Differential regulation of plant innate immunity Project Summary The innate immune system detects pathogen-derived molecules to prevent infections via specialized immune receptors. The immune receptors include cell surface-resident pattern recognition receptors (PRRs), such as Toll-like receptors (TLRs) in mammals and receptor-like kinases (RLKs) in plants, and intracellular NOD-like receptors (NLRs), such as plant nucleotide-binding domain leucine-rich repeat proteins. Plant plasma membrane-localized RLKs function as PRRs that sense pathogen-associated molecular patterns (PAMPs) and collectively contribute to host immunity against a broad-spectrum of pathogens. Plant intracellular NLRs detect pathogen specific effector proteins that are translocated into host cells and trigger pathogen-specific immunity, often accompanied with programmed cell death. The genetic tractability of plants made it possible to identify many plant PRR and NLR immune receptors. However, how the signaling networks underlying PRR- and NLR- mediated immunity are interconnected remains largely unknown. The PI?s laboratory has developed a series of sensitive and high-throughput genetic screens to reveal the complex activation and signaling mechanisms in plant PRR- and NLR-mediated immunity. The screens point to an unexpected role of a group of RLKs with an extracellular malectin-like domain in plant immunity. The ample preliminary evidence supports a tantalizing hypothesis that specific malectin-like RLKs regulate two-tiered plant immunity and cell death by differential modulation of PRR and NLR immune receptor complexes. Specifically, this project seeks to elucidate: how malectin-like RLKs, LET1 and LET2, inversely regulate PRR and NLR complex formation and activation; how LET1/2 are modulated by glycosylphosphatidylinositol (GPI)-anchored LLG1 as an adaptor and secreted peptide RALF9 as a ligand; and how NLR protein SUMM2 stability is inversely regulated by two distinct E3 ubiquitin ligases. By elucidating cell surface-resident malectin-like RLK module as a molecular link of PRR and NLR immune receptors, the project has the potential to change the dogma of the interconnection of PRR and NLR- mediated immunity, which was previously thought to function independently at the receptor level and only converge in downstream signaling events. Plant PRR- and NLR-mediated immunity is analogous to mammalian TLR- and NLR-mediated innate immunity respectively. Uniquely, the enriched genetic and genomic resources, including the collection of whole-genome knockout lines, as well as the well-established cellular and biochemical assays present Arabidopsis as a tractable model system to understand the host immune mechanism at the whole organismal and physiological level. Thus, the impacts of the project will reach beyond plant biology and provide complementary views to the general understanding of innate immune signaling.

Public Health Relevance

Recent advance on the molecular architecture of nonself recognition has revealed remarkable conservation in the mechanisms of microbial perception and innate immune signaling from plants to worms, insects and mammals. Our study on elucidating the signaling networks orchestrating plant immune responses will not only contribute to the current efforts of understanding molecular basis of plant immunity, but also shed light on the evolutionarily convergent mechanisms in cellular signaling of animal innate immunity. We believe that our study is relevant to the mission of NIH and is fundamental for basic medical research.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
2R01GM092893-06A1
Application #
9736890
Study Section
Cellular Signaling and Regulatory Systems Study Section (CSRS)
Program Officer
Somers, Scott D
Project Start
2010-04-01
Project End
2023-06-30
Budget Start
2019-07-01
Budget End
2020-06-30
Support Year
6
Fiscal Year
2019
Total Cost
Indirect Cost
Name
Texas A&M Agrilife Research
Department
Biochemistry
Type
Schools of Arts and Sciences
DUNS #
847205713
City
College Station
State
TX
Country
United States
Zip Code
77843
Zhou, Jinggeng; Liu, Derui; Wang, Ping et al. (2018) Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination. Proc Natl Acad Sci U S A 115:E1906-E1915
Jamieson, Pierce A; Shan, Libo; He, Ping (2018) Plant cell surface molecular cypher: Receptor-like proteins and their roles in immunity and development. Plant Sci 274:242-251
Mang, Hyunggon; Feng, Baomin; Hu, Zhangjian et al. (2017) Differential Regulation of Two-Tiered Plant Immunity and Sexual Reproduction by ANXUR Receptor-Like Kinases. Plant Cell 29:3140-3156
Feng, Baomin; Ma, Shisong; Chen, Sixue et al. (2016) PARylation of the forkhead-associated domain protein DAWDLE regulates plant immunity. EMBO Rep 17:1799-1813
Li, Bo; Meng, Xiangzong; Shan, Libo et al. (2016) Transcriptional Regulation of Pattern-Triggered Immunity in Plants. Cell Host Microbe 19:641-50
Meng, Xiangzong; Zhou, Jinggeng; Tang, Jiao et al. (2016) Ligand-Induced Receptor-like Kinase Complex Regulates Floral Organ Abscission in Arabidopsis. Cell Rep 14:1330-1338
de Oliveira, Marcos V V; Xu, Guangyuan; Li, Bo et al. (2016) Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat Plants 2:15218
Feng, Baomin; Liu, Chenglong; Shan, Libo et al. (2016) Protein ADP-Ribosylation Takes Control in Plant-Bacterium Interactions. PLoS Pathog 12:e1005941
Ma, Xiyu; Xu, Guangyuan; He, Ping et al. (2016) SERKing Coreceptors for Receptors. Trends Plant Sci 21:1017-1033
Zhou, Jinggeng; Lu, Dongping; Xu, Guangyuan et al. (2015) The dominant negative ARM domain uncovers multiple functions of PUB13 in Arabidopsis immunity, flowering, and senescence. J Exp Bot 66:3353-66

Showing the most recent 10 out of 35 publications