From filaments to function: The role of the plant actin cytoskeleton in pathogen perception, signaling and immunity.

The eukaryotic actin cytoskeleton is required for numerous cellular processes, including cell shape, development and movement, gene expression and signal transduction, and response to biotic and abiotic stress. In recent years, research in both plants and animal systems have described a function for actin as the ideal surveillance platform, linking the function and activity of primary physiological processes to the immune system. In this review, we will highlight recent advances that have defined the regulation and breadth of function of the actin cytoskeleton as a network required for defense signaling following pathogen infection. Coupled with an overview of recent work demonstrating specific targeting of the plant actin cytoskeleton by a diversity of pathogens, including bacteria, fungi and viruses, we will highlight the importance of actin as a key signaling hub in plants, one that mediates surveillance of cellular homeostasis and the activation of specific signaling responses following pathogen perception. Based on the studies highlighted herein, we propose a working model that posits changes in actin filament organization is in and of itself a highly specific signal, which induces, regulates and physically directs stimulus-specific signaling processes, most importantly, those associated with response to pathogens.

[1]  David G. Drubin,et al.  A Pathway for Association of Receptors, Adaptors, and Actin during Endocytic Internalization , 2003, Cell.

[2]  S. Lazarowitz,et al.  The Tobamovirus Turnip Vein Clearing Virus 30-Kilodalton Movement Protein Localizes to Novel Nuclear Filaments To Enhance Virus Infection , 2013, Journal of Virology.

[3]  Xiaojun Ding,et al.  Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. , 2010, Cell host & microbe.

[4]  R. Uribe,et al.  A review of actin binding proteins: new perspectives , 2007, Molecular Biology Reports.

[5]  P. Percipalle Co-transcriptional nuclear actin dynamics , 2013, Nucleus.

[6]  Aiming Wang,et al.  The Tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. , 2010, Virology.

[7]  S. He,et al.  Role of stomata in plant innate immunity and foliar bacterial diseases. , 2008, Annual review of phytopathology.

[8]  A. Hardham,et al.  Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack , 2008, BMC Plant Biology.

[9]  Kathryn R. Ayscough,et al.  Functions of actin in endocytosis , 2009, Cellular and Molecular Life Sciences.

[10]  Zhiqi Jia,et al.  Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis thaliana suspension cells , 2006, Protoplasma.

[11]  S. Gilroy,et al.  Feeling green: mechanosensing in plants. , 2009, Trends in cell biology.

[12]  D. MacLean,et al.  Spatio-Temporal Cellular Dynamics of the Arabidopsis Flagellin Receptor Reveal Activation Status-Dependent Endosomal Sorting[C][W] , 2012, Plant Cell.

[13]  E. Schmelzer,et al.  Profilin and Rop GTPases are localized at infection sites of plant cells , 2006, Protoplasma.

[14]  Lili Zhu,et al.  A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination , 2013, The Plant journal : for cell and molecular biology.

[15]  P. Schulze-Lefert,et al.  Secretory Pathways in Plant Immune Responses1 , 2008, Plant Physiology.

[16]  E. Nishida,et al.  Nuclear export of actin: a novel mechanism regulating the subcellular localization of a major cytoskeletal protein , 1998, The EMBO journal.

[17]  R. Mullins,et al.  What we talk about when we talk about nuclear actin , 2013, Nucleus.

[18]  L. Stuart,et al.  Effector-triggered versus pattern-triggered immunity: how animals sense pathogens , 2013, Nature Reviews Immunology.

[19]  G. Grondin,et al.  Impact on the Endoplasmic Reticulum and Golgi Apparatus of Turnip Mosaic Virus Infection , 2012, Journal of Virology.

[20]  Jian-Min Zhou,et al.  Plant immunity triggered by microbial molecular signatures. , 2010, Molecular plant.

[21]  S. Duke,et al.  Modes of Action of Microbially-Produced Phytotoxins , 2011, Toxins.

[22]  A. Roberts,et al.  Two Plant–Viral Movement Proteins Traffic in the Endocytic Recycling Pathwayw⃞ , 2005, The Plant Cell Online.

[23]  M. Bezanilla,et al.  Class II formin targeting to the cell cortex by binding PI(3,5)P2 is essential for polarized growth , 2012, The Journal of cell biology.

[24]  M. Vartiainen,et al.  To be or not to be assembled: progressing into nuclear actin filaments , 2013, Nature Reviews Molecular Cell Biology.

[25]  Sheng Yang He,et al.  Plant Stomata Function in Innate Immunity against Bacterial Invasion , 2006, Cell.

[26]  J. Mundy,et al.  Mitogen-activated protein kinase signaling in plants. , 2010, Annual review of plant biology.

[27]  R. Meagher,et al.  Differential sublocalization of actin variants within the nucleus , 2010, Cytoskeleton.

[28]  Elizabeth A. Savory,et al.  Arabidopsis NDR1 Is an Integrin-Like Protein with a Role in Fluid Loss and Plasma Membrane-Cell Wall Adhesion1[W][OA] , 2011, Plant Physiology.

