Membrane contact sites (MCSs) are interorganellar connections that allow for the direct exchange of molecules, such as lipids or Ca2+ between organelles, but can also serve to tether organelles at specific locations within cells. Here, we identified and characterized three proteins of Arabidopsis thaliana that form a lipid droplet (LD)-plasma membrane (PM) tethering complex in plant cells, namely LD-localized SEED LD PROTEIN (SLDP) 1 and SLDP2 and PM-localized LD-PLASMA MEMBRANE ADAPTOR (LIPA). Using proteomics and different protein-protein interaction assays, we show that both SLDPs associate with LIPA. Disruption of either SLDP1 and SLDP2 expression, or that of LIPA, leads to an aberrant clustering of LDs in Arabidopsis seedlings. Ectopic co-expression of one of the SLDPs with LIPA is sufficient to reconstitute LD-PM tethering in Nicotiana tabacum pollen tubes, a cell type characterized by dynamically moving LDs in the cytosolic streaming. Furthermore, confocal laser scanning microscopy revealed both SLDP2.1 and LIPA to be enriched at LD-PM contact sites in seedlings. These and other results suggest that SLDP and LIPA interact to form a tethering complex that anchors a subset of LDs to the PM during post-germinative seedling growth in Arabidopsis.

Albrecht von Haller Institute for Plant Sciences and Göttingen Center for Molecular Biosciences Department of Plant Biochemistry University of Göttingen Göttingen Germany

Albrecht von Haller Institute for Plant Sciences and Göttingen Center for Molecular Biosciences Molecular Biology of Plant Microbe Interactions Research Group University of Göttingen Göttingen Germany

Department of Molecular and Cellular Biology University of Guelph Guelph ON N1G 2W1 Canada

Electron Microscopy Core Facility Heidelberg University Heidelberg Germany

Göttingen Center for Molecular Biosciences University of Göttingen Göttingen Germany

Institute for Microbiology and Genetics and Göttingen Center for Molecular Biosciences and Service Unit LCMS Protein Analytics Department for Molecular Microbiology and Genetics University of Göttingen Göttingen Germany

Institute of Experimental Botany of the Czech Academy of Sciences Prague Czech Republic

Institute of Plant Biology and Biotechnology Green Biotechnology University of Münster Münster Germany

Zobrazit více v PubMed

Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX  1–2: 19–25

Akdel M, Pires DEV, Porta Pardo E, Jänes J, Zalevsky AO, Mészáros B, Bryant P, Good LL, Laskowski RA, Pozzati G, et al. (2021). A Structural Biology Community Assessment of AlphaFold 2 Applications. Cold Spring Harbor Laboratory, New York PubMed

Bae S, Park J, Kim JS (2014) Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics  30: 1473–1475 PubMed PMC

Baillie AL, Falz AL, Müller-Schüssele SJ, Sparkes I (2020) It started with a kiss: monitoring organelle interactions and identifying membrane contact site components in plants. Front Plant Sci  11: 517. PubMed PMC

Berardini TZ, Reiser L, Li D, Mezheritsky Y, Muller R, Strait E, Huala E (2015) The Arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome. Genesis  53: 474–485 PubMed PMC

Bewley J (1997) Seed germination and dormancy. Plant Cell  9: 1055–1066 PubMed PMC

Bohnert M (2020) Tethering fat: tethers in lipid droplet contact sites. Contact  3: 251525642090814

Cai Y, Goodman JM, Pyc M, Mullen RT, Dyer JM, Chapman KD (2015) Arabidopsis SEIPIN proteins modulate triacylglycerol accumulation and influence lipid droplet proliferation. Plant Cell  27: 2616–2636 PubMed PMC

Chang DK, Cheng SF, Trivedi VD, Lin KL (1999) Proline affects oligomerization of a coiled coil by inducing a kink in a long helix. J Struct Biol  128: 270–279 PubMed

Cheng HY, Schiavone AP, Smithgall TE (2001) A point mutation in the N-terminal coiled-coil domain releases c-Fes tyrosine kinase activity and survival signaling in myeloid leukemia cells. Mol Cell Biol  21: 6170–6180 PubMed PMC

