Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development1[OPEN]

Analysis of mutant plants points to a synergistic role of two regulators of the ESCRT components SKD1 during plant development. SKD1 is a core component of the mechanism that degrades plasma membrane proteins via the Endosomal Sorting Complex Required for Transport (ESCRT) pathway. Its ATPase activity and endosomal recruitment are regulated by the ESCRT components LIP5 and IST1. How LIP5 and IST1 affect ESCRT-mediated endosomal trafficking and development in plants is not known. Here we use Arabidopsis mutants to demonstrate that LIP5 controls the constitutive degradation of plasma membrane proteins and the formation of endosomal intraluminal vesicles. Although lip5 mutants were able to polarize the auxin efflux facilitators PIN2 and PIN3, both proteins were mis-sorted to the tonoplast in lip5 root cells. In addition, lip5 root cells over-accumulated PIN2 at the plasma membrane. Consistently with the trafficking defects of PIN proteins, the lip5 roots showed abnormal gravitropism with an enhanced response within the first 4 h after gravistimulation. LIP5 physically interacts with IST1-LIKE1 (ISTL1), a protein predicted to be the Arabidopsis homolog of yeast IST1. However, we found that Arabidopsis contains 12 genes coding for predicted IST1-domain containing proteins (ISTL1–12). Within the ISTL1–6 group, ISTL1 showed the strongest interaction with LIP5, SKD1, and the ESCRT-III-related proteins CHMP1A in yeast two hybrid assays. Through the analysis of single and double mutants, we found that the synthetic interaction of LIP5 with ISTL1, but not with ISTL2, 3, or 6, is essential for normal plant growth, repression of spontaneous cell death, and post-embryonic lethality.

[1]  Xiangzong Meng,et al.  Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation , 2016, Nature Plants.

[2]  Adam Frost,et al.  Structure and membrane remodeling activity of ESCRT-III helical polymers , 2015, Science.

[3]  L. Benson,et al.  Conformational Changes in the Endosomal Sorting Complex Required for the Transport III Subunit Ist1 Lead to Distinct Modes of ATPase Vps4 Regulation* , 2015, The Journal of Biological Chemistry.

[4]  C. Luschnig,et al.  Tricho- and atrichoblast cell files show distinct PIN2 auxin efflux carrier exploitations and are jointly required for defined auxin-dependent root organ growth , 2015, Journal of experimental botany.

[5]  Zhaohui Xu,et al.  Distinct Mechanisms of Recognizing Endosomal Sorting Complex Required for Transport III (ESCRT-III) Protein IST1 by Different Microtubule Interacting and Trafficking (MIT) Domains* , 2015, The Journal of Biological Chemistry.

[6]  Zhaohui Xu,et al.  A Novel Mechanism of Regulating the ATPase VPS4 by Its Cofactor LIP5 and the Endosomal Sorting Complex Required for Transport (ESCRT)-III Protein CHMP5* , 2015, The Journal of Biological Chemistry.

[7]  Liwen Jiang,et al.  Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation , 2015, Proceedings of the National Academy of Sciences.

[8]  J. Chory,et al.  Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination , 2015, Nature Communications.

[9]  Jun Xia,et al.  A Unique Plant ESCRT Component, FREE1, Regulates Multivesicular Body Protein Sorting and Plant Growth , 2014, Current Biology.

[10]  Daniel R. Lewis,et al.  Block of ATP-Binding Cassette B19 Ion Channel Activity by 5-Nitro-2-(3-Phenylpropylamino)-Benzoic Acid Impairs Polar Auxin Transport and Root Gravitropism1[OPEN] , 2014, Plant Physiology.

[11]  Julie C. Mitchell,et al.  Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly , 2014, The Journal of cell biology.

[12]  Zhaohui Xu,et al.  Vps4 Stimulatory Element of the Cofactor Vta1 Contacts the ATPase Vps4 α7 and α9 to Stimulate ATP Hydrolysis* , 2014, The Journal of Biological Chemistry.

[13]  Yifen Shang,et al.  Arabidopsis LIP5, a Positive Regulator of Multivesicular Body Biogenesis, Is a Critical Target of Pathogen-Responsive MAPK Cascade in Plant Basal Defense , 2014, PLoS pathogens.

[14]  Caiji Gao,et al.  The Arabidopsis Endosomal Sorting Complex Required for Transport III Regulates Internal Vesicle Formation of the Prevacuolar Compartment and Is Required for Plant Development1[C][W][OPEN] , 2014, Plant Physiology.

