Distinct lytic vacuolar compartments are embedded inside the protein storage vacuole of dry and germinating Arabidopsis thaliana seeds.

Plant cell vacuoles are diverse and dynamic structures. In particular, during seed germination, the protein storage vacuoles are rapidly replaced by a central lytic vacuole enabling rapid elongation of embryo cells. In this study, we investigate the dynamic remodeling of vacuolar compartments during Arabidopsis seed germination using immunocytochemistry with antibodies against tonoplast intrinsic protein (TIP) isoforms as well as proteins involved in nutrient mobilization and vacuolar acidification. Our results confirm the existence of a lytic compartment embedded in the protein storage vacuole of dry seeds, decorated by γ-TIP, the vacuolar proton pumping pyrophosphatase (V-PPase) and the metal transporter NRAMP4. They further indicate that this compartment disappears after stratification. It is then replaced by a newly formed lytic compartment, labeled by γ-TIP and V-PPase but not AtNRAMP4, which occupies a larger volume as germination progresses. Altogether, our results indicate the successive occurrence of two different lytic compartments in the protein storage vacuoles of germinating Arabidopsis cells. We propose that the first one corresponds to globoids specialized in mineral storage and the second one is at the origin of the central lytic vacuole in these cells.

[1]  L. Staehelin,et al.  Protein Storage Vacuoles Are Transformed into Lytic Vacuoles in Root Meristematic Cells of Germinating Seedlings by Multiple, Cell Type-Specific Mechanisms1[W] , 2011, Plant Physiology.

[2]  Hideyuki Takahashi,et al.  MAG4/Atp115 is a golgi-localized tethering factor that mediates efficient anterograde transport in Arabidopsis. , 2010, Plant & cell physiology.

[3]  Paul R. Hunter,et al.  In vivo imaging of the tonoplast intrinsic protein family in Arabidopsis roots , 2009, BMC Plant Biology.

[4]  D. Luu,et al.  A look inside: localization patterns and functions of intracellular plant aquaporins. , 2009, The New phytologist.

[5]  T. Zank,et al.  The BURP domain protein AtUSPL1 of Arabidopsis thaliana is destined to the protein storage vacuoles and overexpression of the cognate gene distorts seed development , 2009, Plant Molecular Biology.

[6]  Dominique Thomas,et al.  Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles , 2009, Plant Molecular Biology.

[7]  A. Nakano,et al.  A SNARE Complex Unique to Seed Plants Is Required for Protein Storage Vacuole Biogenesis and Seed Development of Arabidopsis thaliana[W][OA] , 2008, The Plant Cell Online.

[8]  D. Robinson,et al.  Multiple Vacuoles in Plant Cells: Rule or Exception? , 2008, Traffic.

[9]  Hideyuki Takahashi,et al.  A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[10]  D. Robinson,et al.  Newly Formed Vacuoles in Root Meristems of Barley and Pea Seedlings Have Characteristics of Both Protein Storage and Lytic Vacuoles1[W][OA] , 2007, Plant Physiology.

[11]  Paul R. Hunter,et al.  Fluorescent Reporter Proteins for the Tonoplast and the Vacuolar Lumen Identify a Single Vacuolar Compartment in Arabidopsis Cells1[W] , 2007, Plant Physiology.

[12]  D. Robinson,et al.  Protein Mobilization in Germinating Mung Bean Seeds Involves Vacuolar Sorting Receptors and Multivesicular Bodies1[W][OA] , 2007, Plant Physiology.

[13]  Hideyuki Takahashi,et al.  Arabidopsis Vacuolar Sorting Mutants (green fluorescent seed) Can Be Identified Efficiently by Secretion of Vacuole-Targeted Green Fluorescent Protein in Their Seeds[W][OA] , 2007, The Plant Cell Online.

[14]  F. Cordelières,et al.  A guided tour into subcellular colocalization analysis in light microscopy , 2006, Journal of microscopy.

