015

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RGA5-A, a component of the Pia resistance-protein complex (RGA4/RGA5-A) from Oryza sativa L. japonica, has the ability to interact physically with the effector protein AVR-Pia from Magnaporthe oryzae via its effector-interaction domain RGA5-A_S. The interaction between RGA5-A and AVR-Pia relieves the repression of RGA4, leading to AVR-independent cell death by the freed RGA4. To further understand the details of this interaction, the effectorinteraction domain RGA5-A_S was expressed in Escherichia coli and purified to homogeneity. The purified recombinant protein His-RGA5-A_S was successfully crystallized using the sitting-drop vapour-diffusion method. A single crystal obtained using 0.2 M ammonium citrate, 25%(w/v) PEG 3350 diffracted to 2.43 Å resolution. It belonged to space group P4 1 22 or P4 3 22, with unit-cell parameters a = b = 55.2, c = 78.2 Å , = = = 90 .

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The NB‐LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance

Cited by 293 publications

References 79 publications

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

Maize pan-transcriptome provides novel insights into genome complexity and quantitative trait variation

Expression, purification, crystallization and preliminary X-ray diffraction analysis of the effector-interaction domain of the resistance protein RGA5-A fromOryza sativaL.japonica

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