Plants have developed the sophisticated innate immune system to defend pathogen attacks. Our primary research interest is to elucidate the activation and signaling mechanisms of host immunity upon pathogen infections with an integrated genetic, biochemical, and cellular approach using Arabidopsis as a tractable model system. Plant immunity is inextricably linked with plant development and environmental stresses. We are trying to understand the signaling crosstalk that orchestrates plant responses to different extrinsic and intrinsic signals. Ultimately, knowledge gained from studying model plants will be applied to improve crop plants for stress resilience.

Plant immune signaling

Plants have evolved two tiers of immune receptors to detect infections: cell surface-resident pattern recognition receptors (PRRs) sensing microbial signatures and intracellular nucleotide-binding domain leucine-rich repeat (NLR) proteins recognizing pathogen effectors. We have developed a sensitive genetic screen to identify Arabidopsis Genes Governing Immune gene Expression (AGGIEs) that regulate plant PRR- and/or NLR-mediated immunity. Genetic and biochemical analyses of AGGIE1 have delineated an unconventional phosphorylation circuit in which the canonical MAP kinase cascade downstream of multiple PRRs directly phosphorylates cyclin-dependent kinases to induce phosphorylation dynamics of RNA polymerase II to orchestrate immune gene transcription. Analysis of AGGIE2 has revealed an essential, but less characterized posttranslational modification protein poly(ADP-ribosyl)ation in host immune gene activation and immunity. Analysis of AGGIE101 has revealed a molecular link between PRR and NLR protein complexes through cell surface-resident malectin-like domain receptor-like kinases.

B. Feng, C. Liu, M. V. V. Oliveira, A. C. Intorne, B. Li, K. Babilonia, G. A. S. Filho, L. Shan, P. He, Protein poly(ADP-ribosyl)ation regulates Arabidopsis immune gene expression and defense responses. PLoS Genetics 11 (2015).

F. Li, C. Cheng, F. Cui, M. V. V. Oliveira, X. Yu, X. Meng, A. C. Intorne, K. Babilonia, M. Li, X. Chen, X. Ma, S. Xiao, Y. Zeng, Z. Fei, R. Metz, C. D. Johnson, H. Koiwa, W. Sun, Z. Li, G. A. S. Filho, L. Shan, P. He, Modulation of RNA polymerase II phosphorylation downstream of pathogen perception orchestrates plant immunity. Cell Host Microbe 16, 748–758 (2014).

Plant cell death regulation

Immune regulators are often important in maintaining cellular homeostasis. Defects or over-activation of defense could lead to cell death. To understand the mechanisms underlying immunity-related cell death, we have developed an innovative RNAi-based screen for suppressors of cell death caused by immune regulators are often important in maintaining cellular homeostasis. Defects or over-activation of defense could induce autoimmunity, ultimately leading to cell death. To understand the mechanisms underlying immunity-related cell death, we have developed various RNAi-based screens for suppressors of cell death caused by mutations in key immune regulators. This unbiased and highly efficient screen is based on an easy experimental procedure of Agrobacterium-mediated virus-induced gene silencing (VIGS) and a collection of indexed Arabidopsis knockout lines. One screen named “bak to life (BTL)” aims to identify suppressor mutants of cell death due to the loss of the shared PRR coreceptors BAK1 and SERK4. Genetic and biochemical analysis of BTL1 has revealed the critical roles of cyclic nucleotide-gated channels (CNGCs) in the precise control of cellular homeostasis for cell survival and elucidated the regulation of CNGC protein stability by BAK1/SERK4-mediated phosphorylation. Analysis of another BTL gene indicates that protein N-glycosylation and endoplasmic reticulum (ER) quality control play essential roles in restraining cell death and over-activation of defense.

M. V. V. de Oliveira, G. Xu, B. Li, L. de Souza Vespoli, X. Meng, X. Chen, X. Yu, S. A. de Souza, A. C. Intorne, A. M. E. de A. Manhães, A. L. Musinsky, H. Koiwa, G. A. de Souza Filho, L. Shan, P. He, Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat. Plants 2 (2016).

Improving crop resilience

An important goal of our research is to translate knowledge from studying model plants to improve agricultural performance. We have developed various functional genomic, cellular and biochemical platforms in cotton, which serves as a significant source of fiber, feed and oil products, to understand stress signaling and identify essential components to improve cotton resilience to biotic and abiotic stresses, in particular tolerance to fungal wilt pathogens, bacterial blight and drought. We have identified a complete MAP kinase cascade that phosphorylates and activates a key WRKY transcription factor in controlling cotton drought response. We are also developing a targeted systems approach to examine and identify cotton immune receptor genes, which could provide genetic resources to improve cotton resistance to fusarium wilt disease, caused by soil-borne fungal pathogen Fusarium oxysporum f. sp. vasinfectum, andunderstand the pathogenicity and genetic diversity of F. oxysporum f. sp. vasinfectum on cotton.

K. L. Cox, F. Meng, K. E. Wilkins, F. Li, P. Wang, N. J. Booher, L. Q. Chen, H. Zheng, X. Gao, Y. Zheng, Z. Fei, J. Z. Yu, T. Isakeit, T. Wheeler, W. B. Frommer, P. He, A. J. Bogdanove, L. Shan, TAL effector-mediated induction of a SWEET sucrose transporter confers susceptibility to bacterial blight of cotton. Nat. Comm. 8 (2017).