[15]  C. Schwechheimer,et al.  Cytokinin Controls Polarity of PIN1-Dependent Auxin Transport during Lateral Root Organogenesis , 2014, Current Biology.

[16]  H. Lindner,et al.  Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation , 2014, The Journal of cell biology.

[17]  M. Otegui,et al.  A Novel Endosomal Sorting Complex Required for Transport (ESCRT) Component in Arabidopsis thaliana Controls Cell Expansion and Development* , 2014, The Journal of Biological Chemistry.

[18]  C. Luschnig,et al.  Arabidopsis TOL Proteins Act as Gatekeepers for Vacuolar Sorting of PIN2 Plasma Membrane Protein , 2013, Current Biology.

[19]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[20]  Y. Kawamura,et al.  Cellular Auxin Homeostasis under High Temperature Is Regulated through a SORTING NEXIN1–Dependent Endosomal Trafficking Pathway[C][W] , 2013, Plant Cell.

[21]  H. Fu,et al.  IRT1 DEGRADATION FACTOR1, a RING E3 Ubiquitin Ligase, Regulates the Degradation of IRON-REGULATED TRANSPORTER1 in Arabidopsis[C][W][OPEN] , 2013, Plant Cell.

[22]  Andrew P Norgan,et al.  Relief of Autoinhibition Enhances Vta1 Activation of Vps4 via the Vps4 Stimulatory Element* , 2013, The Journal of Biological Chemistry.

[23]  M. Komada,et al.  The ubiquitin code and its decoding machinery in the endocytic pathway. , 2013, Journal of biochemistry.

[24]  Miguel C. Teixeira,et al.  A Major Facilitator Superfamily Transporter Plays a Dual Role in Polar Auxin Transport and Drought Stress Tolerance in Arabidopsis[W] , 2013, Plant Cell.

[25]  M. Van Montagu,et al.  Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism , 2013, Proceedings of the National Academy of Sciences.

[26]  C. Luschnig,et al.  Dynamics in PIN2 auxin carrier ubiquitylation in gravity-responding Arabidopsis roots , 2012, Plant signaling & behavior.

[27]  Zhenbiao Yang,et al.  ABP1 and ROP6 GTPase Signaling Regulate Clathrin-Mediated Endocytosis in Arabidopsis Roots , 2012, Current Biology.

[28]  A. Cardona,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[29]  E. Zažímalová,et al.  Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth , 2012, Proceedings of the National Academy of Sciences.

[30]  M. Curtiss,et al.  Regulation of Membrane Protein Degradation by Starvation‐Response Pathways , 2012, Traffic.

[31]  D. Gerlich,et al.  ESCRT-III polymers in membrane neck constriction. , 2012, Trends in cell biology.

[32]  Jinxing Lin,et al.  The Signal Transducer NPH3 Integrates the Phototropin1 Photosensor with PIN2-Based Polar Auxin Transport in Arabidopsis Root Phototropism[C][W] , 2012, Plant Cell.

[33]  M. Otegui,et al.  Plant endosomal trafficking pathways. , 2011, Current opinion in plant biology.

[34]  S. Jakobs,et al.  Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane , 2011, Molecular systems biology.

[35]  D. Ren,et al.  BON1 interacts with the protein kinases BIR1 and BAK1 in modulation of temperature-dependent plant growth and cell death in Arabidopsis. , 2011, The Plant journal : for cell and molecular biology.

[36]  A. Audhya,et al.  Association of the Endosomal Sorting Complex ESCRT-II with the Vps20 Subunit of ESCRT-III Generates a Curvature-sensitive Complex Capable of Nucleating ESCRT-III Filaments* , 2011, The Journal of Biological Chemistry.

[37]  C. Schwechheimer,et al.  The Arabidopsis Deubiquitinating Enzyme AMSH3 Interacts with ESCRT-III Subunits and Regulates Their Localization[C][W] , 2011, Plant Cell.

[38]  Scott D Emr,et al.  The ESCRT pathway. , 2011, Developmental cell.

[39]  P. He,et al.  Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity , 2011, Science.

[40]  C. Schwechheimer,et al.  Gibberellin Regulates PIN-FORMED Abundance and Is Required for Auxin Transport–Dependent Growth and Development in Arabidopsis thaliana[C][W] , 2011, Plant Cell.