[29]  Laurent Blanchoin,et al.  Actin dynamics, architecture, and mechanics in cell motility. , 2014, Physiological reviews.

[30]  Melissa A. Chesarone,et al.  Unleashing formins to remodel the actin and microtubule cytoskeletons , 2010, Nature Reviews Molecular Cell Biology.

[31]  S. Winder,et al.  Actin-binding proteins , 2005, Journal of Cell Science.

[32]  R. Merriam,et al.  Diffusible and bound actin in nuclei of xenopus laevis oocytes , 1977, Cell.

[33]  P. Aspenström Formin-binding proteins: modulators of formin-dependent actin polymerization. , 2010, Biochimica et biophysica acta.

[34]  Scott D. Hansen,et al.  In vitro studies of actin filament and network dynamics. , 2013, Current opinion in cell biology.

[35]  Xiaorong Tao,et al.  Nucleocapsid of Tomato spotted wilt tospovirus forms mobile particles that traffic on an actin/endoplasmic reticulum network driven by myosin XI-K. , 2013, The New phytologist.

[36]  W. Kiosses,et al.  Vesicular trafficking through cortical actin during exocytosis is regulated by the Rab27a effector JFC1/Slp1 and the RhoA-GTPase–activating protein Gem-interacting protein , 2012, Molecular biology of the cell.

[37]  B. Day,et al.  ACTIN DEPOLYMERIZING FACTOR4 Regulates Actin Dynamics during Innate Immune Signaling in Arabidopsis[W][OPEN] , 2014, Plant Cell.

[38]  L. Deslandes,et al.  The plant cell nucleus , 2011, Plant signaling & behavior.

[39]  Jinxing Lin,et al.  Endocytosis and its regulation in plants. , 2015, Trends in plant science.

[40]  I. Dawes,et al.  Actin - a biosensor that determines cell fate in yeasts. , 2014, FEMS yeast research.

[41]  Samara L. Reck-Peterson,et al.  Nuclear actin and actin-related proteins in chromatin remodeling. , 2002, Annual review of biochemistry.

[42]  F. Ausubel Are innate immune signaling pathways in plants and animals conserved? , 2005, Nature Immunology.

[43]  V. Dolja,et al.  Myosins XI modulate host cellular responses and penetration resistance to fungal pathogens , 2014, Proceedings of the National Academy of Sciences.

[44]  S. Robatzek Vesicle trafficking in plant immune responses , 2007, Cellular microbiology.

[45]  Xin Chen,et al.  Soybean actin-depolymerizing factor 2 interacts with Soybean mosaic virus-encoded P3 protein , 2014, Virus Genes.

[46]  D. Gilbert,et al.  Actin up in the nucleus , 2004, Nature Reviews Molecular Cell Biology.

[47]  P. Hussey,et al.  Interactions between plant endomembrane systems and the actin cytoskeleton , 2015, Front. Plant Sci..

[48]  K. Shimamoto,et al.  Rho family GTPase-dependent immunity in plants and animals , 2014, Front. Plant Sci..

[49]  Imara Y. Perera,et al.  Phosphoinositide-signaling is one component of a robust plant defense response , 2014, Front. Plant Sci..

[50]  L. Blanchoin,et al.  Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array , 2009, The Journal of cell biology.

[51]  S. Meinhardt,et al.  Role of the Arginyl-Glycyl-Aspartic Motif in the Action of Ptr ToxA Produced by Pyrenophora tritici-repentis 1 , 2002, Plant Physiology.

[52]  David A Jones,et al.  Cytoskeleton and cell wall function in penetration resistance. , 2007, Current opinion in plant biology.

[53]  Richard O Hynes,et al.  Integrins Bidirectional, Allosteric Signaling Machines , 2002, Cell.

[54]  Min Woo Lee,et al.  HopW1 from Pseudomonas syringae Disrupts the Actin Cytoskeleton to Promote Virulence in Arabidopsis , 2014, PLoS Pathogens.

[55]  J. Borst,et al.  The Cytosolic Nucleoprotein of the Plant-Infecting Bunyavirus Tomato Spotted Wilt Recruits Endoplasmic Reticulum–Resident Proteins to Endoplasmic Reticulum Export Sites[C][W] , 2013, Plant Cell.

[56]  L. Ciuffetti,et al.  Localization of Ptr ToxA Produced by Pyrenophora tritici-repentis Reveals Protein Import into Wheat Mesophyll Cells , 2005, The Plant Cell Online.

[57]  A. Emons,et al.  Golgi body motility in the plant cell cortex correlates with actin cytoskeleton organization. , 2011, Plant & cell physiology.

[58]  R. Voegele,et al.  TaADF7, an actin-depolymerizing factor, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. , 2014, The Plant journal : for cell and molecular biology.

[59]  F. Cvrčková Formins and membranes: anchoring cortical actin to the cell wall and beyond , 2013, Front. Plant Sci..

[60]  Jeff H. Chang,et al.  The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns , 2013, PLoS pathogens.