Cheng M-C, Hsieh E-J, Chen J-H, Chen H-Y, Lin T-P (2012) Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol  158: 363–375 PubMed PMC

Cockcroft S, Raghu P (2018) Phospholipid transport protein function at organelle contact sites. Curr Opin Cell Biol  53: 52–60 PubMed PMC

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J  16: 735–743 PubMed

Corradi V, Sejdiu BI, Mesa-Galloso H, Abdizadeh H, Noskov SY, Marrink SJ, Tieleman DP (2019) Emerging diversity in lipid–protein interactions. Chem Rev  119: 5775–5848 PubMed PMC

Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics  13: 2513–2526 PubMed PMC

Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol  26: 1367–1372 PubMed

Cui S, Hayashi Y, Otomo M, Mano S, Oikawa K, Hayashi M, Nishimura M (2016) Sucrose production mediated by lipid metabolism suppresses the physical interaction of peroxisomes and oil bodies during germination of Arabidopsis thaliana. J Biol Chem  291: 19734–19745 PubMed PMC

Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol  133: 462–469 PubMed PMC

Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol  139: 5–17 PubMed PMC

de Vries J, Ischebeck T (2020) Ties between stress and lipid droplets pre-date seeds. Trends Plant Sci  25: 1203–1214 PubMed

Eastmond PJ (2006) SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell  18: 665–675 PubMed PMC

Eisenberg-Bord M, Shai N, Schuldiner M, Bohnert M (2016) A tether is a tether is a tether: tethering at membrane contact sites. Dev Cell  39: 395–409 PubMed

Esnay N, Dyer JM, Mullen RT, Chapman KD (2020) Lipid droplet–peroxisome connections in plants. Contact  3: 251525642090876

Fan J, Yu L, Xu C (2017) A central role for triacylglycerol in membrane lipid breakdown, fatty acid β-oxidation, and plant survival under extended darkness. Plant Physiol  174: 1517–1530 PubMed PMC

Freyre CAC, Rauher PC, Ejsing CS, Klemm RW (2019) MIGA2 links mitochondria, the ER, and lipid droplets and promotes de novo lipogenesis in adipocytes. Mol Cell  76: 811–825.e14 PubMed

Gao Q, Goodman JM (2015) The lipid droplet—a well-connected organelle. Front Cell Dev Biol  3: 1–12 PubMed PMC

Gautier R, Douguet D, Antonny B, Drin G (2008) HELIQUEST: a web server to screen sequences with specific α-helical properties. Bioinformatics  24: 2101–2102 PubMed

Geltinger F, Tevini J, Briza P, Geiser A, Bischof J, Richter K, Felder T, Rinnerthaler M (2020) The transfer of specific mitochondrial lipids and proteins to lipid droplets contributes to proteostasis upon stress and aging in the eukaryotic model system Saccharomyces cerevisiae. GeroScience  42: 19–38 PubMed PMC

Gidda SK, Park S, Pyc M, Yurchenko O, Cai Y, Wu P, Andrews DW, Chapman KD, Dyer JM, Mullen RT (2016) Lipid droplet-associated proteins (LDAPs) are required for the dynamic regulation of neutral lipid compartmentation in plant cells. Plant Physiol. 170: 2052–2071 PubMed PMC

Gietz RD, Schiestl RH (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc  2: 31–34 PubMed

Greer MS, Cai Y, Gidda SK, Esnay N, Kretzschmar FK, Seay D, McClinchie E, Ischebeck T, Mullen RT, Dyer JM, et al. (2020). SEIPIN isoforms interact with the membrane-tethering protein VAP27-1 for lipid droplet formation. Plant Cell  32: 2932–2950 PubMed PMC

Hariri H, Speer N, Bowerman J, Rogers S, Fu G, Reetz E, Datta S, Feathers JR, Ugrankar R, Nicastro D, et al. (2019) Mdm1 maintains endoplasmic reticulum homeostasis by spatially regulating lipid droplet biogenesis. J Cell Biol  218: 1319–1334 PubMed PMC

Hillmer S, Viotti C, Robinson DG (2012) An improved procedure for low-temperature embedding of high-pressure frozen and freeze-substituted plant tissues resulting in excellent structural preservation and contrast. J Microsc  247: 43–47 PubMed

