Dataset Information

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

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.

SUBMITTER: Yang L

PROVIDER: S-EPMC4183272 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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

Yang Long L Qin Li L Liu Guosheng G Peremyslov Valera V VV Dolja Valerian V VV Wei Yangdou Y

Proceedings of the National Academy of Sciences of the United States of America 20140908 38

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-tri ...[more]

PMID: 25201952

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Project description:The integrity and dynamics of actin cytoskeleton is necessary not only for plant cell architecture but also for membrane trafficking-mediated processes such as polar auxin transport, senescence, and cell death. In Arabidopsis, the inactivation of actin-based molecular motors, class XI myosins, affects the membrane trafficking and integrity of actin cytoskeleton, and thus causes defective plant growth and morphology, altered lifespan and reduced fertility. To evaluate the potential contribution of class XI myosins to the auxin response, senescence and cell death, we followed the flower and leaf development in the triple gene knockout mutant xi1 xi2 xik (3KO) and in rescued line stably expressing myosin XI-K:YFP (3KOR). Assessing the development of primary inflorescence shoots we found that the 3KO plants produced more axillary branches. Exploiting the auxin-dependent reporters DR5::GUS and IAA2::GUS, a significant reduction in auxin responsiveness was found throughout the development of the 3KO plants. Examination of the flower development of the plants stably expressing the auxin transporter PIN1::PIN1-GFP revealed partial loss of PIN1 polarization in developing 3KO pistils. Surprisingly, the stable expression of PIN1::PIN1-GFP significantly enhanced the semi-sterile phenotype of the 3KO plants. Further we investigated the localization of myosin XI-K:YFP in the 3KOR floral organs and revealed its expression pattern in floral primordia, developing pistils, and anther filaments. Interestingly, the XI-K:YFP and PIN1::PIN1-GFP shared partially overlapping but distinct expression patterns throughout floral development. Assessing the foliar development of the 3KO plants revealed increased rosette leaf production with signs of premature yellowing. Symptoms of the premature senescence correlated with massive loss of chlorophyll, increased cell death, early plasmolysis of epidermal cells, and strong up-regulation of the stress-inducible senescence-associated gene SAG13 in 3KO plants. Simultaneously, the reduced auxin responsiveness and premature leaf senescence were accompanied by significant anthocyanin accumulation in 3KO tissues. Collectively, our results provide genetic evidences that Arabidopsis class XI myosins arrange the flower morphogenesis and leaf longevity via contributing to auxin responses, leaf senescence, and cell death.

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

Publications

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

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