[41]  C. Curie,et al.  Monoubiquitin-dependent endocytosis of the IRON-REGULATED TRANSPORTER 1 (IRT1) transporter controls iron uptake in plants , 2011, Proceedings of the National Academy of Sciences.

[42]  J. Dacks,et al.  Multivesicular bodies in the enigmatic amoeboflagellate Breviata anathema and the evolution of ESCRT 0 , 2011, Journal of Cell Science.

[43]  T. Fujiwara,et al.  High Boron-induced Ubiquitination Regulates Vacuolar Sorting of the BOR1 Borate Transporter in Arabidopsis thaliana* , 2010, The Journal of Biological Chemistry.

[44]  J. Friml,et al.  Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells , 2010, Proceedings of the National Academy of Sciences.

[45]  A. Shestakova,et al.  Coordination of Substrate Binding and ATP Hydrolysis in Vps4-Mediated ESCRT-III Disassembly , 2010, Molecular biology of the cell.

[46]  M. Hülskamp,et al.  The AAA-type ATPase AtSKD1 contributes to vacuolar maintenance of Arabidopsis thaliana. , 2010, The Plant journal : for cell and molecular biology.

[47]  Dong Yang,et al.  Structural role of the Vps4-Vta1 interface in ESCRT-III recycling. , 2010, Structure.

[48]  T. Baskin,et al.  Gravitropism of Arabidopsis thaliana Roots Requires the Polarization of PIN2 toward the Root Tip in Meristematic Cortical Cells[C][W] , 2010, Plant Cell.

[49]  Weiqiang Qian,et al.  Temperature Modulates Plant Defense Responses through NB-LRR Proteins , 2010, PLoS pathogens.

[50]  Matthew West,et al.  Regulators of Vps4 ATPase Activity at Endosomes Differentially Influence the Size and Rate of Formation of Intralumenal Vesicles , 2010, Molecular biology of the cell.

[51]  Filip Vandenbussche,et al.  Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana , 2010, Development.

[52]  M. Uemura,et al.  Auxin Response in Arabidopsis under Cold Stress: Underlying Molecular Mechanisms[C][W] , 2009, The Plant Cell Online.

[53]  Nathan D. Miller,et al.  Plasticity of Arabidopsis Root Gravitropism throughout a Multidimensional Condition Space Quantified by Automated Image Analysis1[W][OA] , 2009, Plant Physiology.

[54]  S. Grün,et al.  Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem1[W] , 2009, Plant Physiology.

[55]  S. Ameer-Beg,et al.  Essential role of hIST1 in cytokinesis. , 2009, Molecular biology of the cell.

[56]  M. Sliwinski,et al.  The ESCRT-Related CHMP1A and B Proteins Mediate Multivesicular Body Sorting of Auxin Carriers in Arabidopsis and Are Required for Plant Development[W] , 2009, The Plant Cell Online.

[57]  W. Sundquist,et al.  Biochemical analyses of human IST1 and its function in cytokinesis. , 2009, Molecular biology of the cell.

[58]  S. Emr,et al.  Functional Reconstitution of ESCRT-III Assembly and Disassembly , 2009, Cell.

[59]  M. Sauer,et al.  Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting , 2008, Proceedings of the National Academy of Sciences.

[60]  Mark C. Field,et al.  Evolution of the Multivesicular Body ESCRT Machinery; Retention Across the Eukaryotic Lineage , 2008, Traffic.

[61]  J. Glazebrook,et al.  Interplay between MAMP-triggered and SA-mediated defense responses. , 2008, The Plant journal : for cell and molecular biology.

[62]  Rujin Chen,et al.  Light Plays an Essential Role in Intracellular Distribution of Auxin Efflux Carrier PIN2 in Arabidopsis thaliana , 2008, PloS one.

[63]  M. Curtiss,et al.  Ist1 regulates Vps4 localization and assembly. , 2007, Molecular biology of the cell.

[64]  S. Emr,et al.  Novel Ist1-Did2 complex functions at a late step in multivesicular body sorting. , 2007, Molecular biology of the cell.

[65]  P. Masson,et al.  ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. , 2007, The Plant journal : for cell and molecular biology.

[66]  Y. Jaillais,et al.  The Retromer Protein VPS29 Links Cell Polarity and Organ Initiation in Plants , 2007, Cell.

[67]  Nathan D. Miller,et al.  Computer-vision analysis of seedling responses to light and gravity. , 2007, The Plant journal : for cell and molecular biology.

