Basic Immune System of Plants

During the last several decades, extensive analyses revealed that plants utilize a two-branched immune system for defence against pathogens. In the first branch, transmembrane pattern recognition receptors (PRR), which are membrane-associated kinase or membrane-associated kinase interacting protein, are used to recognize and respond to slowly evolving microbe-associated molecular patterns (MAMP). In the second branch, either a direct or an indirect recognition of the pathogen through disease-resistance (R) proteins is used for response to pathogen virulence factors (Effector).

While extensive genetic screens successfully identified a number of receptors and components which affect abundance and maturation of the receptors, signal transduction mechanisms that lead to defence responses is thus far limited. This partly stems from limitations of forward genetics caused by lethality and/or genetic redundancy. Accordingly, my group takes comparative and evolutionary genomics/proteomics approaches to understand the basic framework of the plant immune system.


1. Phosphoproteomic dissection of PRR-triggered immunity

Several studies indicated that distinct PRRs share downstream components to induce defence responses. To identify crucial components for PRR-triggered immunity (PTI), we have been monitoring phosphoproteome dynamics upon different MAMP treatments.

One of the key requirements for successful posttranslational modification (PTM)-oriented proteomics is the establishment of efficient enrichment methods for posttranslationally modified peptides. We have developed a posttranslational modification (PTM)-oriented proteomics platform, with an emphasis on phosphorylation as this plays a significant role in early events of plant immune responses.

References and further reading

Marques DN, Stolze SC, Harzen A, Nogueira ML, Batagin-Piotto KD, Piotto FA, Mason C, Azevedo RA, Nakagami H, “Comparative phosphoproteomic analysis of tomato genotypes with contrasting cadmium tolerance”, Plant Cell Reports, Oct;40(10):2001-2008 (2021)

Li X, Sanagi M, Lu Y, Nomura Y, Stolze SC, Yasuda S, Saijo Y, Schulze WX, Feil R, Stitt M, Lunn JE, Nakagami H, Sato T, Yamaguchi J, “Protein phosphorylation dynamics under identification of a cell death-related receptor-like kinase in Arabidopsis”, Frontiers in Plant Science, Apr 3;11:377 (2020)

Kimura S, Hunter K, Vaahtera L, Tran HC, Citterico M, Vaattovaara A, Rokka A, Stolze SC, Harzen A, Meißner L, Tabea Wilkens MMT, Hamann T, Toyota M, Nakagami H, Wrzaczek M, “CRK2 and C-terminal phosphorylation of NADPH oxidase RBOHD regulate ROS production in Arabidopsis”, The Plant Cell, 32(4):1063-1080 (2020)

Matsui H, Nomura Y, Egusa M, Hamada T, Hyon GS, Kaminaka H, Watanabe Y, Ueda T, Trujillo M, Shirasu K, Nakagami H, “The GYF domain protein PSIG1 dampens the induction of cell death during plant-pathogen interactions”, PLoS Genetics, 13(10):e1007037 (2017)

Nakagami H, “StageTip-based HAMMOC, an efficient and inexpensive phosphopeptide enrichment method for plant shotgun phosphoproteomics”, Methods in Molecular Biology, 1072:595-607 (2014)

Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K, “Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants”, Plant Physiology, 153(3):1161-74 (2010)

Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y, “Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis”, Molecular Systems Biology, 4:193 (2008)


2. Immune system in the liverwort Marchantia

The comparative and evolutionary genomics/proteomics are efficient approaches to elucidate fundamental components and systems that are broadly conserved across the plant kingdom. Therefore, we started to investigate whether emerging model organism liverworts Marchantia polymorpha can be used as new model system to understand plant immunity. Importantly, Marchantia genome has been reported to have highly streamlined architecture, with smaller gene families and less redundancy compared with flowering plants. Transformation and targeted genome modification techniques for Marchantia have been already established. Analysis of Marchantia with simple gene networks is expected to facilitate exploring the fundamental components of plant immune system.

References and further reading

Jeon HW, Iwakawa H, Naramoto S, Herrfurth C, Gutsche N, Schlüter T, Kyozuka J, Miyauchi S, Feussner I, Zachgo S, Nakagami H, “Contrasting and conserved roles of NPR proteins in diverged land plant lineages”, bioRxiv (2022)

Bowman JL, Arteaga-Vazquez M, Berger F, …, Nakagami H, … et al., “The Renaissance and Enlightenment of Marchantia as a model system”, The Plant Cell, 2022 Aug 17:koac219. doi: 10.1093/plcell/koac219. Online ahead of print

Melkonian K, Stolze SC, Harzen A, Nakagami H, “miniTurbo-based interactomics of two plasma membrane-localized SNARE proteins in Marchantia polymorpha”, New Phytologist, 235(2):786-800 (2022)

Matsumoto A, Schlüter T, Melkonian K, Takeda A, Nakagami H, Mine A, “A versatile Tn7 transposon-based bioluminescence tagging tool for quantitative and spatial detection of bacteria in plants”, Plant Communications, 20;3(1):100227 (2021)

Iwakawa H, Melkonian K, Schlüter T, Jeon HW, Nishihama R, Motose H, Nakagami H, “Agrobacterium-mediated transient transformation of Marchantia liverworts”, Plant Cell & Physiology, 10;62(11):1718-1727 (2021)

Matsui H, Iwakawa H, Hyon GS, Yotsui I, Katou S, Monte I, Nishihama R, Franzen R, Solano R, Nakagami H, “Isolation of natural fungal pathogens from Marchantia polymorpha reveals antagonism between salicylic acid and jasmonate during liverwort-fungus interactions”, Plant Cell & Physiology, 61(2):265-275 (2020)

Carella P, Gogleva A, Hoey DJ, Bridgen AJ, Stolze SC, Nakagami H, Schornack S, “Conserved biochemical defenses underpin host responses to oomycete infection in an early-divergent land plant lineage”, Current Biology, 29(14):2282-2294.e5 (2019)

Bowman JL, Kohchi T, Yamato KT, …, Nakagami H, … et al., “Insights into land plant evolution garnered from the Marchantia polymorpha genome”, Cell, 171(2):287-304.e15 (2017)

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