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Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants

  • Current Topics in Plant Research
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Abstract

Plants have evolved various means for controlled and organized cell destruction, known as programmed cell death (PCD). In plant immune responses against microbial infection, hypersensitive cell death as a form of PCD is a crucial event to prevent the spread of biotrophic pathogens. Recent live cell imaging techniques have revealed dynamic features and significant roles of cytoskeletons and the vacuole during defense responses and the PCD. Actin microfilaments (MFs) focus on the infection sites and function as tracks for the polar transport of antimicrobial materials. To accomplish hypersensitive cell death, further dynamic changes in cytoskeletons are induced. MFs play a role in the structural and functional regulation of the vacuole, leading to execution of the PCD. We here overview spatiotemporal dynamic changes in the cytoskeletons and the vacuoles triggered by signals from pathogens, and propose a hypothetical model for MF-regulated vacuole-mediated PCD in plant immunity.

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Acknowledgments

The authors thank to Drs. Tatsuaki Goh (Kobe University), Yasuhiro Kadota (The Sainsbury Laboratory), Teruyuki Hayashi (National Institute of Agrobiological Sciences), Natsumaro Kutsuna (The University of Tokyo), and Toshio Sano (Hosei University) for helpful discussions. This work was supported in part by Grants-in-Aid Scientific Research on Priority Areas (17051027 to K.K., 19039008 and 20061008 to S.H.), for Scientific Research on Innovative Areas (21200067 to T.K.), for Exploratory Research (21658118 to K.K.) and for Young Scientists (B) (21780041 to T.K.) from the Ministry of Education, Science, Culture, Sports and Technology of Japan, and by grants from Japan Science and Technology Agency, for Adaptable and Seamless Technology transfer Program through target-driven R&D (AS221Z03504E) to T.K.

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  1. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha, Kashiwa, Chiba, 277-8562, Japan

    Takumi Higaki & Seiichiro Hasezawa

  2. Department of Applied Biological Science, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510, Japan

    Takumi Higaki, Takamitsu Kurusu & Kazuyuki Kuchitsu

  3. Research Institute for Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510, Japan

    Takamitsu Kurusu & Kazuyuki Kuchitsu

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  1. Takumi Higaki
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Correspondence to Kazuyuki Kuchitsu.

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Supplemental Fig. 1

Reorganization of actin microfilaments (MFs) in S-phase-synchronized tobacco (Nicotiana tabacum) BY-2 cells treated with cryptogein. Cell cortex (a and b) and mid-plane images (c and d) were obtained in synchronized BY-2 cells expressing GFP-ABD2 just after (S phase; a and c) and 12 h after (b and d) cryptogein treatment. Fine cortical meshworks of MFs at S phase (a) change into transversely oriented heavy bundles after cryptogein treatment (b). Endoplasmic MFs that connect the nuclear periphery to the cell cortex (c) decrease, which accompanies nuclear translocation from the cell center to the cell periphery (d). Scale bars: 20 μm (TIFF 5460 kb)

Supplemental Fig. 2

Reorganization of microtubules (MTs) in S-phase-synchronized tobacco (Nicotiana tabacum) BY-2 cells treated with cryptogein. Cell cortex (a and b) and mid-plane images (c and d) were obtained in synchronized BY-2 cells expressing GFP-tubulin just after (S phase; a and c) and 12 h after (b and d) cryptogein treatment. Most of the cortical MTs at S phase (a) were disrupted at 12 h after cryptogein treatment (b). Endoplasmic MTs that connect the nuclear periphery to the cell cortex (c) are decreased accompanying nuclear translocation from the cell center to the cell periphery (d). Scale bars: 20 μm (TIFF 6571 kb)

Supplemental Fig. 3

Changes in vacuolar morphology and permeability in S-phase-synchronized tobacco (Nicotiana tabacum) BY-2 cells treated with cryptogein. Vacuoles are prestained with a fluorescent probe, BCECF. DIC (a-c) and BCECF fluorescence images (d-f) in representative cells at 0 (S phase; a and d), 12 (b and e), and 24 h (c and f) after cryptogein treatment are shown. The complicated morphology of vacuoles that are passed through by transvacuolar strands at S phase (a and d) changes into simple structures around 12 h after cryptogein treatment (b and e). Thereafter, cells without BCECF fluorescence appear (c and f; an arrowed cell). Double staining of Evans blue and BCECF (g) shows the cells without BCECF fluorescence are dead. Yellow dashed lines indicate the dead cells stained with Evans blue. Scale bars: 20 μm (TIFF 7302 kb)

Supplemental Fig. 4

Reorganization of the vacuolar membranes (VMs) in S-phase-synchronized tobacco (Nicotiana tabacum) BY-2 cells treated with cryptogein. Optical sections at mid-plane were obtained in synchronized BY-2 cells expressing GFP-AtVAM3 just after (S phase; a), 12 h after (b), and 18 h after (c) cryptogein treatment. Most of the TVSs at S phase (a) were converted into bulb-like structures by 12 h after cryptogein treatment (b). Thereafter, the bulb-like structures disappeared and the large vacuole became simple-shaped structures (c). Scale bars: 20 μm (TIFF 2856 kb)

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Higaki, T., Kurusu, T., Hasezawa, S. et al. Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants. J Plant Res 124, 315–324 (2011). https://doi.org/10.1007/s10265-011-0408-z

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