Actin Depolymerizing Factor Modulates Rhizobial Infection and Nodule Organogenesis in Common Bean

Actin plays a critical role in the rhizobium–legume symbiosis. Cytoskeletal rearrangements and changes in actin occur in response to Nod factors secreted by rhizobia during symbiotic interactions with legumes. These cytoskeletal rearrangements are mediated by diverse actin-binding proteins, such as actin depolymerization factors (ADFs). We examined the function of an ADF in the Phaseolus vulgaris–rhizobia symbiotic interaction (PvADFE). PvADFE was preferentially expressed in rhizobia-inoculated roots and nodules. PvADFE promoter activity was associated with root hairs harbouring growing infection threads, cortical cell divisions beneath root hairs, and vascular bundles in mature nodules. Silencing of PvADFE using RNA interference increased the number of infection threads in the transgenic roots, resulting in increased nodule number, nitrogen fixation activity, and average nodule diameter. Conversely, overexpression of PvADFE reduced the nodule number, nitrogen fixation activity, average nodule diameter, as well as NODULE INCEPTION (NIN) and EARLY NODULIN2 (ENOD2) transcript accumulation. Hence, changes in ADFE transcript levels affect rhizobial infection and nodulation, suggesting that ADFE is fine-tuning these processes.

[1]  B. Day,et al.  Battlefield Cytoskeleton: Turning the Tide on Plant Immunity. , 2019, Molecular plant-microbe interactions : MPMI.

[2]  C. Gutjahr.  Symbiosis: Plasmodesmata Link Root-Nodule Organogenesis with Infection , 2018, Current Biology.

[3]  Yoselin Benitez-Alfonso,et al.  Callose-Regulated Symplastic Communication Coordinates Symbiotic Root Nodule Development , 2018, Current Biology.

[4]  Juan Tian,et al.  The host actin cytoskeleton channels rhizobia release and facilitates symbiosome accommodation during nodulation in Medicago truncatula. , 2018, The New phytologist.

[5]  Sudhir Kumar,et al.  MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. , 2018, Molecular biology and evolution.

[6]  V. Nalam,et al.  Arabidopsis ACTIN-DEPOLYMERIZING FACTOR3 Is Required for Controlling Aphid Feeding from the Phloem1[OPEN] , 2017, Plant Physiology.

[7]  S. Long.  SnapShot: Signaling in Symbiosis , 2016, Cell.

[8]  Arif Hasan Khan Robin,et al.  Genome-Wide Identification, Characterization and Expression Profiling of ADF Family Genes in Solanum lycopersicum L. , 2016, Genes.

[9]  M. Frame,et al.  Cellular functions of the ADF/cofilin family at a glance , 2016, Journal of Cell Science.

[10]  J. Murray.  The Cell Cycle in Nodulation , 2016 .

[11]  Katie Porter,et al.  From filaments to function: The role of the plant actin cytoskeleton in pathogen perception, signaling and immunity. , 2016, Journal of integrative plant biology.

[12]  Z. Kang,et al.  TaADF3, an Actin-Depolymerizing Factor, Negatively Modulates Wheat Resistance Against Puccinia striiformis , 2016, Front. Plant Sci..

[13]  N. Inada,et al.  Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus1[OPEN] , 2016, Plant Physiology.

[14]  R. Meagher,et al.  Phylogenetic Patterns of Codon Evolution in the ACTIN-DEPOLYMERIZING FACTOR/COFILIN (ADF/CFL) Gene Family , 2015, PloS one.

[15]  Trevor L. Wang,et al.  SCARN a Novel Class of SCAR Protein That Is Required for Root-Hair Infection during Legume Nodulation , 2015, PLoS genetics.

[16]  T. Bisseling,et al.  ARP2/3-Mediated Actin Nucleation Associated With Symbiosome Membrane Is Essential for the Development of Symbiosomes in Infected Cells of Medicago truncatula Root Nodules. , 2015, Molecular plant-microbe interactions : MPMI.

[17]  E. Limpens,et al.  Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair1 , 2015, Plant Physiology.

[18]  E. Bennett,et al.  The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize , 2015, Nature Plants.

[19]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[20]  M. Sokabe,et al.  Single-molecule imaging and kinetic analysis of cooperative cofilin–actin filament interactions , 2014, Proceedings of the National Academy of Sciences.

[21]  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.

[22]  J. Kunkel,et al.  Visualization of highly dynamic F-actin plus ends in growing phaseolus vulgaris root hair cells and their responses to Rhizobium etli nod factors. , 2014, Plant & cell physiology.

[23]  A. Alexandre,et al.  Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. , 2014, Microbiological research.

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

[25]  T. Ketelaar.  The actin cytoskeleton in root hairs: all is fine at the tip. , 2013, Current opinion in plant biology.

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

[27]  G. Oldroyd.  Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants , 2013, Nature Reviews Microbiology.

[28]  Minh Anh Nguyen,et al.  Ultrafast Approximation for Phylogenetic Bootstrap , 2013, Molecular biology and evolution.

[29]  Men-Chi Chang,et al.  Comprehensive analysis of differentially expressed rice actin depolymerizing factor gene family and heterologous overexpression of OsADF3 confers Arabidopsis Thaliana drought tolerance , 2012, Rice.

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

[31]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[32]  P. Poole,et al.  The rules of engagement in the legume-rhizobial symbiosis. , 2011, Annual review of genetics.

[33]  P. Lappalainen,et al.  Actin‐depolymerizing factor homology domain: A conserved fold performing diverse roles in cytoskeletal dynamics , 2011, Cytoskeleton.