[61]  P. Hussey,et al.  Control of the actin cytoskeleton in plant cell growth. , 2006, Annual review of plant biology.

[62]  B. Jockusch,et al.  Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes , 1984, Cell.

[63]  P. Percipalle,et al.  The F-actin severing protein cofilin-1 is required for RNA polymerase II transcription elongation. , 2011, Nucleus.

[64]  Hongyan Wang,et al.  Integrin signalling and function in immune cells , 2012, Immunology.

[65]  R. Doerge,et al.  Cytokinins Secreted by Agrobacterium Promote Transformation by Repressing a Plant Myb Transcription Factor , 2013, Science Signaling.

[66]  R. Deal,et al.  ACTIN DEPOLYMERIZING FACTOR9 controls development and gene expression in Arabidopsis , 2008, Plant Molecular Biology.

[67]  J. Mathur,et al.  Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation , 2003, Development.

[68]  I. Kobayashi,et al.  Microwounding is a pivotal factor for the induction of actin-dependent penetration resistance against fungal attack , 2013, Planta.

[69]  J. Imler,et al.  Microbial sensing by Toll receptors: a historical perspective. , 2011, Arteriosclerosis, thrombosis, and vascular biology.

[70]  E. Grill,et al.  A LIM Domain Protein from Tobacco Involved in Actin-Bundling and Histone Gene Transcription , 2012, Molecular plant.

[71]  A. Asch,et al.  Post‐transcriptional regulation of the Ras‐ERK/MAPK signaling pathway , 2012, Journal of cellular physiology.

[72]  M. Bezanilla,et al.  Plant formins: membrane anchors for actin polymerization. , 2013, Trends in cell biology.

[73]  Jian-Kang Zhu,et al.  Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase , 2013, Front. Plant Sci..

[74]  B. Day,et al.  The pathogen-actin connection: a platform for defense signaling in plants. , 2011, Annual review of phytopathology.

[75]  H. Hirt,et al.  Signaling mechanisms in pattern-triggered immunity (PTI). , 2015, Molecular plant.

[76]  B. Day,et al.  Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity , 2015, Nature Communications.

[77]  Daniel R. Ruzicka,et al.  Arabidopsis Actin-Depolymerizing Factor AtADF4 Mediates Defense Signal Transduction Triggered by the Pseudomonas syringae Effector AvrPphB1[W][OA] , 2009, Plant Physiology.

[78]  Xuetong Shen,et al.  Mechanisms of nuclear actin in chromatin-remodeling complexes. , 2014, Trends in cell biology.

[79]  Natsumaro Kutsuna,et al.  Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. , 2010, The Plant journal : for cell and molecular biology.

[80]  J. Gurdon,et al.  Transcriptional regulation and nuclear reprogramming: roles of nuclear actin and actin-binding proteins , 2012, Cellular and Molecular Life Sciences.

[81]  R. Barrero,et al.  Arabidopsis CAP Regulates the Actin Cytoskeleton Necessary for Plant Cell Elongation and Division Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010301. , 2002, The Plant Cell Online.

[82]  N. Stergiopulos,et al.  Gelsolin superfamily proteins: key regulators of cellular functions , 2004, Cellular and Molecular Life Sciences CMLS.

[83]  Kari-Pekka Skarp,et al.  Active maintenance of nuclear actin by importin 9 supports transcription , 2012, Proceedings of the National Academy of Sciences.

[84]  L. Blanchoin,et al.  Arabidopsis Capping Protein (AtCP) Is a Heterodimer That Regulates Assembly at the Barbed Ends of Actin Filaments* , 2003, Journal of Biological Chemistry.

[85]  J. Schultz,et al.  FHOD proteins in actin dynamics—a formin’ class of its own , 2014, Small GTPases.

[86]  J. Cooper,et al.  Actin dynamics and endocytosis in yeast and mammals. , 2010, Current opinion in biotechnology.

[87]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[88]  S. Gelvin,et al.  Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells , 2008, Plant Methods.

[89]  Shanwei Li,et al.  Profilin as a regulator of the membrane-actin cytoskeleton interface in plant cells , 2013, Front. Plant Sci..

[90]  J. Cooper,et al.  Roles for actin assembly in endocytosis. , 2012, Annual review of biochemistry.

[91]  R. Dominguez,et al.  Regulation of actin cytoskeleton dynamics in cells , 2010, Molecules and cells.

[92]  I. Somssich,et al.  The Role of WRKY Transcription Factors in Plant Immunity[W] , 2009, Plant Physiology.

[93]  B. Day,et al.  Arabidopsis Actin-Depolymerizing Factor-4 Links Pathogen Perception, Defense Activation and Transcription to Cytoskeletal Dynamics , 2012, PLoS pathogens.

[94]  A. Maule,et al.  Differing requirements for actin and myosin by plant viruses for sustained intercellular movement , 2009, Proceedings of the National Academy of Sciences.

[95]  Matthew D. Welch,et al.  A nucleator arms race: cellular control of actin assembly , 2010, Nature Reviews Molecular Cell Biology.