Research Faculty #74
Full Professor (Departments of Botany, UBC)
B.Sc. Genetics (1989), Fudan Univ.;
Ph.D. Biochemistry and Molecular Biology (1995), Oklahoma State Univ.;
Postdoctoral Fellow (1995-98) University of North Carolina, Chapel Hill;
Postdoctoral Fellow (1998-99) Duke University;
Assistant and Associate Investigator (2005-2011), NIBS, Beijing
We are interested in how local resistance and systemic acquired resistance are regulated in plants.
Sensing and defending against microbial infections is essential to the survival of multicellular organisms. Recognition of PAMPs (pathogen-associated molecular patterns) or effector proteins from pathogens by plant immune receptors leads to activation of downstream signaling cascades and plant resistance to pathogens at the infection site. Activation of local defense further induces a secondary immune response in the distal parts of plants termed systemic acquired resistance (SAR). Our research is focused on the following two areas.
1. Signal Transduction Pathways downstream of Plant Immune Receptors
In plants, there are three main classes of immune receptors. The largest class encodes intracellular NB-LRR type Resistance (R) proteins. The other two classes belong to the transmembrane receptor-like kinase (RLK) and receptor-like protein (RLP) families. We have obtained a series of mutants such as snc2-1D, snc4-1D, bir1-1, and mkk1 mkk2 that constitutively activate immunity mediated by these three classes of immune receptors. To identify components downstream of the receptors, suppressor screens have been performed in these mutant backgrounds. Cloning the suppressor genes and analyzing biochemical functions of proteins encoded by them will help us build the signal transduction network of plant immunity.
2. Systemic Acquired Resistance
Genetic analysis of SAR has been hampered by lack of good assays for studying SAR in Arabidopsis. We developed an SAR assay in which we inoculated the local leaves with the bacterial pathogen P.s.m. ES4326 and assayed the distal leaves for induced resistance against the virulent oomycete pathogen H. a. Noco2. This new assay is sensitive and reproducible and it can be used to screen a large number of plants. Using this high-throughput assay, we have carried out both forward and reverse genetic screens to look for mutants with defects in SAR. Identification and characterization of genes required for SAR will help us better understand the underlining mechanisms of SAR.
Tian, H., Chen, S., Wu, Z., Ao, K., Yaghmaiean, H., Sun, T., Huang, W., Xu, F., Zhang, Y., Wang, S., Li, X.**, and Zhang, Y.** (2021). Activation of TIR signaling boosts pattern-triggered immunity. Nature, https://doi.org/10.1038/s41586-021-03987-1.
Peng, Y., Yang, J., Li, X. and Zhang, Y. (2021) Salicylic acid: Biosynthesis and Signaling. Annual Review in Plant Biology, 72:761-791.
Mohnike, L., Rekhter, D., Huang, W., Feussner, K., Tian, H., Herrfurth, C., Zhang, Y.*(* Co-corresponding author) and Feussner, I*. (2021) The glycosyltransferase UGT76B1 modulates N-hydroxy-pipecolic acid homeostasis and plant Immunity. Plant Cell, 33(3), 735-749.
Liu, Y., Sun, T., Sun, Y., Zhang, Y., Radojičić, A., Ding, Y., Tian, H., Huang, X., Lan, J., Chen, S. and Orduna, A.R., Zhang, K., Jetter, R., Li, X. and Zhang, Y. (2020) Diverse Roles of the Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Plant Immunity. Plant Cell, 32(12), 4002-4016.
Sun, T. and Zhang, Y. (2020) Short and long-distance signaling in plant defense. Plant Journal, https://doi.org/10.1111/tpj.15068.
Liu, Y., Zhong, X., Zhang, Z., Lan, J., Huang, X., Tian, H., Li, X. and Zhang, Y. * (2020) Receptor-like kinases MDS1 and MDS2 promote SUMM2-mediated immunity. Journal of Integrative Plant Biology, 63 (2):277-282.
Zhou, J.* and Zhang, Y.* (* Co-corresponding author) (2020) Plant immunity: danger perception and signaling. Cell, 181(5): 978-989.
Nitta, Y., Qiu, Y., Yaghmaiean, H., Zhang, Q., Huang, J., Adams, K. and Zhang, Y. (2020) MEKK2 inhibits activation of MAP kinases in Arabidopsis. Plant Journal, 103(2):705-714.
