VPS45 is required for both diffuse and tip growth of Arabidopsis thaliana cells

Mugume, Yosia; Roy, Rahul; Agbemafle, William; Shepard, Gabriella N.; Vue, Yee; Bassham, Diane C.

doi:10.3389/fpls.2023.1120307

VPS45 is required for both diffuse and tip growth of Arabidopsis thaliana cells

Journal Article · Mon Feb 27 00:00:00 EST 2023 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2023.1120307· OSTI ID:1958885

Mugume, Yosia; Roy, Rahul; Agbemafle, William; Shepard, Gabriella N.; Vue, Yee; Bassham, Diane C.

Introduction

VPS45 belongs to the Sec1/Munc18 family of proteins, which interact with and regulate Qa-SNARE function during membrane fusion. We have shown previously that Arabidopsis thaliana VPS45 interacts with the SYP61/SYP41/VTI12 SNARE complex, which locates on the trans -Golgi network (TGN). It is required for SYP41 stability, and it functions in cargo trafficking to the vacuole and in cell expansion. It is also required for correct auxin distribution during gravitropism and lateral root growth.

Results

As vps45 knockout mutation is lethal in Arabidopsis, we identified a mutant, vps45-3 , with a point mutation in the VPS45 gene causing a serine 284-to-phenylalanine substitution. The VPS45-3 protein is stable and maintains interaction with SYP61 and SYP41. However, vps45-3 plants display severe growth defects with significantly reduced organ and cell size, similar to vps45 RNAi transgenic lines that have reduced VPS45 protein levels. Root hair and pollen tube elongation, both processes of tip growth, are highly compromised in vps45-3 . Mutant root hairs are shorter and thicker than those of wild-type plants, and are wavy. These root hairs have vacuolar defects, containing many small vacuoles, compared with WT root hairs with a single large vacuole occupying much of the cell volume. Pollen tubes were also significantly shorter in vps45-3 compared to WT.

Discussion

We thus show that VPS45 is essential for proper tip growth and propose that the observed vacuolar defects lead to loss of the turgor pressure needed for tip growth.

View Journal Article

Research Organization:: Iowa State University, Ames, IA (United States)

Sponsoring Organization:: US National Science Foundation (NSF); USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0014038

OSTI ID:: 1958885

Alternate ID(s):: OSTI ID: 2471902

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 14; ISSN 1664-462X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

References (48)