Horn PJ, Chapman KD, Ischebeck T (2021) Isolation of lipid droplets for protein and lipid analysis. Methods Mol Biol  2295: 295–320 PubMed

Hornung E, Pernstich C, Feussner I (2002) Formation of conjugated Δ11 Δ13-double bonds by Δ12-linoleic acid (1,4)-acyl-lipid-desaturase in pomegranate seeds. Eur J Biochem  269: 4852–4859 PubMed

Hugenroth M, Bohnert M (2020) Come a little bit closer! Lipid droplet-ER contact sites are getting crowded. Biochim Biophys Acta-Mol Cell Res  1867: 118603. PubMed

Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph  14: 33–38 PubMed

Ischebeck T, Krawczyk HE, Mullen RT, Dyer JM, Chapman KD (2020) Lipid droplets in plants and algae: distribution, formation, turnover and function. Semin Cell Dev Biol  108: 82–93 PubMed

Johnson MR, Stephenson RA, Ghaemmaghami S, Welte MA (2018) Developmentally regulated H2AV buffering via dynamic sequestration to lipid droplets in Drosophila embryos. eLife  7: 1–28 PubMed PMC

Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, et al. (2021) Highly accurate protein structure prediction with AlphaFold. Nature  596: 583–589 PubMed PMC

Jurrus E, Engel D, Star K, Monson K, Brandi J, Felberg LE, Brookes DH, Wilson L, Chen J, Liles K, et al. (2018) Improvements to the APBS biomolecular solvation software suite. Protein Sci  27: 112–128 PubMed PMC

Kang B-H, Anderson CT, Arimura S-I, Bayer E, Bezanilla M, Botella MA, Brandizzi F, Burch-Smith TM, Chapman KD, Dünser K, et al. (2021) A glossary of plant cell structures: current insights and future questions. Plant Cell  34: 10–52 PubMed PMC

Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA (2016) A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J  88: 1058–1070 PubMed

Kory N, Farese RV, Walther TC (2016) Targeting fat: mechanisms of protein localization to lipid droplets. Trends Cell Biol  26: 535–546 PubMed PMC

Kretzschmar FK, Doner NM, Krawczyk HE, Scholz P, Schmitt K, Valerius O, Braus GH, Mullen RT, Ischebeck T (2020) Identification of low-abundance lipid droplet proteins in seeds and seedlings. Plant Physiol  182: 1326–1345 PubMed PMC

Kretzschmar FK, Mengel LA, Müller AO, Schmitt K, Blersch KF, Valerius O, Braus GH, Ischebeck T (2018) PUX10 is a lipid droplet-localized scaffold protein that interacts with CELL DIVISION CYCLE48 and is involved in the degradation of lipid droplet proteins. Plant Cell  30: 2137–2160 PubMed PMC

Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol  157: 105–132 PubMed

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods  25: 402–408 PubMed

Lundquist PK, Shivaiah KK, Espinoza-Corral R (2020) Lipid droplets throughout the evolutionary tree. Prog Lipid Res  78: 101029. PubMed

Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science  252: 1162–1164 PubMed

Marrink SJ, Corradi V, Souza PCT, Ingólfsson HI, Tieleman DP, Sansom MSP (2019) Computational modeling of realistic cell membranes. Chem Rev  119: 6184–6226 PubMed PMC

Mier P, Alanis-Lobato G, Andrade-Navarro MA (2017) Protein-protein interactions can be predicted using coiled coil co-evolution patterns. J Theor Biol  412: 198–203 PubMed

Miquel M, Browse J (1992) Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis: Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. J Biol Chem  267: 1502–1509 PubMed

Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M (2021) ColabFold - Making Protein Folding Accessible to All. BioRxiv. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY PubMed PMC

Muliyil S, Levet C, Düsterhöft S, Dulloo I, Cowley SA, Freeman M (2020) ADAM 17‐triggered TNF signalling protects the ageing Drosophila retina from lipid droplet‐mediated degeneration. EMBO J  39: e104415. PubMed PMC

Müller AO, Blersch KF, Gippert AL, Ischebeck T (2017) Tobacco pollen tubes - a fast and easy tool for studying lipid droplet association of plant proteins. Plant J  89: 1055–1064 PubMed

