Yinong Yang, Ph.D.

Areas of Interest

Molecular plant-pathogen interactions; CRISPR/Cas-enabled genome editing, precision breeding and disease diagnostics.

Program Interests

Rice is a model plant for monocots and one of the most important food crops for over half of the world's population. Rice blast (Magnaporthe oryzae) and sheath blight (Rhizoctonia solani) are the two most destructive diseases that negatively affect world-wide rice production. My research program aims to understand the molecular mechanism of pathogen virulence and host immunity during the rice-fungus interaction, and to translate basic knowledge into agricultural productivity via genome engineering and biotechnology. Our current research activities involve the following areas:

1. Pathogen virulence: Our recent studies focus on molecular, biochemical and functional characterization of the fungal effectors and their corresponding host protein targets. For example, the Nep1-like toxins and the zinc-finger effectors from Magnaporthe oryzae were found to interfere with host protein degradation or manipulate host chromatin configuration and gene expression, respectively. Using the yeast two-hybrid assay, in vitro protein binding, in vivo co-immunoprecipitation, bimolecular fluorescence complementation, and transgenic analyses, we have been elucidating the mode of action of the fungal effectors and characterizing the host target complexes for the underlying mechanism of pathogenesis and host susceptibility.

2. Host immunity: Our previous studies on rice defense signaling pathways reveal the distinctive roles of salicylic acid (SA), jasmonic acid (JA), ethylene (ET) and abscisic acid (ABA) in mediating rice resistance to different pathogens. The cross-talk between jasmonate and gibberellin pathways was shown to play an important role in rice growth and defense response. Using a combination of molecular, biochemical, physiological and functional genomic approaches, a number of stress-responsive rice mitogen-activated protein kinases (MAPKs) were found to modulate hormone signaling and mediate cross-talks between disease resistance and abiotic stress tolerance. To gain novel insights into the rice protein kinase signal transduction, we have been characterizing protein substrates of the stress-responsive MAPKs and calcium-dependent protein kinases (CDPKs) and determining the role of the CDPK-MAPK cross-talk in rice biotic and abiotic stress tolerance.

3. Translational biotechnology: Based on the mechanistic studies of pathogen virulence and host immunity, we have generated genetically modified rice crop with enhanced disease resistance and/or abiotic stress tolerance. Recently, the bacterial CRISPR-Cas9 system has been adapted and improved in my laboratory for plant genome editing and precision breeding of transgene-free, genetically improved crops such as rice, potato and mushroom. A series of plasmid vector systems (see www.addgene.org/Yinong_Yang/) and bioinformatic tools (www.genome.arizona.edu/crispr) have been developed by our group to facilitate the application of CRISPR-Cas9 editing technology in plant genome engineering and crop improvement.

Teaching

PPEM 417W Mechanisms of Bacterial Pathogenesis in Plants (3 credits, 100%, every other spring),

PPATH 597 Genome Editing (3 credits, 100%, every fall)

PPATH 533 Molecular Genetics of Plant-pathogen Interaction (3 credits, 50%, every other fall)

PLBIO 513 Plant Communication and Growth Regulation (4 credits, team-taught, every spring)

PLBIO 516 Modern Techniques and Concepts in Plant Molecular Biology (2 credits, 50%, every spring)

Recent Awards and Honors

Fellow, American Phytopathological Society (2023)

Fellow, American Association for the Advancement of Science (2022)

Research Innovator Award, College of Agricultural Sciences, Penn State University (2019)

Recent Publications

Google Scholar (https://scholar.google.com/citations?user=Rgvd2Q8AAAAJ&hl=en)

Li, H., Zhang, Y., Wu, C., Bi, J., Chen, Y., Jiang, C., Cui, M., Chen, Y., Hou, X., Yuan, M., Xiong, L., Yang, Y.* and Xie, K.* 2022. Fine-tuning OsCPK18/OsCPK4 activity via genome editing of phosphorylation motif improves rice yield and immunity. Plant Biotechnol Journal. https://doi.org/10.1111/pbi.13905 (*co-corresponding author)

Wheatley, M. S., Qin Wang, Q., Wei, W., Bottner-Parker, K., Zhao, Y., and Yang, Y. 2022. Cas12a-based diagnostics for potato purple top disease complex associated with infection by ‘Candidatus Phytoplasma trifolii’-related strains. Plant Disease 106: 2039-2045.