Vacuolar Staining Methods in Plant Cells Scheuring, David; Schöller, Maria; Kleine-Vehn, Jürgen Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-1902-4_8	book	October 2014
Screening of Mutations by TILLING in Plants Wang, Nian; Shi, Lei Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-1966-6_15	book	October 2014
DNA Barcoding for Plants de Vere, Natasha; Rich, Tim C. G.; Trinder, Sarah A. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-1966-6_8	book	October 2014
Growth and ultrastructure ofArabidopsis root hairs: therhd3 mutation alters vacuole enlargement and tip growth Galway, M. E.; Heckman, J. W.; Schiefelbein, J. W. Planta, Vol. 201, Issue 2 https://doi.org/10.1007/BF01007706	journal	June 1997
Journey to the cell surface—the central role of the trans-Golgi network in plants Gendre, Delphine; Jonsson, Kristoffer; Boutté, Yohann Protoplasma, Vol. 252, Issue 2 https://doi.org/10.1007/s00709-014-0693-1	journal	September 2014
Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic Lippincott-Schwartz, Jennifer; Yuan, Lydia; Tipper, Christopher Cell, Vol. 67, Issue 3 https://doi.org/10.1016/0092-8674(91)90534-6	journal	November 1991
The Mechanisms of Vesicle Budding and Fusion Bonifacino, Juan S.; Glick, Benjamin S. Cell, Vol. 116, Issue 2 https://doi.org/10.1016/S0092-8674(03)01079-1	journal	January 2004
Cell growth: How to grow and where to grow Mathur, J.; Hülskamp, M. Current Biology, Vol. 11, Issue 10 https://doi.org/10.1016/S0960-9822(01)00219-6	journal	May 2001
At the junction of SNARE and SM protein function Carr, Chavela M.; Rizo, Josep Current Opinion in Cell Biology, Vol. 22, Issue 4 https://doi.org/10.1016/j.ceb.2010.04.006	journal	August 2010
YKT6 is a Core Constituent of Membrane Fusion Machineries at the Arabidopsis trans-Golgi Network Chen, Yong; Shin, Yeon-Kyun; Bassham, Diane C. Journal of Molecular Biology, Vol. 350, Issue 1 https://doi.org/10.1016/j.jmb.2005.04.061	journal	July 2005
Polarized growth: maintaining focus on the tip Cole, Rex A.; Fowler, John E. Current Opinion in Plant Biology, Vol. 9, Issue 6 https://doi.org/10.1016/j.pbi.2006.09.014	journal	December 2006
Tethering the assembly of SNARE complexes Hong, WanJin; Lev, Sima Trends in Cell Biology, Vol. 24, Issue 1 https://doi.org/10.1016/j.tcb.2013.09.006	journal	January 2014
Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes Šamaj, Jozef; Müller, Jens; Beck, Martina Trends in Plant Science, Vol. 11, Issue 12 https://doi.org/10.1016/j.tplants.2006.10.002	journal	December 2006
Topological restriction of SNARE-dependent membrane fusion Parlati, Francesco; McNew, James A.; Fukuda, Ryouichi Nature, Vol. 407, Issue 6801 https://doi.org/10.1038/35025076	journal	September 2000
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Chaperoning SNARE assembly and disassembly Baker, Richard W.; Hughson, Frederick M. Nature Reviews Molecular Cell Biology, Vol. 17, Issue 8 https://doi.org/10.1038/nrm.2016.65	journal	June 2016
SNAREs — engines for membrane fusion Jahn, Reinhard; Scheller, Richard H. Nature Reviews Molecular Cell Biology, Vol. 7, Issue 9 https://doi.org/10.1038/nrm2002	journal	August 2006
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313X.1998.00343.x	journal	December 1998
The N-terminal peptide of the syntaxin Tlg2p modulates binding of its closed conformation to Vps45p Furgason, M. L. M.; MacDonald, C.; Shanks, S. G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 34 https://doi.org/10.1073/pnas.0902976106	journal	August 2009
Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants Uemura, T.; Kim, H.; Saito, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1115146109	journal	January 2012
Rabenosyn-5, a Novel Rab5 Effector, Is Complexed with Hvps45 and Recruited to Endosomes through a Fyve Finger Domain Nielsen, Erik; Christoforidis, Savvas; Uttenweiler-Joseph, Sandrine Journal of Cell Biology, Vol. 151, Issue 3 https://doi.org/10.1083/jcb.151.3.601	journal	October 2000
Water Uptake by Growing Cells: An Assessment of the Controlling Roles of Wall Relaxation, Solute Uptake, and Hydraulic Conductance Cosgrove, Daniel J. International Journal of Plant Sciences, Vol. 154, Issue 1 https://doi.org/10.1086/297087	journal	March 1993
AtVPS45 Complex Formation at the trans -Golgi Network Bassham, Diane C.; Sanderfoot, Anton A.; Kovaleva, Valentina Molecular Biology of the Cell, Vol. 11, Issue 7 https://doi.org/10.1091/mbc.11.7.2251	journal	July 2000
SNARE VTI13 plays a unique role in endosomal trafficking pathways associated with the vacuole and is essential for cell wall organization and root hair growth in arabidopsis Larson, Emily R.; Domozych, David S.; Tierney, Mary L. Annals of Botany, Vol. 114, Issue 6 https://doi.org/10.1093/aob/mcu041	journal	April 2014
Vps45p stabilizes the syntaxin homologue Tlg2p and positively regulates SNARE complex formation Bryant, N. J. The EMBO Journal, Vol. 20, Issue 13 https://doi.org/10.1093/emboj/20.13.3380	journal	July 2001
Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana Ueda, T. The EMBO Journal, Vol. 20, Issue 17 https://doi.org/10.1093/emboj/20.17.4730	journal	September 2001
AtVPS45 Is a Positive Regulator of the SYP41/SYP61/VTI12 SNARE Complex Involved in Trafficking of Vacuolar Cargo Zouhar, Jan; Rojo, Enrique; Bassham, Diane C. Plant Physiology, Vol. 149, Issue 4 https://doi.org/10.1104/pp.108.134361	journal	February 2009