Müller AO, Ischebeck T (2018) Characterization of the enzymatic activity and physiological function of the lipid droplet-associated triacylglycerol lipase AtOBL1. New Phytol  217: 1062–1076 PubMed

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant  15: 473–497

Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J  41: 697–709 PubMed

Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol  48: 443–453 PubMed

Noack LC, Jaillais Y (2020) Functions of anionic lipids in plants. Annu Rev Plant Biol  71: 71–102 PubMed

Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol  302: 205–217 PubMed

Olarte M-J,, Swanson JMJ,, Walther TC,, Farese RV (2022) The CYTOLD and ERTOLD pathways for lipid droplet–protein targeting. Trends Biochem Sci 47: 39–51 PubMed PMC

Olzmann JA, Carvalho P (2019) Dynamics and functions of lipid droplets. Nat Rev Mol Cell Biol  20: 137–155 PubMed PMC

Park J, Bae S, Kim JS (2015) Cas-Designer: a web-based tool for choice of CRISPR-Cas9 target sites. Bioinformatics  31: 4014–4016 PubMed

Petrie JR, Shrestha P, Liu Q, Mansour MP, Wood CC, Zhou XR, Nichols PD, Green AG, Singh SP (2010) Rapid expression of transgenes driven by seed-specific constructs in leaf tissue: DHA production. Plant Methods  6: 8. PubMed PMC

Prinz WA, Toulmay A, Balla T (2020) The functional universe of membrane contact sites. Nat Rev Mol Cell Biol  21: 7–24 PubMed PMC

Pyc M, Gidda SK, Seay D, Esnay N, Kretzschmar FK, Cai Y, Doner NM, Greer MS, Hull JJ, Coulon D, et al. (2021). LDIP cooperates with SEIPIN and LDAP to facilitate lipid droplet biogenesis in Arabidopsis. Plant Cell  33: 3076–3103 PubMed PMC

Pyc M, Cai Y, Gidda SK, Yurchenko O, Park S, Kretzschmar FK, Ischebeck T, Valerius O, Braus GH, Chapman KD, et al. (2017) Arabidopsis lipid droplet-associated protein (LDAP) – interacting protein (LDIP) influences lipid droplet size and neutral lipid homeostasis in both leaves and seeds. Plant J  92: 1182–1201 PubMed

Rakotonirina-Ricquebourg R,, Costa V,, Teixeira V (2022) Hello from the other side: Membrane contact of lipid droplets with other organelles and subsequent functional implications. Prog Lipid Res  85: 101141. PubMed

Read SM, Clarke AE, Bacic A (1993) Stimulation of growth of cultured Nicotiana tabacum W 38 pollen tubes by poly(ethylene glycol) and Cu(II) salts. Protoplasma  177: 1–14

Richardson LGL, Howard ASM, Khuu N, Gidda SK, McCartney A, Morphy BJ, Mullen RT (2011) Protein–protein interaction network and subcellular localization of the Arabidopsis thaliana ESCRT machinery. Front Plant Sci  2: 20. PubMed PMC

Rossini M, Pizzo P, Filadi R (2020) Better to keep in touch: investigating inter-organelle cross-talk. FEBS J  288: 740–755 PubMed

Rotsch AH, Kopka J, Feussner I, Ischebeck T (2017) Central metabolite and sterol profiling divides tobacco male gametophyte development and pollen tube growth into eight metabolic phases. Plant J  92: 129–146 PubMed

Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, Eliceiri KW (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics  18: 1–26. PubMed PMC

Rylott EL, Rogers CA, Gilday AD, Edgell T, Larson TR, Graham IA (2003) Arabidopsis mutants in short- and medium-chain acyl-CoA oxidase activities accumulate acyl-CoAs and reveal that fatty acid β-oxidation is essential for embryo development. J Biol Chem  278: 21370–21377 PubMed

Salo VT, Li S, Vihinen H, Holtta-Vuori M, Szkalisity A, Horvath P, Belevich I, Peranen J, Thiele C, Somerharju P, et al. (2019). Seipin facilitates triglyceride flow to lipid droplet and counteracts droplet ripening via endoplasmic reticulum contact. Dev Cell  50: 478–493.e9 PubMed