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

[35]  A. Geitmann,et al.  Spatial and temporal expression of actin depolymerizing factors ADF7 and ADF10 during male gametophyte development in Arabidopsis thaliana. , 2011, Plant & cell physiology.

[36]  Zhenbiao Yang,et al.  RHO GTPase in plants , 2010, Small GTPases.

[37]  Jens Stougaard,et al.  The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus , 2010, Nature communications.

[38]  E. D. L. Cruz.  How cofilin severs an actin filament , 2009, Biophysical Reviews.

[39]  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.

[40]  M. Hossain,et al.  Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti[C][W] , 2009, The Plant Cell Online.

[41]  F. Sánchez,et al.  Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). , 2008, The Plant journal : for cell and molecular biology.

[42]  F. Sánchez,et al.  Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. , 2008, Plant, cell & environment.

[43]  A. Timmers,et al.  The role of the plant cytoskeleton in the interaction between legumes and rhizobia , 2008, Journal of microscopy.

[44]  L. Vidali,et al.  Actin depolymerizing factor is essential for viability in plants, and its phosphoregulation is important for tip growth. , 2008, The Plant journal : for cell and molecular biology.

[45]  Daniel R. Ruzicka,et al.  The ancient subclasses of Arabidopsis Actin Depolymerizing Factor genes exhibit novel and differential expression. , 2007, The Plant journal : for cell and molecular biology.

[46]  P. Gresshoff,et al.  Fast, efficient and reproducible genetic transformation of Phaseolus spp. by Agrobacterium rhizogenes , 2007, Nature Protocols.

[47]  E. Andrianantoandro,et al.  Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. , 2006, Molecular cell.

[48]  Qingpo Liu,et al.  Comparative study of rice and Arabidopsis actin-depolymerizing factors gene families. , 2006, Journal of plant physiology.

[49]  Adrienne R Hardham,et al.  The Cytoskeleton as a Regulator and Target of Biotic Interactions in Plants , 2004, Plant Physiology.

[50]  G. Gheysen,et al.  Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. , 2004, The Plant journal : for cell and molecular biology.

[51]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[52]  Manuel Middendorf,et al.  Discriminative topological features reveal biological network mechanisms , 2004, BMC Bioinformatics.

[53]  L. Vidali,et al.  The Regulation of Actin Organization by Actin-Depolymerizing Factor in Elongating Pollen Tubes Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003038. , 2002, The Plant Cell Online.

[54]  Ilha Lee,et al.  Petunia actin-depolymerizing factor is mainly accumulated in vascular tissue and its gene expression is enhanced by the first intron. , 2002, Gene.

[55]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[56]  P. Hussey,et al.  The ADF/cofilin family: actin-remodeling proteins , 2002, Genome Biology.

[57]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[58]  W. Newcomb,et al.  Changes in actin microfilament arrays in developing pea root nodule cells , 2001 .

[59]  P. Hussey,et al.  Phosphorylation of plant actin‐depolymerising factor by calmodulin‐like domain protein kinase , 2001, FEBS letters.

[60]  C. Schutt,et al.  A comparative structural analysis of the ADF/Cofilin family , 2000, Proteins.

[61]  J. Stougaard.  Regulators and regulation of legume root nodule development. , 2000, Plant physiology.

[62]  J. Feijó,et al.  Ion changes in legume root hairs responding to Nod factors. , 2000, Plant physiology.

[63]  E. Kondorosi,et al.  Mitotic B-type cyclins are differentially regulated by phytohormones and during yellow lupine nodule development , 2000 .

[64]  Leif Schauser,et al.  A plant regulator controlling development of symbiotic root nodules , 1999, Nature.

[65]  Jaime Mora,et al.  Rhizobium etli Genetically Engineered for the Heterologous Expression of Vitreoscilla sp. Hemoglobin: Effects on Free-Living and Symbiosis , 1999 .

[66]  T. Bisseling,et al.  Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes , 1999 .

[67]  P. Hussey,et al.  Interaction of maize actin‐depolymerising factor with actin and phosphoinositides and its inhibition of plant phospholipase C. , 1998 .

[68]  D. Drubin,et al.  The ADF homology (ADF-H) domain: a highly exploited actin-binding module. , 1998, Molecular biology of the cell.

[69]  D. Davies,et al.  Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by a calcium-stimulated protein kinase and is essential for the control of functional activity. , 1998, The Plant journal : for cell and molecular biology.

[70]  F. Sánchez,et al.  Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals , 1998, Plant physiology.

[71]  P. Hussey,et al.  The maize actin-depolymerizing factor, ZmADF3, redistributes to the growing tip of elongating root hairs and can be induced to translocate into the nucleus with actin. , 1997, The Plant journal : for cell and molecular biology.

[72]  A. Fedorov,et al.  Essential functions and actin‐binding surfaces of yeast cofilin revealed by systematic mutagenesis , 1997, The EMBO journal.

[73]  E. Kondorosi,et al.  Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals , 1996 .

[74]  D. Ehrhardt,et al.  Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals , 1996, Cell.

[75]  D. Ehrhardt,et al.  Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. , 1992, Science.

[76]  E. Nishida,et al.  A short sequence responsible for both phosphoinositide binding and actin binding activities of cofilin. , 1991, The Journal of biological chemistry.

[77]  R. Jefferson.  Assaying chimeric genes in plants: The GUS gene fusion system , 1987, Plant Molecular Biology Reporter.

[78]  W. Broughton,et al.  Control of leghaemoglobin synthesis in snake beans. , 1971, The Biochemical journal.

[79]  E. M. De La Cruz.  How cofilin severs an actin filament , 2009, Biophysical reviews.

[80]  D. McCurdy,et al.  Actin and actin-binding proteins in higher plants , 2005, Protoplasma.