Huang, W., Wang, Y., Li, X. and Zhang, Y. (2020) Biosynthesis and regulation of salicylic acid and N-hydroxypipecolic acid in plant immunity. Molecular Plant, 13 (1): 31-41.
Sun, T., Huang, J., Xu, Y., Verma, V., Jing, B., Sun, Y., Ordunac, A., Tian, H., Huang, X., Xia, S., Schaferc, L., Jetter, R., Zhang, Y.* (* Co-corresponding author) and Li, X.* (2019) Redundant CAMTA transcription factors negatively regulate the biosynthesis of salicylic acid and N-hydroxypipecolic acid by modulating the expression of SARD1 and CBP60g. Molecular Plant, 13: 144-156.
Rekhter, D., Lüdke, D., Ding, Y., Feussner, K., Zienkiewicz, K., Lipka, V., Wiermer, M.*, Zhang, Y.* (* Co-corresponding author) and Feussner, I*. (2019) Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science, 365, 498-502.
Zhang, Y. and Li, X. (2019) Salicylic acid: Biosynthesis, perception and contributions to plant immunity. Current Opinion in Plant Biology, 50:1-8.
Lian, K., Gao, F., Sun, T., Wersch, R., Ao, K., Kong, Q., Nitta, Y., Wu, W., Krysan, P., and Zhang, Y. 2018. Arabidopsis MKK6 functions in two parallel MAP kinase cascades in immune signaling. Plant Physiology, 178, 1284-1295.
Ding, Y., Sun, T., Ao, K., Peng, Y., Zhang, Y., Li, X. and Zhang, Y. 2018. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell, 173, 1454–1467.
Sun, T., Nitta, Y., Zhang, Q., Wu, D., Tian, H., Lee, J.S. and Zhang, Y. 2018. Antagonistic interactions between two MAP kinase cascades in plant development and immune signaling. EMBO Reports, e45324.
Sun, T., Busta, L., Zhang, Q., Ding, P., Jetter, R. and Zhang, Y. 2018. TGACG-BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g). New Phytologist, 217: 344–354. doi:10.1111/nph.14780.
Ma C., Liu Y., Bai B., Han Z, Tang J., Zhang H., Yaghmaiean H., Zhang Y. (Co-corresponding author) and Chai J. 2017. Structural basis for BIR1-mediated negative regulation of plant immunity. Cell Research, 27, 1521–1524.
Ding, P., Rekhter, D., Ding, Y., Feussner, K., Busta, L., Haroth, S., Xu, S., Li, X., Jetter, R., Feussner, I. and Zhang, Y. 2016. Characterization of a pipecolic pcid biosynthesis pathway required for systemic acquired resistance. Plant Cell, 28: 2603–2615.
Zhang Z., Liu Y., Huang H., Gao M., Wu D., Kong Q. and Zhang Y. 2016. Sensing the disruption of a MAP kinase cascade by an NLR protein through a MAP kinase substrate. EMBO Reports, pii: e201642704.
Liu, Y., Huang, X., Li, M., He, P. and Zhang, Y. 2016. Loss-of-function of Arabidopsis receptor-like kinase BIR1 activates cell death and defense responses mediated by BAK1 and SOBIR1. New Phytologist, doi: 10.1111/nph.14072. [Epub ahead of print].
Kong, Q., Sun, T., Qu, N., Ma, J., Li, M., Cheng, Y.-t., Zhang, Q., Wu, D., Zhang, Z. and Zhang, Y. 2016. Two redundant receptor-like cytoplasmic kinases function downstream of pattern recognition receptors to regulate activation of SA biosynthesis in Arabidopsis. Plant Physiology, 171(2): 1344-1354.
Liang, X., Ding, P., Lian, K., Wang, J., Ma, M., Li, L., Li, L., Li, M., Zhang, X., Chen, S., Zhang, Y. (Co-corresponding author) and Zhou, J. 2016. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. eLife 5, e13568.
Sun T., Zhang Y., Li Y., Zhang Q., Ding Y. and Zhang, Y. 2015. ChIP-seq analysis reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nature Communications, 6:10159.
Li, X., Kapos, P. and Zhang, Y. (2015). NLRs in plants. Current Opinion in Immunology, 32, 114-121.
