Tomato I2 immune receptor can be engineered to confer partial resistance to the oomycete<i>Phytophthora infestans</i>in addition to the fungus<i>Fusarium oxysporum</i>

Giannakopoulou, Artemis; Steele, John F. C.; Segretin, María Eugenia; Bozkurt, Tolga O; Zhou, Ji; Robatzek, Silke; Banfield, M.J.; Pais, Marina; Kamoun, Sophien

doi:10.1101/022079

Cited by 20 publications

(25 citation statements)

References 92 publications

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“…For example, R3a and I2, which are located at a complex R gene locus in a colinear region on chromosome 11 in potato and tomato (Solanum lycopersicum), confer resistance to the oomycete Phytophthora infestans and the soil-borne fungal pathogen Fusarium oxysporum, respectively (Huang et al, 2005). Interestingly, I2 also is able to show a weak recognition response to the cognate R3a elicitor Avr3a, which could be enhanced by a single mutation in the CC domain and even result in partial late blight resistance (Segretin et al, 2014;Giannakopoulou et al, 2015). Apparently, the R3a and I2 recognition specificity has evolved over time by sequence diversification, which enables the detection of different pathogen species.…”

Section: Discussionmentioning

confidence: 99%

Sequence Exchange between Homologous NB-LRR Genes Converts Virus Resistance into Nematode Resistance, and Vice Versa

et al. 2017

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Plants have evolved a limited repertoire of NB-LRR disease resistance (R) genes to protect themselves against myriad pathogens. This limitation is thought to be counterbalanced by the rapid evolution of NB-LRR proteins, as only a few sequence changes have been shown to be sufficient to alter resistance specificities toward novel strains of a pathogen. However, little is known about the flexibility of NB-LRR R genes to switch resistance specificities between phylogenetically unrelated pathogens. To investigate this, we created domain swaps between the close homologs Gpa2 and Rx1, which confer resistance in potato (Solanum tuberosum) to the cyst nematode Globodera pallida and Potato virus X, respectively. The genetic fusion of the CC-NB-ARC of Gpa2 with the LRR of Rx1 (Gpa2 CN /Rx1 L ) results in autoactivity, but lowering the protein levels restored its specific activation response, including extreme resistance to Potato virus X in potato shoots. The reciprocal chimera (Rx1 CN /Gpa2 L ) shows a loss-of-function phenotype, but exchange of the first three LRRs of Gpa2 by the corresponding region of Rx1 was sufficient to regain a wild-type resistance response to G. pallida in the roots. These data demonstrate that exchanging the recognition moiety in the LRR is sufficient to convert extreme virus resistance in the leaves into mild nematode resistance in the roots, and vice versa. In addition, we show that the CC-NB-ARC can operate independently of the recognition specificities defined by the LRR domain, either aboveground or belowground. These data show the versatility of NB-LRR genes to generate resistance to unrelated pathogens with completely different lifestyles and routes of invasion.

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Section: Discussionmentioning

confidence: 99%

Sequence Exchange between Homologous NB-LRR Genes Converts Virus Resistance into Nematode Resistance, and Vice Versa

et al. 2017

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“…Previously, site-directed and random mutagenesis approaches have been used to expand the recognition spectra of the NLRs Rx and R3a (Harris et al, 2013;Segretin et al, 2014;Giannakopoulou et al, 2015) against their respective cognate effectors, generating both allele-specific and 'trigger-happy', sensitized mutant variants of each NLR. Expansion of RPP1 specificity may have similarly occurred in various homologs, but through a combination of repeat expansion and sequence variation.…”

Section: New Phytologistmentioning

confidence: 99%

Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector

et al. 2016

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Nucleotide-binding leucine-rich repeat (NB-LRR, or NLR) receptors mediate pathogen recognition. The Arabidopsis thaliana NLR RPP1 recognizes the tandem WY-domain effector ATR1 from the oomycete Hyaloperonospora arabidopsidis through direct association with C-terminal LRRs. We isolated and characterized homologous NLR genes RPP1-EstA and RPP1-ZdrA from two Arabidopsis ecotypes, Estland (Est-1) and Zdarec (Zdr-1), responsible for recognizing a novel spectrum of ATR1 alleles. RPP1-EstA and -ZdrA encode nearly identical NLRs that are phylogenetically distinct from known immunity-activating RPP1 homologs and possess greatly expanded LRR domains. Site-directed mutagenesis and truncation analysis of ATR1 suggests that these homologs recognize a novel surface of the 2(nd) WY domain of ATR1, partially specified by a C-terminal region of the LRR domain. Synteny comparison with RPP1 loci involved in hybrid incompatibility suggests that these functions evolved independently. Closely related RPP1 homologs have diversified their recognition spectra through LRR expansion and sequence variation, allowing them to detect multiple surfaces of the same pathogen effector. Engineering NLR receptor specificity may require a similar combination of repeat expansion and tailored amino acid variation.