[15]  M. Maeshima,et al.  Vacuolar transporters and their essential role in plant metabolism. , 2006, Journal of experimental botany.

[16]  J. Browse,et al.  A role for caleosin in degradation of oil-body storage lipid during seed germination. , 2006, The Plant journal : for cell and molecular biology.

[17]  O. Foresti,et al.  Overexpression of the Arabidopsis Syntaxin PEP12/SYP21 Inhibits Transport from the Prevacuolar Compartment to the Lytic Vacuole in Vivo[W] , 2006, The Plant Cell Online.

[18]  K. Rockland,et al.  Improved Golgi-like Visualization in Retrogradely Projecting Neurons after EGFP-Adenovirus Infection in Adult Rat and Monkey , 2006, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[19]  Jan Traas,et al.  The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins , 2006, Journal of Cell Science.

[20]  S. Thomine,et al.  Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron , 2005, The EMBO journal.

[21]  A. Vitale,et al.  Sorting of proteins to storage vacuoles: how many mechanisms? , 2005, Trends in plant science.

[22]  P. Dupree,et al.  A unique family of proteins associated with internalized membranes in protein storage vacuoles of the Brassicaceae. , 2004, The Plant journal : for cell and molecular biology.

[23]  B. Satiat-Jeunemaitre,et al.  The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells , 2004, Journal of Cell Science.

[24]  N. Raikhel,et al.  Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. , 2001, Molecular biology of the cell.

[25]  J. Tiedemann,et al.  Different functions of vicilin and legumin are reflected in the histopattern of globulin mobilization during germination of vetch (Vicia sativa L.) , 2000, Planta.

[26]  T. Phillips,et al.  Tonoplast Intrinsic Protein Isoforms as Markers for Vacuolar Functions , 1999, Plant Cell.

[27]  J. Neuhaus,et al.  Sorting of proteins to vacuoles in plant cells , 1998, Plant Molecular Biology.

[28]  T. Kirchhausen,et al.  A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  N. Raikhel,et al.  The syntaxin homolog AtPEP12p resides on a late post-Golgi compartment in plants. , 1997, The Plant cell.

[30]  T. Rausch,et al.  The 32 kDa tonoplast polypeptide Di associated with the V0‐type H+‐ATPase of Mesembryanthemum crystallinum L. in the CAM state: A proteolytically processed subunit B? , 1996, FEBS letters.

[31]  C. Stanley,et al.  Plant Cells Contain Two Functionally Distinct Vacuolar Compartments , 1996, Cell.

[32]  M. Nishimura,et al.  Molecular characterization of proteins in protein-body membrane that disappear most rapidly during transformation of protein bodies into vacuoles. , 1995, The Plant journal : for cell and molecular biology.

[33]  M. Nishimura,et al.  Accumulation of Vacuolar H+-Pyrophosphatase and H+-ATPase during Reformation of the Central Vacuole in Germinating Pumpkin Seeds , 1994, Plant physiology.

[34]  E. Herman,et al.  Vegetative and Seed-Specific Forms of Tonoplast Intrinsic Protein in the Vacuolar Membrane of Arabidopsis thaliana. , 1992, Plant physiology.

[35]  R. J. Poole,et al.  Radiation-inactivation analysis of vacuolar H(+)-ATPase and H(+)-pyrophosphatase from Beta vulgaris L. Functional sizes for substrate hydrolysis and for H+ transport. , 1992, The Biochemical journal.

[36]  J. Torrey.  Plant Cell Biology , 1969, Nature.

[37]  J. Botto,et al.  The plant cell , 2007, Plant Molecular Biology Reporter.

[38]  M. Freeman.  A look inside. , 2007, Neuron Glia Biology.

[39]  P. A. Rea,et al.  The protein storage vacuole: a unique compound organelle , 2001 .

[40]  Andrew M. Parsons,et al.  Fluorescent probes for living plant cells , 2022 .