High-Throughput Screening for Induced Point Mutations Colbert, Trenton; Till, Bradley J.; Tompa, Rachel Plant Physiology, Vol. 126, Issue 2 https://doi.org/10.1104/pp.126.2.480	journal	June 2001
OSM1/SYP61: A Syntaxin Protein in Arabidopsis Controls Abscisic Acid–Mediated and Non-Abscisic Acid–Mediated Responses to Abiotic Stress Zhu, Jianhua; Gong, Zhizhong; Zhang, Changqing The Plant Cell, Vol. 14, Issue 12 https://doi.org/10.1105/tpc.006981	journal	November 2002
The VTI Family of SNARE Proteins Is Necessary for Plant Viability and Mediates Different Protein Transport Pathways Surpin, Marci; Zheng, Haiyan; Morita, Miyo T. The Plant Cell, Vol. 15, Issue 12 https://doi.org/10.1105/tpc.016121	journal	November 2003
The Arabidopsis Rab GTPase RabA4b Localizes to the Tips of Growing Root Hair Cells[W] Preuss, Mary L.; Serna, Jannie; Falbel, Tanya G. The Plant Cell, Vol. 16, Issue 6 https://doi.org/10.1105/tpc.021634	journal	June 2004
Vacuolar H ⁺ -ATPase Activity Is Required for Endocytic and Secretory Trafficking in Arabidopsis Dettmer, Jan; Hong-Hermesdorf, Anne; Stierhof, York-Dieter The Plant Cell, Vol. 18, Issue 3 https://doi.org/10.1105/tpc.105.037978	journal	February 2006
The cell morphogenesis geneSPIRRIGin Arabidopsis encodes a WD/BEACH domain protein Saedler, Rainer; Jakoby, Marc; Marin, Birger The Plant Journal, Vol. 59, Issue 4 https://doi.org/10.1111/j.1365-313X.2009.03900.x	journal	August 2009
SEC1A is a major Arabidopsis Sec1/Munc18 gene in vesicle trafficking during pollen tube tip growth Beuder, Steven; Lara‐Mondragón, Cecilia; Dorchak, Alexandria The Plant Journal, Vol. 110, Issue 5 https://doi.org/10.1111/tpj.15742	journal	April 2022
Growth Mechanisms in Tip-Growing Plant Cells Rounds, Caleb M.; Bezanilla, Magdalena Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120150	journal	April 2013
The Evolution of Organellar Coat Complexes and Organization of the Eukaryotic Cell Rout, Michael P.; Field, Mark C. Annual Review of Biochemistry, Vol. 86, Issue 1 https://doi.org/10.1146/annurev-biochem-061516-044643	journal	June 2017
Chaperoning SNARE Folding and Assembly Zhang, Yongli; Hughson, Frederick M. Annual Review of Biochemistry, Vol. 90, Issue 1 https://doi.org/10.1146/annurev-biochem-081820-103615	journal	June 2021
The Membrane Fusion Enigma: SNAREs, Sec1/Munc18 Proteins, and Their Accomplices—Guilty as Charged? Rizo, Josep; Südhof, Thomas C. Annual Review of Cell and Developmental Biology, Vol. 28, Issue 1 https://doi.org/10.1146/annurev-cellbio-101011-155818	journal	November 2012
SNARE Protein Structure and Function Ungar, Daniel; Hughson, Frederick M. Annual Review of Cell and Developmental Biology, Vol. 19, Issue 1 https://doi.org/10.1146/annurev.cellbio.19.110701.155609	journal	November 2003
Root Hairs Grierson, Claire; Schiefelbein, John The Arabidopsis Book, Vol. 1 https://doi.org/10.1199/tab.0060	journal	January 2002
Root hair growth: it's a one way street Mendrinna, Amelie; Persson, Staffan F1000Prime Reports, Vol. 7 https://doi.org/10.12703/P7-23	journal	February 2015
Cell Polarity and Patterning by PIN Trafficking through Early Endosomal Compartments in Arabidopsis thaliana Tanaka, Hirokazu; Kitakura, Saeko; Rakusová, Hana PLoS Genetics, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pgen.1003540	journal	May 2013
The Sec1/Munc18 Protein Vps45 Regulates Cellular Levels of Its SNARE Binding Partners Tlg2 and Snc2 in Saccharomyces cerevisiae Shanks, Scott G.; Carpp, Lindsay N.; Struthers, Marion S. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0049628	journal	November 2012
Method for Preparation of Epidermal Imprints Using Agarose Mathur, Jaideep; Koncz, Csaba BioTechniques, Vol. 22, Issue 2 https://doi.org/10.2144/97222bm19	journal	February 1997
Control of Pollen Tube Tip Growth by a Rop GTPase-Dependent Pathway That Leads to Tip-Localized Calcium Influx Li, Hai; Lin, Yakang; Heath, Rachel M. The Plant Cell, Vol. 11, Issue 9 https://doi.org/10.2307/3871050	journal	September 1999
News and Views into the SNARE Complexity in Arabidopsis Kim, Sang-Jin; Brandizzi, Federica Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00028	journal	January 2012
Interactions between plant endomembrane systems and the actin cytoskeleton Wang, Pengwei; Hussey, Patrick J. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00422	journal	June 2015
The Sec1/Munc18 protein Vps45 holds the Qa-SNARE Tlg2 in an open conformation Eisemann, Travis J.; Allen, Frederick; Lau, Kelly eLife, Vol. 9 https://doi.org/10.7554/ELIFE.60724	journal	August 2020

Similar Records

The Sec1/Munc18‐like proteins TgSec1 and TgVps45 play pivotal roles in assembly of the pellicle and sub‐pellicle network in Toxoplasma gondii

Journal Article · Mon Nov 18 19:00:00 EST 2019 · Molecular Microbiology · OSTI ID:1598059

Genetic control of polar cell expansion in Arabidopsis thaliana

Conference · Tue May 01 00:00:00 EDT 1990 · Plant Physiology, Supplement; (USA) · OSTI ID:5627945

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Plant Sciences
SM protein
arabidopsis
endomembrane
root hairs
tip growth
vacuole

VPS45 is required for both diffuse and tip growth of Arabidopsis thaliana cells

Citation Formats

References (48)

Similar Records

Related Subjects