Molla K. A.*, Shih, J.*, Wheatley, M. S., and Yang, Y. 2022. Predictable NHEJ insertion and assessment of HDR editing strategies in plants. Front. Genome Editing 4: 825236. doi:10.3389/fgeed. (*co-first author)

Chen, K., Ke, R., Du, M., Yi, Y., Chen, Y., Wang, X., Yao, L., Liu, H., Hou, X., Xiong, L., Yang, Y., and Xie, K. 2022. A FLASH pipeline for arrayed CRISPR library construction and the gene function discovery of rice receptor-like kinases. Molecular Plant 15:243-257.

Zhang, Y. M., Yang, Y., and Xie, K. 2021. CRISPR-Cas12a-based DNA detection for fast pathogen diagnosis and GMO test in plants. In: Islam M.T., Molla K.A. (eds) CRISPR-Cas Methods. Springer Protocols Handbooks. Humana, New York, NY. (doi.org/10.1007/978-1-0716-1657-4_15).

Reeger, J. E., Wheatley, M., Yang, Y., and Brown, K. M. 2021. Targeted mutation of transcription factor genes alters metaxylem vessel size and number in rice roots. Plant Direct 5:e00328 (doi.org/10.1002/pld3.328).

Wheatley, M., Duan, Y.-P., and Yang, Y. 2021. Highly sensitive and rapid detection of citrus Huanglongbing pathogen (Candidatus Liberibacter asiaticus) using Cas12a-based methods. Phytopathology 111:2375-2382.

Li, H., Wu, C., Du, M., Chen, Y., Hou, X., Yang, Y., and Xie, K. 2021. A versatile nanoluciferase toolkit and optimized in-gel detection method for protein analysis in plants. Mol Breeding 41:13 (doi.org/10.1007/s11032-021-01210-7)

Wheatley, M. and Yang, Y. 2021. Versatile applications of the CRISPR/Cas toolkit in plant pathology and disease management. Phytopathology 111:1080-1090.

Yang, X., Medford, J. I., Markel, K., Shih, P. M., De Paoli, H. C., Trinh, C. T., McCormick, A. J., Ployet, R., Hussey, S. G., Myburg, A. A., Jensen, P. E., Hassan, M. M., Zhang, J., Muchero, W., Kalluri, U. C., Yin, H., Zhuo, R., Abraham, P. E., Chen, J.-G., Weston, D. J., Yang, Y., Liu, D., Li, Y., Labbe, J., Yang, B., Lee, J. H., Cottingham, R. W., Martin, S., Lu, M., Tschaplinski, T. J., Yuan, G., Lu, H., Ranjan, P., Mitchell, J. C., Wullschleger, S. D., & Tuskan, G. A. 2020. Plant biosystems design research roadmap 1.0. BioDesign Research (doi.org/10.34133/2020/8051764)

Zeng, Z., Han, N., Liu, C., Buerte, B., Zhou, C., Chen, J., Wang, M., Zhang, Y., Tang, Y., Zhu, M., Wang, J., Yang, Y., and Bian, H. 2020. Functional dissection of HGGT and HPT in barley vitamin E biosynthesis via CRISPR/Cas9-enabled genome editing. Annals of Botany (doi.org/10.1093/aob/mcaa115)

Molla, K.A. and Yang, Y. 2020. CRISPR-Cas-mediated single base editing at more than one locus in rice genome. In: Islam M., Bhowmik P., Molla K. (eds) CRISPR-Cas Methods. Springer Protocols Handbooks. Humana, New York, NY. (doi.org/10.1007/978-1-0716-0616-2_4)

Hsieh-Feng, V. and Yang, Y. 2020. Efficient expression of multiple guide RNAs for CRISPR/Cas genome editing. aBIOTECH 1:123-134. (doi.org/10.1007/s42994-019-00014-w)

