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Myosins XI modulate host cellular responses and penetration resistance to fungal pathogens

Remodeling of actin cytoskeleton is thought to contribute to the establishment of effective barriers at the periphery of plant cells against fungal ingress. However, there is little information on the molecular mechanisms that regulate actin remodeling during interactions with invading pathogens.

Long Yang, Li Qin, Guosheng Liu, Valera V. Peremyslov, Valerian V. Dolja, and Yangdou Wei

 

Significance

 

Remodeling of actin cytoskeleton is thought to contribute to the establishment of effective barriers at the periphery of plant cells against fungal ingress. However, there is little information on the molecular mechanisms that regulate actin remodeling during interactions with invading pathogens. Here we show that disruption of myosin motors in Arabidopsis prevents dynamic reorganizations of actin filaments, focal organelle accumulation, and delivery of cell wall defense compounds toward the pathogen penetration site. Furthermore, the quadruple knockout mutant of class XI myosins exhibits impaired penetration resistance at the cell wall and enhanced overall disease susceptibility to both adapted and nonadapted fungal pathogens. This study provides insights into how myosins regulate cellular responses that contribute to plant immunity.

 

Abstract

 

The rapid reorganization and polarization of actin filaments (AFs) toward the pathogen penetration site is one of the earliest cellular responses, yet the regulatory mechanism of AF dynamics is poorly understood. Using live-cell imaging in Arabidopsis, we show that polarization coupled with AF bundling involves precise spatiotemporal control at the site of attempted penetration by the nonadapted barley powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). We further show that the Bgh-triggered AF mobility and organelle aggregation are predominately driven by the myosin motor proteins. Inactivation of myosins by pharmacological inhibitors prevents bulk aggregation of organelles and blocks recruitment of lignin-like compounds to the penetration site and deposition of callose and defensive protein, PENETRATION 1 (PEN1) into the apoplastic papillae, resulting in attenuation of penetration resistance. Using gene knockout analysis, we demonstrate that highly expressed myosins XI, especially myosin XI-K, are the primary contributors to cell wall-mediated penetration resistance. Moreover, the quadruple myosin knockout mutant xi-1 xi-2 xi-i xi-k displays impaired trafficking pathway responsible for the accumulation of PEN1 at the cell periphery. Strikingly, this mutant shows not only increased penetration rate but also enhanced overall disease susceptibility to both adapted and nonadapted fungal pathogens. Our findings establish myosins XI as key regulators of plant antifungal immunity.

 

See: http://www.pnas.org/content/111/38/13996.abstract.html?etoc

PNAS Sept 23, 2014; vol. 111 no. 38: 13996–14001

 

Fig. 3.Myosin inhibitor prevents focal accumulation and papillary deposition of cell wall materials. Leaves of Col-0 expressing PEN1::GFP–PEN1 infiltrated with water (mock) or 1 mM NEM were inoculated with Bgh conidiospores. (A) Accumulation and deposition of lignin-like compounds. The autofluorescence in both nonpenetrated (papillae) and penetrated (haustorial encasement) sites of fresh Col-0 leaves at 36 hpi was directly viewed by fluorescence microscopy. Insets depict close views of haustorial structures under transmitted light. (B) Accumulation and deposition of callose. The callose fluorescence in both nonpenetrated and penetrated sites of fixed and aniline blue-stained Col-0 leaves at 16 hpi was viewed by fluorescence microscopy. (C) Accumulation and deposition of GFP–PEN1. At 16 hpi, leaves of GFP–PEN1 plants were examined under a confocal microscope. Fungal conidia and appressoria were staining with PI (red). The same inoculation sites were viewed on the peripheral surface or into cells of the leaf epidermis. app, appressorium; en, haustorial encasement; ha, haustorium; pap, papilla. (Scale bars: 10 µm.)

 

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