Plant Immune Network Structure and Dynamics

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In nature, plants are constantly surrounded by a wide range of microbes (mutualists, commensals and pathogens), and at the same time exposed to environmental fluctuations such as abiotic stresses. Phytohormones are small molecules produced and perceived in plants that govern plant responses to environments as well as plant growth. Salicylic acid and jasmonates are major defense-related phytohormones. Other phytohormones such as ethylene, abscisic acid, auxin, gibberellins, cytokinins, and brassinosteroids are also involved in defense responses. Signaling pathways mediated by phytohormones intimately interact antagonistically or synergistically to form phytohormone signaling networks, which enable plants to activate appropriate and effective defense responses as well as to balance defense and growth. The importance of hormone signaling networks in plant defense is reflected by the fact that many microbes interfere with hormone signaling or produce hormones that increase microbial fitness.

Plants sense microbial molecules and turn on a battery of immune responses. PAMP/pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) are well-defined modes of plant immunity against pathogens. Recognition of pathogen/microbe-associated molecular patterns (PAMPs/MAMPs) shared by certain types of microbes, such as flg22, a part of bacterial flagellin, triggers PTI. MAMPs are recognized by pattern-recognition receptors (PRRs), which are typically receptor-like kinases (RLKs). Plant-derived damage-associated molecular patterns (DAMPs) that are released upon infection or herbivore feeding are recognized similarly to MAMPs and also trigger immune responses [Yamada et al EMBO J 2016; Ross et al EMBO J 2014]. Adapted pathogens deliver virulence effectors into the plant cell that manipulate plant immune systems, for instance PTI signaling [Tsuda et al Plant J 2012]. ETI is triggered by specific recognition of effectors by resistance (R) proteins, typically nucleotide-binding leucine-rich repeat (NLR) proteins [Cui et al Annu Rev Plant Biol 2015]. Common immune responses such as the production of reactive oxygen species, activation of MAP kinases (MAPK), and transcriptional reprogramming occur in both PTI and ETI, but with temporal and quantitative differences [Tsuda and Katagiri Curr Opin Plant Biol 2010].

We study properties, structures and functions of phytohormone signaling networks in the model plant Arabidopsis thaliana as well as other Brassicaceae plants during plant-microbe interactions. We aim at understanding plant-bacteria interactions in a holistic way [Mine and Tsuda Front Plant Sci 2014; Katagiri and Tsuda MPMI 2010] as well as underlying molecular mechanisms.

Figure 1. Signaling networks in plants and microbes.

Plants recognize microbial molecules or actions via receptors to activate defense signaling. Signaling pathways (or genes) are highly interconnected to form networks. Plant networks affect microbial signaling networks to control microbial behaviors.

Project 1 Phytohormone signaling networks in plant immunity

Understanding phytohormones signaling networks at the molecular level is crucial to understand plant adaptations to environments. We dissect phytohormone signaling networks in A. thaliana by systems approaches and molecular genetics.
[Tsuda Plant Cell Physiol 2018; Mine et al EMBO Rep 2017; Anver and Tsuda Springer 2015; Seyfferth and Tsuda Front Plant Sci 2014; Kim et al Cell Host Microbe 2014; Tintor et al PNAS 2013; Wang et al Plant J 2011; Sato et al PLoS Pathogens 2010; Qi et al MPMI 2010; Tsuda et al PLoS Genet 2009; Wang et al PLoS Pathogens 2009; Tsuda et al Plant J 2008]


Project 2 Plant transcriptional reprogramming

Time-series transcriptome analysis is powerful for disentangling complex biological processes. We generated large scale data for transcriptome response of various genotypes of A. thaliana infected with the bacterial pathogen Pseudomonas syringae or treated with the MAMP flg22 at multiple time points by RNA-seq. These data provided tremendous insights into mechanisms for transcriptional reprogramming and its significance for resistance and generated many testable hypotheses.
[Mine et al Plant Cell 2018; Jacob et al New Phytol 2018; Hillmer et al PLoS Genet 2017; Tsuda and Somssich New Phytol 2015]


Project 3 In planta bacterial transcriptome

There is an enormous gap in our understanding of how plant immunity affects bacterial behaviors for defense. We have established a method for in planta bacterial transcriptome of P. syringae in A. thaliana leaves. Bacterial cells were physically isolated from infected plant leaves in a condition that fixes and stabilizes bacterial RNA, followed by RNA-seq for bacterial mRNA. This method allows us to monitor bacterial transcriptome in a large number of samples with a reasonable cost. The work revealed hundreds of bacterial genes under control of immunity and generated many testable hypotheses. Dual plant and bacterial transcriptome analyses would lead to a holistic understanding of plant-bacteria interactions.
[Nobori et al PNAS 2018; Nobori et al FEBS Lett 2018]


Project 4 Direct suppression of bacterial growth

The mechanism by which bacterial growth is suppressed by plant immunity is not understood. We investigate plant mechanisms for direct suppression of bacterial growth. For instance, we uncovered that an evolutionarily conserved and un-described plant-secreted protease serves as molecular scissors to directly suppress growth of P. syringae in A. thaliana. Overexpression of the protease increases resistance but triggers neither immune activation nor plant growth retardation. Our finding suggests a means for producing disease resistant crops without reducing the yield.
[Nobori et al FEBS Lett 2018]


Project 5 Evolution of plant immune networks

We comprehend plant adaptations to environments only when we understand why, when, and how defense signaling pathways and their crosstalk evolved. We focus on genome-sequenced species of Brassicaceae family to which A. thaliana belongs to and compare immune responses such as transcriptional reprogramming and defense metabolites.
[Berens et al Annu Rev Phytopathol 2018]


Project 6 Abiotic and biotic stress crosstalk

Trade-off between abiotic and biotic stress responses is thought to contribute to maximizing responses to one stress over the other thereby increasing plant fitness in one stress condition. However, this does not explain if and how this trade-off is beneficial in combined stress environments, expected in nature. We investigate how plants cope with simultaneous stresses in A. thaliana and other Brassicaceae plants.


Project 7 Stomata aperture regulation

Regulation of stomata aperture is important for water vapor and gas exchange as well as immunity. Plants close stomata upon recognition of microbes to restrict their entry into plant tissues. Some P. syringae strains produce the JA mimic coronatine to open stomata to invade plant leaves. Also, many pathogens are known to activate JA signaling. We study how plants regulate and microbes manipulate stomata aperture in A. thaliana and other Brassicaceae plants.


Project 8 MAP kinases in plant defense

MAP kinases (MAPKs) are evolutionarily conserved kinases. Upon activation by upstream MAPK kinases, MAPKs modulate functions of a number of substrates via phosphorylation, thereby regulating diverse biological processes including plant immunity. We investigate functions of A. thaliana MAPKs MPK3 and MPK6 and regulations of their activity in plant immunity.
[Yamada et al EMBO J 2016; Tsuda et al PLoS Genet 2013]

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