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“…The term is often used as a synonym for QDR, but it is important to note that there are several examples of strain-specific quantitative resistance loci (QRLs) (Poland et al, 2009). On the other hand, PRRs can confer a broad spectrum defense (Zipfel, 2014) and single R genes can also mediate broad-spectrum resistance (Xiao et al, 2001;Zhao et al, 2004;Narusaka et al, 2009) or can be engineered to achieve this type of resistance (Segretin et al, 2014;Giannakopoulou et al, 2015).…”

Section: Quantitative Resistance Enters Into the Gamementioning

confidence: 99%

Unraveling the molecules hidden in the gray shadows of quantitative disease resistance to pathogens

2018

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One of the most challenging questions in plant breeding and molecular plant pathology research is what are the genetic and molecular bases of quantitative disease resistance (QDR)?. The scarce knowledge of how this type of resistance works has hindered plant breeders to fully take advantage of it. To overcome these obstacles new methodologies for the study of quantitative traits have been developed. Approaches such as genetic mapping, identification of quantitative trait loci (QTL) and association mapping, including candidate gene approach and genome wide association studies, have been historically undertaken to dissect quantitative traits and therefore to study QDR. Additionally, great advances in quantitative phenotypic data collection have been provided to improve these analyses. Recently, genes associated to QDR have been cloned, leading to new hypothesis concerning the molecular bases of this type of resistance. In this review we present the more recent advances about QDR and corresponding application, which have allowed postulating new ideas that can help to construct new QDR models. Some of the hypotheses presented here as possible explanations for QDR are related to the expression level and alternative splicing of some defense-related genes expression, the action of "weak alleles" of R genes, the presence of allelic variants in genes involved in the defense response and a central role of kinases or pseudokinases. With the information recapitulated in this review it is possible to conclude that the conceptual distinction between qualitative and quantitative resistance may be questioned since both share important components. Keywords: breeding, complex traits, genome, gene expression, plant immunity, quantitative disease resistance (QDR), quantitative trait loci (QTL). RESUMENUna de las preguntas más desafiantes del fitomejoramiento y de la fitopatología molecular es ¿cuáles son las bases genéticas y moleculares de la resistencia cuantitativa a enfermedades?. El escaso conocimiento de cómo este tipo de resistencia funciona ha obstaculizado que los fitomejoradores la aprovecharlo plenamente. Para superar estos obstáculos se han desarrollado nuevas metodologías para el estudio de rasgos cuantitativos. Los enfoques como el mapeo genético, la identificación de loci de rasgos cuantitativos (QTL) y el mapeo por asociaciones, incluyendo el enfoque de genes candidatos y los estudios de asociación amplia del genoma, se han llevado a cabo históricamente para describir rasgos cuantitativos y por lo tanto para estudiar QDR. Además, se han proporcionado grandes avances en la obtención de datos fenotípicos cuantitativos para mejorar estos análisis. Recientemente, algunos genes asociados a QDR han sido clonados, lo que conduce a nuevas hipótesis sobre las bases moleculares de este tipo de resistencia. En esta revisión presentamos los avances más recientes sobre QDR y la correspondiente aplicación, que han permitido postular nuevas ideas que pueden ayudar a construir nuevos modelos. Algunas de las hipótesis presen...

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Tomato I2 immune receptor can be engineered to confer partial resistance to the oomycetePhytophthora infestansin addition to the fungusFusarium oxysporum

Cited by 20 publications

References 92 publications

Sequence Exchange between Homologous NB-LRR Genes Converts Virus Resistance into Nematode Resistance, and Vice Versa

Sequence Exchange between Homologous NB-LRR Genes Converts Virus Resistance into Nematode Resistance, and Vice Versa

Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector

Unraveling the molecules hidden in the gray shadows of quantitative disease resistance to pathogens

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