Silencing of Dicer‐like protein 2a restores the resistance phenotype in the rice mutant, sxi4 ( suppressor of Xa21‐mediated immunity 4 )

Liu, Furong; Chern, Mawsheng; Jain, Rashmi; Martin, Joel A.; Schakwitz, Wendy S.; Ronald, Pamela C.

doi:10.1111/tpj.15692

Title: Silencing of Dicer‐like protein 2a restores the resistance phenotype in the rice mutant, sxi4 ( suppressor of Xa21‐mediated immunity 4 )

Journal Article · Mon Feb 21 00:00:00 EST 2022 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.15692· OSTI ID:1996592

^[1]; Chern, Mawsheng ^[1]; Jain, Rashmi ^[1]; Martin, Joel A. ^[2]; Schakwitz, Wendy S. ^[2]; Ronald, Pamela C. ^[3]

Department of Plant Pathology and Genome Center University of California Davis CA 95616 USA
Department of Energy Joint Genome Institute Berkeley CA 94720 USA
Department of Plant Pathology and Genome Center University of California Davis CA 95616 USA, Feedstocks Division The Joint Bioenergy Institute Emeryville CA 94608 USA

SUMMARY The rice immune receptor XA21 confers resistance to Xanthomonas oryzae pv. oryzae ( Xoo ), and upon recognition of the RaxX21‐sY peptide produced by Xoo , XA21 activates the plant immune response. Here we screened 21 000 mutant plants expressing XA21 to identify components involved in this response, and reported here the identification of a rice mutant, sxi4, which is susceptible to Xoo. The sxi4 mutant carries a 32‐kb translocation from chromosome 3 onto chromosome 7 and displays an elevated level of DCL2a transcript, encoding a Dicer‐like protein . Silencing of DCL2a in the sxi4 genetic background restores resistance to Xoo . RaxX21‐sY peptide‐treated leaves of sxi4 retain the hallmarks of XA21‐mediated immune response. However, WRKY45‐1 , a known negative regulator of rice resistance to Xoo , is induced in the sxi4 mutant in response to RaxX21‐sY peptide treatment. A CRISPR knockout of a short interfering RNA (TE‐siRNA815) in the intron of WRKY45‐1 restores the resistance phenotype in sxi4 . These results suggest a model where DCL2a accumulation negatively regulates XA21‐mediated immunity by altering the processing of TE‐siRNA815.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐AC02‐05CH11231

OSTI ID:: 1996592

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Vol. 110 Journal Issue: 3; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (59)

Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9 Dong, Oliver Xiaoou; Yu, Shu; Jain, Rashmi Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14981-y	journal	March 2020
Plant and Animal Sensors of Conserved Microbial Signatures Ronald, P. C.; Beutler, B. Science, Vol. 330, Issue 6007 https://doi.org/10.1126/science.1189468	journal	November 2010
A novel DCL2-dependent miRNA pathway in tomato affects susceptibility to RNA viruses Wang, Zhengming; Hardcastle, Thomas J.; Canto Pastor, Alex Genes & Development, Vol. 32, Issue 17-18 https://doi.org/10.1101/gad.313601.118	journal	August 2018
OsWRKY62 is a Negative Regulator of Basal and Xa21-Mediated Defense against Xanthomonas oryzae pv. oryzae in Rice Peng, Ying; Bartley, Laura E.; Chen, Xuewei Molecular Plant, Vol. 1, Issue 3 https://doi.org/10.1093/mp/ssn024	journal	May 2008
Rapid and efficientAgrobacterium-mediated transformation in rice Toki, Seiichi Plant Molecular Biology Reporter, Vol. 15, Issue 1 https://doi.org/10.1007/BF02772109	journal	March 1997
Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor Luu, Dee Dee; Joe, Anna; Chen, Yan Proceedings of the National Academy of Sciences, Vol. 116, Issue 17 https://doi.org/10.1073/pnas.1818275116	journal	April 2019
Rice WRKY45 Plays a Crucial Role in Benzothiadiazole-Inducible Blast Resistance Shimono, Masaki; Sugano, Shoji; Nakayama, Akira The Plant Cell, Vol. 19, Issue 6 https://doi.org/10.1105/tpc.106.046250	journal	June 2007
Repression of microRNA biogenesis by silencing of OsDCL1 activates the basal resistance to Magnaporthe oryzae in rice Zhang, Dandan; Liu, Muxing; Tang, Mingzhi Plant Science, Vol. 237 https://doi.org/10.1016/j.plantsci.2015.05.002	journal	August 2015
The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium Pruitt, Rory N.; Schwessinger, Benjamin; Joe, Anna Science Advances, Vol. 1, Issue 6 https://doi.org/10.1126/sciadv.1500245	journal	July 2015
Small RNA on the Move Eckardt, Nancy A. The Plant Cell, Vol. 16, Issue 8 https://doi.org/10.1105/tpc.104.160810	journal	August 2004
Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements Barrett, Lucy W.; Fletcher, Sue; Wilton, Steve D. Cellular and Molecular Life Sciences, Vol. 69, Issue 21 https://doi.org/10.1007/s00018-012-0990-9	journal	April 2012
Plant 22-nt siRNAs mediate translational repression and stress adaptation Wu, Huihui; Li, Bosheng; Iwakawa, Hiro-oki Nature, Vol. 581, Issue 7806 https://doi.org/10.1038/s41586-020-2231-y	journal	April 2020
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 Song, W. -Y.; Wang, G. -L.; Chen, L. -L. Science, Vol. 270, Issue 5243 https://doi.org/10.1126/science.270.5243.1804	journal	December 1995
Transposon-Derived Non-coding RNAs and Their Function in Plants Cho, Jungnam Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00600	journal	May 2018
Knock-down of OsDCL2 in Rice Negatively Affects Maintenance of the Endogenous dsRNA Virus, Oryza sativa Endornavirus Urayama, Syunichi; Moriyama, Hiromitsu; Aoki, Nanako Plant and Cell Physiology, Vol. 51, Issue 1 https://doi.org/10.1093/pcp/pcp167	journal	November 2009
A rice transient assay system identifies a novel domain in NRR required for interaction with NH1/OsNPR1 and inhibition of NH1-mediated transcriptional activation Chern, Mawsheng; Bai, Wei; Sze-To, Wing Hoi Plant Methods, Vol. 8, Issue 1 https://doi.org/10.1186/1746-4811-8-6	journal	January 2012
A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors Boller, Thomas; Felix, Georg Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105346	journal	June 2009
Sensing of molecular patterns through cell surface immune receptors Ranf, Stefanie Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.011	journal	August 2017
Genome-Wide Prediction of Highly Specific Guide RNA Spacers for CRISPR–Cas9-Mediated Genome Editing in Model Plants and Major Crops Xie, Kabin; Zhang, Jianwei; Yang, Yinong Molecular Plant, Vol. 7, Issue 5 https://doi.org/10.1093/mp/ssu009	journal	May 2014
Ectopic expression of rice Xa21 overcomes developmentally controlled resistance to Xanthomonas oryzae pv. oryzae Park, Chang-Jin; Lee, Sang-Won; Chern, Mawsheng Plant Science, Vol. 179, Issue 5 https://doi.org/10.1016/j.plantsci.2010.07.008	journal	November 2010
Intron retention and 3′-UTR analysis of Arabidopsis Dicer-like 2 transcripts He, Qiongji; Peng, Jiejun; Yan, Fei Molecular Biology Reports, Vol. 39, Issue 3 https://doi.org/10.1007/s11033-011-1095-5	journal	June 2011
Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning Henderson, Ian R.; Zhang, Xiaoyu; Lu, Cheng Nature Genetics, Vol. 38, Issue 6 https://doi.org/10.1038/ng1804	journal	May 2006