[68]  Nathan D. Miller,et al.  Separating the Roles of Acropetal and Basipetal Auxin Transport on Gravitropism with Mutations in Two Arabidopsis Multidrug Resistance-Like ABC Transporter Genes[W][OA] , 2007, The Plant Cell Online.

[69]  M. Sliwinski,et al.  The Arabidopsis AAA ATPase SKD1 Is Involved in Multivesicular Endosome Function and Interacts with Its Positive Regulator LYST-INTERACTING PROTEIN5[W] , 2007, The Plant Cell Online.

[70]  I. Hwang,et al.  Clathrin-Mediated Constitutive Endocytosis of PIN Auxin Efflux Carriers in Arabidopsis , 2007, Current Biology.

[71]  Matthew West,et al.  Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes , 2006, The Journal of cell biology.

[72]  Kazuo Shinozaki,et al.  MEKK1 Is Required for MPK4 Activation and Regulates Tissue-specific and Temperature-dependent Cell Death in Arabidopsis* , 2006, Journal of Biological Chemistry.

[73]  Y. Jaillais,et al.  AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis , 2006, Nature.

[74]  C. Pieterse,et al.  Significance of inducible defense-related proteins in infected plants. , 2006, Annual review of phytopathology.

[75]  Ben Scheres,et al.  Polar PIN Localization Directs Auxin Flow in Plants , 2006, Science.

[76]  T. Stevens,et al.  Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[77]  M. Hauser,et al.  Exploring the ESCRTing machinery in eukaryotes. , 2006, Trends in plant science.

[78]  D. Eckert,et al.  Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1 , 2006, The Journal of cell biology.

[79]  Jiří Friml,et al.  Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism , 2006, Nature Cell Biology.

[80]  K. Shinozaki,et al.  A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. , 2005, The Plant journal : for cell and molecular biology.

[81]  David A. Morris,et al.  Auxin inhibits endocytosis and promotes its own efflux from cells , 2005, Nature.

[82]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[83]  P. Schulze-Lefert,et al.  RAR1 Positively Controls Steady State Levels of Barley MLA Resistance Proteins and Enables Sufficient MLA6 Accumulation for Effective Resistance , 2004, The Plant Cell Online.

[84]  I. Heiser,et al.  Juvenility of tobacco induced by cytokinin gene introduction decreases susceptibility to Tobacco necrosis virus and confers tolerance to oxidative stress , 2004 .

[85]  E. Lam,et al.  Controlled cell death, plant survival and development , 2004, Nature Reviews Molecular Cell Biology.

[86]  J. Kaplan,et al.  Characterization of Vta1p, a Class E Vps Protein in Saccharomyces cerevisiae* , 2004, Journal of Biological Chemistry.

[87]  A. Nakano,et al.  The Arabidopsis GNOM ARF-GEF Mediates Endosomal Recycling, Auxin Transport, and Auxin-Dependent Plant Growth , 2003, Cell.

[88]  Markus Babst,et al.  Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. , 2002, Developmental cell.

[89]  G. Sandberg,et al.  AUX1 Promotes Lateral Root Formation by Facilitating Indole-3-Acetic Acid Distribution between Sink and Source Tissues in the Arabidopsis Seedling , 2002, The Plant Cell Online.

[90]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

[91]  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.

[92]  A. Murphy,et al.  Multidrug Resistance–like Genes of Arabidopsis Required for Auxin Transport and Auxin-Mediated Development Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010350. , 2001, The Plant Cell Online.

[93]  D. Higgins,et al.  T-Coffee: A novel method for fast and accurate multiple sequence alignment. , 2000, Journal of molecular biology.

[94]  P. Schulze-Lefert,et al.  A Novel Class of Eukaryotic Zinc-Binding Proteins Is Required for Disease Resistance Signaling in Barley and Development in C. elegans , 1999, Cell.

[95]  K. Köhrer,et al.  Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. , 1996, Molecular biology of the cell.

[96]  D. Klessig,et al.  A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. , 1994, The Plant cell.

[97]  E. Spalding.  Diverting the downhill flow of auxin to steer growth during tropisms. , 2013, American journal of botany.

[98]  H. Fu,et al.  IRT 1 DEGRADATION FACTOR 1 , a RING E 3 Ubiquitin Ligase , Regulates the Degradation of IRON-REGULATED TRANSPORTER 1 in Arabidopsis , 2013 .

[99]  J. Adamec,et al.  ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[100]  Zhaohui Xu,et al.  ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. , 2008, Developmental cell.