Molla, K.A., Shih, J., and Yang, Y. 2020. Single-nucleotide editing for zebra3 and wsl5 phenotypes in rice using CRISPR/Cas9-mediated adenine base editors. aBIOTECH 1:106-118. (doi.org/10.1007/s42994-020-00018-x)

Molla, K.A. and Yang, Y. 2020. Predicting CRISPR/Cas9-induced mutation for precise genome editing. Trends in Biotechnology 38:136-141. (doi.org/10.1016/j.tibtech.2019.08.002)

Osdaghi, E., Martins, S.J., Ramos-Sepulveda, L., Vieira, F.R., Pecchia, J.A., Beyer, D.M., Bell, T.H., Yang, Y., Hockett, K.L., and Bull, C.T. 2019. 100 years since Tolaas: Bacterial blotch of mushrooms in the 21^st century. Plant Disease 103:2714-2732.

Xie, S., Wang, Y., Wei, W., Li, C., Liu, Y., Qu, J., Meng, Q., Lin, Y., Yin, W., Yang,Y., and Luo, C. 2019. The Bax inhibitor UvBI-1, a negative regulator of mycelial growth and conidiation, mediates stress response and is critical for pathogenicity of the rice false smut fungus Ustilaginoidea virens. Current Genetics 65:1185-1197.

Molla, K.A. and Yang, Y. 2019. CRISPR/Cas-mediated base editing: Technical considerations and practical applications. Trends in Biotechnology 37:1121-1142.

Minkenberg, B., Zhang, J., Xie, K., and Yang, Y. 2019. CRISPR-PLANT v2: An online resource for highly specific guide RNA spacers based on improved off-target analysis. Plant Biotechnology J. 17:5-8.

Xie, K. and Yang, Y. 2019. A multiplexed CRISPR-Cas9 editing system based on the endogenous tRNA processing. Methods in Molecular Biology 1917:63-73.

Zhao, H., Wang, X., Jia, Y., Minkenberg, B., Wheatley, M., Fan, J., Jia, M. H., Famoso, A., Edwards, J.D., Wamishe, Y., Valent, B., Wang, G.-L., Yang, Y. 2018. The rice blast resistance gene Ptr encodes a novel protein and confers broad spectrum disease resistance. Nature Communications 9:2039.

Minkenberg, B., Wheatley, M., Yang, Y. 2017. CRISPR/Cas9-enabled multiplex genome editing and its application. In Donald P. Weeks and Bing Yang, editors: Gene Editing in Plants, Vol 149, PMBTS, UK: Academic Press, pp. 111-132.

Minkenberg, B., Xie, K., and Yang, Y. 2017. Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinase genes. Plant J. 89:636-648.

Dong, F., Xie, K., Chen, Y., Yang, Y.*, Mao, Y.* 2017. Polycistronic tRNA and CRISPR guide-RNA enables highly efficient multiplexed genome engineering in human cells. Biochem Biophys Res Commun. 482:889-895. (*co-corresponding author)

Lu, W., Deng, M., Guo, F., Wang, M., Zeng, Z, Han, N., Yang, Y., Zhu, M., Bian, H. 2016. Suppression of OsVPE3 enhances salt tolerance by attenuating vacuole rupture during programmed cell death and affects stomata development in rice. Rice 9:65. 

Helliwell, E.E., Wang, Q., and Yang, Y. 2016. Ethylene biosynthesis and signaling is required for rice immune response and basal resistance against Magnaporthe oryzae infection. Mol. Plant-Microbe Interact. 29:831-843.

Guo, F., Han, N., Xie, Y., Fang, K., Yang, Y., Zhu, M., Wang, J., and Bian, H. 2016. The miR393a/target module regulates seed germination and seedling establishment under submergence in rice (Oryza sativa L.). Plant Cell Environment 39:2288-2302.

Xie, K., Minkenberg, B., and Yang, Y. 2015. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA processing system. Proc. Natl. Acad. Sci. USA 112:3570-3575.

Xie, K., Minkenberg, B., and Yang, Y. 2014. Targeted gene mutation in rice using a CRISPR-Cas9 system. Bio-Protocol 4:e1225.