Sun, T., Zhang, Q., Gao, M. and Zhang, Y. 2014. Regulation of SOBIR1 accumulation and activation of defense responses in bir1-1 by specific components of ER quality control. Plant Journal, 77(5):748-56.
Zhang, Z., Liu, Y., Ding, P., Li, Y., Kong, Q. and Zhang, Y.2014. Splicing of Receptor-like kinase-encoding SNC4 and CERK1 is regulated by two conserved splicing factors that are required for plant immunity. Molecular Plant, 7(12):1766-75.
Liu, J., Ding, P., Sun, T., Nitta, Y., Dong, O., Huang, X., Yang, W., Li, X., Botella, J. and Zhang, Y. 2013. Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiology, 161(4), 2146-2158.
Zhang Z., Wu Y., Gao M., Zhang J., Kong Q., Liu Y., Ba H., Zhou J.M. and Zhang Y. 2012. Disruption of a PAMP-induced MAP Kinase Cascade Activates Plant Immunity Mediated by an NB-LRR Protein. Cell Host & Microbe,11(3):253-63.
Kong, Q., Qu, N., Gao, M., Zhang, Z., Ding, X., Yang, F., Li, Y., Dong, X., Chen, S., Li, X., and Zhang, Y. 2012. The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a MAP kinase kinase kinase. Plant Cell, 24(5):2225-36.
Yang, Y., Zhang, Y., Ding, P., Johnson, K., Li, X., and Zhang Y. 2012. The ankyrin-repeat transmembrane protein BDA1 functions downstream of the receptor-like protein SNC2 to regulate plant immunity. Plant Physiology, 159(4):1857-65.
Xu, S., Zhang, Z., Jing, B., Gannon, P., Ding, J., Xu, F., Li, X. and Zhang, Y. 2011. Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLoS Genetics, 7(6): e1002159.
Jing, B., Xu, S., Xu, M., Li, Y., Li, S., Ding, J. and Zhang, Y. 2011. Brush and Spray: A high throughput systemic acquired resistance assay suitable for large-scale genetic screening. Plant Physiology, 157(3):973-80.
Germain, H., Qu, N., Cheng, Y.T., Lee, E.K., Huang, H., Dong, O.X., Gannon, P., Huang, S., Ding, P., Li, Y., Sack, F. and Zhang, Y. (co-corresponding), and Li X. 2010. MOS11: a new component in the mRNA export pathway. PLoS Genetics, 6(12): e1001250.
Zhang, Y., Xu, S., Ding, P., Wang, D., Cheng, Y., He, J., Gao, M., Xu, F., Li, Y., Zhu, Z., Li, X., and Zhang, Y. 2010. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. PNAS (track II).107(42):18220-18225.
Li, Y., Li, S., Bi, D., Cheng, Y., Li, X. and Zhang, Y. 2010. SRFR1 negatively regulates plant NB-LRR Resistance protein accumulation to prevent autoimmunity. PLoS Pathogens, 6 (9), e1001111.
Zhang, Y., Yang, Y., Fang, B., Gannon, P., Ding, P., Li, X., and Zhang, Y. 2010. snc2-1D activates receptor like protein-mediated immunity transduced through WRKY70. Plant Cell, 22(9):3153-3163.
Zhu, Z., Xu, F., Zhang, Y., Cheng, Y., Wiermer, M., Li, X., and Zhang, Y. 2010. Arabidopsis Resistance protein SNC1 activates immune responses through association with a transcriptional co-repressor. PNAS (track II). 107(31):13960-13965.
Bi, D., Cheng, Y., Li, X., and Zhang, Y. 2010. Activation of plant immune responses by a gain-of-function mutation in an atypical receptor-like kinase. Plant Physiology, 153(4):1771-1779.
Li, Y., Tessaro, M., Li, X., and Zhang, Y. 2010. Regulation of the expression of plant Resistance gene SNC1 by a Protein with a Conserved BAT2 Domain. Plant Physiology, 153(3):1425-1434.
Gao, M., Wang, X., Wang, D., Xu, F., Ding, X., Zhang, Z., Bi, D., Cheng, Y.T., Chen, S., Li, X., and Zhang, Y. 2009. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host & Microbe 6:34-44.
Gao, M., Liu, J., Bi, D., Zhang, Z., Cheng, F., Chen, S., and Zhang, Y. 2008. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Research 18:1190-1198. (Cover story)