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Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses

View ORCID ProfileBenjamin Schwessinger, View ORCID ProfileOfir Bahar, Nicolas Thomas, View ORCID ProfileNicolas Holton, View ORCID ProfileVladimir Nekrasov, View ORCID ProfileDeling Ruan, View ORCID ProfilePatrick E. Canlas, View ORCID ProfileArsalan Daudi, View ORCID ProfileChristopher J. Petzold, View ORCID ProfileVasanth R Singan, View ORCID ProfileRita Kuo, View ORCID ProfileMansi Chovatia, View ORCID ProfileChristopher Daum, View ORCID ProfileJoshua L. Heazlewood, View ORCID ProfileCyril Zipfel, View ORCID ProfilePamela C. Ronald
doi: https://doi.org/10.1101/006155
Benjamin Schwessinger
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
2Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, 94720, USA
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Ofir Bahar
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
5Current address: Department of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, P. O. Box 155, Bet Dagan 5025001, Israel
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Nicolas Thomas
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
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Nicolas Holton
3The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK
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Vladimir Nekrasov
3The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK
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  • ORCID record for Vladimir Nekrasov
Deling Ruan
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
2Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, 94720, USA
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Patrick E. Canlas
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
2Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, 94720, USA
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Arsalan Daudi
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
6Current address: bio-protocol, P.O. Box 61231, Palo Alto, California 94306, USA
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Christopher J. Petzold
2Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, 94720, USA
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Vasanth R Singan
4Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California, 94598, USA
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Rita Kuo
4Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California, 94598, USA
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Mansi Chovatia
4Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California, 94598, USA
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Christopher Daum
4Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California, 94598, USA
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Joshua L. Heazlewood
2Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, 94720, USA
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Cyril Zipfel
3The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK
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Pamela C. Ronald
1Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
2Joint BioEnergy Institute and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, 94720, USA
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  • For correspondence: pcronald@ucdavis.edu
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Abstract

Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components.

Author Summary Plants possess multi-layered immune recognition systems. Early in the infection process, plants use receptor proteins to recognize pathogen molecules. Some of these receptors are present in only in a subset of plant species. Transfer of these taxonomically restricted immune receptors between plant species by genetic engineering is a promising approach for boosting the plant immune system. Here we show the successful transfer of an immune receptor from a species in the mustard family, called EFR, to rice. Rice plants expressing EFR are able to sense the bacterial ligand of EFR and elicit an immune response. We show that the EFR receptor is able to use components of the rice immune signaling pathway for its function. Under laboratory conditions, this leads to an enhanced resistance response to two weakly virulent isolates of an economically important bacterial disease of rice.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted March 10, 2015.
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Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses
Benjamin Schwessinger, Ofir Bahar, Nicolas Thomas, Nicolas Holton, Vladimir Nekrasov, Deling Ruan, Patrick E. Canlas, Arsalan Daudi, Christopher J. Petzold, Vasanth R Singan, Rita Kuo, Mansi Chovatia, Christopher Daum, Joshua L. Heazlewood, Cyril Zipfel, Pamela C. Ronald
bioRxiv 006155; doi: https://doi.org/10.1101/006155
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Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses
Benjamin Schwessinger, Ofir Bahar, Nicolas Thomas, Nicolas Holton, Vladimir Nekrasov, Deling Ruan, Patrick E. Canlas, Arsalan Daudi, Christopher J. Petzold, Vasanth R Singan, Rita Kuo, Mansi Chovatia, Christopher Daum, Joshua L. Heazlewood, Cyril Zipfel, Pamela C. Ronald
bioRxiv 006155; doi: https://doi.org/10.1101/006155

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