A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling Navarro, L.; Dunoyer, P.; Jay, F. Science, Vol. 312, Issue 5772 https://doi.org/10.1126/science.1126088	journal	April 2006
Roles of DCL4 and DCL3b in rice phased small RNA biogenesis Song, Xianwei; Li, Pingchuan; Zhai, Jixian The Plant Journal, Vol. 69, Issue 3 https://doi.org/10.1111/j.1365-313X.2011.04805.x	journal	November 2011
Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA Polymerase gene families and their expression analysis during reproductive development and stress in rice Kapoor, Meenu; Arora, Rita; Lama, Tenisha BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-451	journal	January 2008
RNA silencing is required for Arabidopsis defence against Verticillium wilt disease Ellendorff, Ursula; Fradin, Emilie F.; de Jonge, Ronnie Journal of Experimental Botany, Vol. 60, Issue 2 https://doi.org/10.1093/jxb/ern306	journal	December 2008
Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis Jagadeeswaran, Guru; Saini, Ajay; Sunkar, Ramanjulu Planta, Vol. 229, Issue 4 https://doi.org/10.1007/s00425-009-0889-3	journal	January 2009
A computer-based systematic survey reveals the predominance of small inverted-repeat elements in wild-type rice genes. Bureau, T. E.; Ronald, P. C.; Wessler, S. R. Proceedings of the National Academy of Sciences, Vol. 93, Issue 16 https://doi.org/10.1073/pnas.93.16.8524	journal	August 1996
DICER-LIKE1: blind men and elephants in Arabidopsis development Schauer, Stephen E.; Jacobsen, Steven E.; Meinke, David W. Trends in Plant Science, Vol. 7, Issue 11 https://doi.org/10.1016/S1360-1385(02)02355-5	journal	November 2002
Agrobacterium- transformed rice plants expressing synthetic cryIA(b) and cryIA(c) genes are highly toxic to striped stem borer and yellow stem borer Cheng, Xiongying; Sardana, Ravinder; Kaplan, Harvey Proceedings of the National Academy of Sciences, Vol. 95, Issue 6 https://doi.org/10.1073/pnas.95.6.2767	journal	March 1998
Regulation of gene expression by alternative untranslated regions Hughes, Thomas A. Trends in Genetics, Vol. 22, Issue 3 https://doi.org/10.1016/j.tig.2006.01.001	journal	March 2006
Slice and Dice: DCL2 Mediates the Production of 22-Nucleotide siRNAs that Influence Trait Variation in Soybean Benoit, Matthias The Plant Cell, Vol. 32, Issue 12 https://doi.org/10.1105/tpc.20.00884	journal	October 2020
Genome-Wide Investigation of MicroRNAs and Their Targets in Response to Freezing Stress in Medicago sativa L., Based on High-Throughput Sequencing Shu, Yongjun; Liu, Ying; Li, Wei G3 Genes\|Genomes\|Genetics, Vol. 6, Issue 3 https://doi.org/10.1534/g3.115.025981	journal	March 2016
A novel class of bacteria-induced small RNAs in Arabidopsis Katiyar-Agarwal, Surekha; Gao, Shang; Vivian-Smith, Adam Genes & Development, Vol. 21, Issue 23 https://doi.org/10.1101/gad.1595107	journal	November 2007
A pathogen-inducible endogenous siRNA in plant immunity Katiyar-Agarwal, S.; Morgan, R.; Dahlbeck, D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 47 https://doi.org/10.1073/pnas.0608258103	journal	October 2006
Genome wide analysis of 3′ UTR sequence elements and proteins regulating mRNA stability during maternal-to-zygotic transition in zebrafish Vejnar, Charles E.; Abdel Messih, Mario; Takacs, Carter M. Genome Research, Vol. 29, Issue 7 https://doi.org/10.1101/gr.245159.118	journal	June 2019
Controlling plant architecture by manipulation of gibberellic acid signalling in petunia Liang, Yin-Chih; Reid, Michael S.; Jiang, Cai-Zhong Horticulture Research, Vol. 1, Issue 1 https://doi.org/10.1038/hortres.2014.61	journal	December 2014
The Sequences of 1504 Mutants in the Model Rice Variety Kitaake Facilitate Rapid Functional Genomic Studies Li, Guotian; Jain, Rashmi; Chern, Mawsheng The Plant Cell, Vol. 29, Issue 6 https://doi.org/10.1105/tpc.17.00154	journal	June 2017
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.199	journal	June 2007
The Role of WRKY Transcription Factors in Plant Immunity: Figure 1. Pandey, Shree P.; Somssich, Imre E. Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.138990	journal	May 2009
Molecular Identification and Analysis of Arsenite Stress-Responsive miRNAs in Rice Liu, Qingpo; Zhang, Hengmu Journal of Agricultural and Food Chemistry, Vol. 60, Issue 26 https://doi.org/10.1021/jf300724t	journal	June 2012
TOLL-like receptors linking innate and adaptive immune response Werling, Dirk; Jungi, Thomas W. Veterinary Immunology and Immunopathology, Vol. 91, Issue 1 https://doi.org/10.1016/S0165-2427(02)00228-3	journal	January 2003
Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen Zhang, Tao; Zhao, Yun-Long; Zhao, Jian-Hua Nature Plants, Vol. 2, Issue 10 https://doi.org/10.1038/nplants.2016.153	journal	September 2016
A Genetic Screen for Impaired Systemic RNAi Highlights the Crucial Role of DICER-LIKE 2 Taochy, Christelle; Gursanscky, Nial R.; Cao, Jiangling Plant Physiology, Vol. 175, Issue 3 https://doi.org/10.1104/pp.17.01181	journal	September 2017
Genome sequence of the model rice variety KitaakeX Jain, Rashmi; Jenkins, Jerry; Shu, Shengqiang BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6262-4	journal	November 2019
Suppression of the MicroRNA Pathway by Bacterial Effector Proteins Navarro, Lionel; Jay, Florence; Nomura, Kinya Science, Vol. 321, Issue 5891 https://doi.org/10.1126/science.1159505	journal	August 2008
OsWRKY80-OsWRKY4 Module as a Positive Regulatory Circuit in Rice Resistance Against Rhizoctonia solani Peng, Xixu; Wang, Haihua; Jang, Jyan-Chyun Rice, Vol. 9, Issue 1 https://doi.org/10.1186/s12284-016-0137-y	journal	November 2016
Activation of rice WRKY transcription factors: an army of stress fighting soldiers? Viana, Vívian Ebeling; Busanello, Carlos; da Maia, Luciano Carlos Current Opinion in Plant Biology, Vol. 45 https://doi.org/10.1016/j.pbi.2018.07.007	journal	October 2018
The role of the 3' untranslated region in post-transcriptional regulation of protein expression in mammalian cells. Matoulkova, Eva; Michalova, Eva; Vojtesek, Borivoj RNA Biology, Vol. 9, Issue 5 https://doi.org/10.4161/rna.20231	journal	May 2012
The Phylogenetically-Related Pattern Recognition Receptors EFR and XA21 Recruit Similar Immune Signaling Components in Monocots and Dicots Holton, Nicholas; Nekrasov, Vladimir; Ronald, Pamela C. PLOS Pathogens, Vol. 11, Issue 1 https://doi.org/10.1371/journal.ppat.1004602	journal	January 2015
Paladin, a tyrosine phosphatase-like protein, is required for XA21-mediated immunity in rice Chen, Tsung-Chi; Chern, Mawsheng; Steinwand, Michael Plant Communications, Vol. 2, Issue 4 https://doi.org/10.1016/j.xplc.2021.100215	journal	July 2021
Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1: NRR, a negative regulator of resistance Chern, Mawsheng; Canlas, Patrick E.; Fitzgerald, Heather A. The Plant Journal, Vol. 43, Issue 5 https://doi.org/10.1111/j.1365-313X.2005.02485.x	journal	August 2005
Dicer-like (DCL) proteins in plants Liu, Qingpo; Feng, Ying; Zhu, Zhujun Functional & Integrative Genomics, Vol. 9, Issue 3 https://doi.org/10.1007/s10142-009-0111-5	journal	February 2009
Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing Parent, Jean-Sébastien; Bouteiller, Nathalie; Elmayan, Taline The Plant Journal, Vol. 81, Issue 2 https://doi.org/10.1111/tpj.12720	journal	December 2014
A Pair of Allelic WRKY Genes Play Opposite Roles in Rice-Bacteria Interactions Tao, Zeng; Liu, Hongbo; Qiu, Deyun Plant Physiology, Vol. 151, Issue 2 https://doi.org/10.1104/pp.109.145623	journal	August 2009
A single transcription factor promotes both yield and immunity in rice Wang, Jing; Zhou, Lian; Shi, Hui Science, Vol. 361, Issue 6406 https://doi.org/10.1126/science.aat7675	journal	September 2018
Plant pattern-recognition receptors Zipfel, Cyril Trends in Immunology, Vol. 35, Issue 7 https://doi.org/10.1016/j.it.2014.05.004	journal	July 2014
Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage: Rapid report Giacomelli, Jorge I.; Weigel, Detlef; Chan, Raquel L. New Phytologist, Vol. 195, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04259.x	journal	July 2012
Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses Schwessinger, Benjamin; Bahar, Ofir; Thomas, Nicolas PLOS Pathogens, Vol. 11, Issue 3 https://doi.org/10.1371/journal.ppat.1004809	journal	March 2015

Similar Records

The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium

Journal Article · Fri Jul 24 00:00:00 EDT 2015 · Science Advances · OSTI ID:1996592

Pruitt, Rory N.; Schwessinger, Benjamin; Joe, Anna; +27 more

Mutation of the rice XA21 predicted nuclear localization sequence does not affect resistance to Xanthomonas oryzae pv. oryzae

Journal Article · Wed Oct 05 00:00:00 EDT 2016 · PeerJ · OSTI ID:1996592

Wei, Tong; Chen, Tsung-Chi; Ho, Yuen Ting; +1 more

Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor

Journal Article · Thu Apr 04 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1996592

Luu, Dee Dee; Joe, Anna; Chen, Yan; +10 more

Title: Silencing of Dicer‐like protein 2a restores the resistance phenotype in the rice mutant, sxi4 ( suppressor of Xa21‐mediated immunity 4 )

Citation Formats

References (59)

Similar Records

Related Subjects