Xie, K., Chen, J., Wang, Q., and Yang, Y. 2014. Direct phosphorylation and activation of a mitogen-activated protein kinase by a calcium-dependent protein kinase in rice. Plant Cell 26:3077-3089.

Bai, Y., Han, N., Wu, J., Yang, Y., Wang, J., Zhu, M., and Bian, H. 2014. A transient gene expression system using barley protoplasts to evaluate microRNAs for post-transcriptional regulation of their target genes. Plant Cell Tiss Organ Cult 119: 211-219.

Wang, M., Yang, Y., and Bian, H. 2014. New genome targeting modification technology using a CRISPR-Cas system. Chinese J. Biochem Mol. Biol. 30:426-433.

Xie, K., Zhang, J. and Yang, Y. 2014. Genome-wide prediction of highly specific guide RNA spacers for the CRISPR-Cas9 mediated genome editing in model plants and major crops. Mol. Plant 7:923-926.

Xie, K. and Yang, Y. 2013. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant 6:1975-1983. (Cover story)

Yang, D.L., Yang, Y., and He, Z. 2013. Roles of plant hormones and their interplay in rice immunity. Mol. Plant 6:675-685.

Helliwell, E. H., Wang, Q., and Yang, Y. 2013. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Maganporthe oryzae and Rhizhoctonia solani. Plant Biotechnology J. 11:33-42.

Yang, Y. (Editor) 2013. Methods in Molecular Biology: Rice Protocols. Humana Press Inc., Springer Science + Business Media.

Jia, Y., Liu, G., Park, D.-S., Correa-Vectoria, F., and Yang, Y. 2013. Inoculation and scoring methods for rice sheath blight disease. Methods in Molecular Biology: Rice Protocols 956:257-268.

Helliwell, E. H. and Yang, Y. 2013. Molecular strategies to improve rice disease resistance. Methods in Molecular Biology: Rice Protocols 956:285-309.

Liu, W., Xie, K., and Yang, Y. 2013. Genomic and bioinformatic resources for rice research. Methods in Molecular Biology: Rice Protocols 956:327-332.

Bian, H., Xie Y., Guo, F., Han, N., Ma, S., Zeng, Z., Wang, J., Yang, Y., and Zhu, M. 2012. Distinctive expression patterns and roles of the miRNA393⁄TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytologist 196:149–161.

Yang, D.-L., Yao, J., Mei, C.-S., Tong, X.-H., Zeng, L.-J., Li, Q., Xiao, L-T., Sun, T.-P., Li, F., Deng, X.-W., Lee, C.-M., Thomashow, M., Yang, Y.*, He, Z.-H.*, and He, S. Y.* 2012. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc. Natl. Acad. Sci. USA 109:7152-7153. (*co-corresponding author)

Patents

Yang, Y. and Xie, K. 2023. Methods and compositions for RNA-guided multiplex genome editing and other RNA technologies. (US Patent 11,702,667)

Yang, Y., Wheatley, M. S. and Wang, Q. 2023. Methods and compositions for supersensitive and specific detection of citrus greening and phytoplasma pathogens. (US Patent Application)

Yang, Y. and Xie, K. 2019. Methods and compositions for RNA-guided multiplex genome editing and other RNA technologies. (US Patent 10,308,947; International patents issued in Canada and China, and pending in Brazil and European Union)

Yang, Y. and Xie, K. 2014. Gene targeting and genetic modification of plants via RNA-guided genome editing. PCT WO2014/194190A1 and US2015/0067922A1 (US Patent Application No. 14/291,605; PCT/US2014/040220)

Yang, Y. and Xiong, L. 2008. Mitogen-activated protein kinase and method of use to enhance biotic and abiotic stress tolerance in plants. (US. Patent 7,345,219)

Felton, G., Yang, Y. and Wang, Q. 2004. Apparatus and method for increasing insect resistance in transgenic plants. (U.S. Patent Application: 20040259080).

Klessig, D.F. and Yang, Y. 1999. Novel genes associated with enhanced disease resistance in plants.  (U.S. Patent 5,939,601)