Schaffer JE (2003) Lipotoxicity: when tissues overeat. Curr Opin Lipidol  14: 281–287 PubMed

Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, et al. (2008). Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell  20: 3374–3388 PubMed PMC

Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, Wenk MR, De Camilli P, Reinisch KM (2014) Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature  510: 552–555 PubMed PMC

Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet  37: 501–506 PubMed

Schuldiner M, Bohnert M (2017) A different kind of love – lipid droplet contact sites. Biochim Biophys Acta - Mol Cell Biol Lipids  1862: 1188–1196 PubMed

Shai N, Yifrach E, van Roermund CWT, Cohen N, Bibi C, Ijlst L, Cavellini L, Meurisse J, Schuster R, Zada L, et al. (2018). Systematic mapping of contact sites reveals tethers and a function for the peroxisome-mitochondria contact. Nat Commun  9: 1761. PubMed PMC

Shai N, Schuldiner M, Zalckvar E (2016) No peroxisome is an island - peroxisome contact sites. Biochim Biophys Acta - Mol Cell Res  1863: 1061–1069 PubMed PMC

Shockey JM, Gidda SK, Chapital DC, Kuan JC, Dhanoa PK, Bland JM, Rothstein SJ, Mullen RT, Dyer JM (2006) Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell  18: 2294–2313 PubMed PMC

Siao W, Wang P, Voigt B, Hussey PJ, Baluska F (2016) Arabidopsis SYT1 maintains stability of cortical endoplasmic reticulum networks and VAP27-1-enriched endoplasmic reticulum-plasma membrane contact sites. J Exp Bot  67: 6161–6171 PubMed PMC

Souza PCT, Alessandri R, Barnoud J, Thallmair S, Faustino I, Grünewald F, Patmanidis I, Abdizadeh H, Bruininks BMH, Wassenaar TA, et al. (2021). Martini 3: a general purpose force field for coarse-grained molecular dynamics. Nat Methods  18: 382–388 PubMed

Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc  1: 2019–2025 PubMed

Srinivasan S, Zoni V, Vanni S (2021) Estimating the accuracy of the MARTINI model towards the investigation of peripheral protein–membrane interactions. Faraday Discuss  232: 131–148 PubMed

Sui X, Arlt H, Brock KP, Lai ZW, DiMaio F, Marks DS, Liao M, Farese RV, Walther TC (2018) Cryo–electron microscopy structure of the lipid droplet–formation protein seipin. J Cell Biol  217: jcb.201809067 PubMed PMC

Thiam AR, Beller M (2017) The why, when and how of lipid droplet diversity. J Cell Sci  130: 315–324 PubMed

Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev  5: 496–507 PubMed

Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods  13: 731–740 PubMed

Ugrankar R, Bowerman J, Hariri H, Chandra M, Chen K, Bossanyi MF, Datta S, Rogers S, Eckert KM, Vale G, et al. (2019) Drosophila snazarus regulates a lipid droplet population at plasma membrane-droplet contacts in adipocytes. Dev Cell  50: 557–572.e5 PubMed PMC

Valm AM, Cohen S, Legant WR, Melunis J, Hershberg U, Wait E, Cohen AR, Davidson MW, Betzig E, Lippincott-Schwartz J (2017) Applying systems-level spectral imaging and analysis to reveal the organelle interactome. Nature  546: 162–167 PubMed PMC

Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A, et al. (2022). AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res  50: D439–D444 PubMed PMC

Velázquez AP, Tatsuta T, Ghillebert R, Drescher I, Graef M (2016) Lipid droplet-mediated ER homeostasis regulates autophagy and cell survival during starvation. J Cell Biol  212: 621–631 PubMed PMC

Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, Dianes JA, Sun Z, Farrah T, Bandeira N, et al. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol  32: 223–226. PubMed PMC

Waese J, Fan J, Pasha A, Yu H, Fucile G, Shi R, Cumming M, Kelley LA, Sternberg MJ, Krishnakumar V, et al. (2017). ePlant: visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell  29: 1806–1821 PubMed PMC

Wang Z-P, Xing H-L, Dong L, Zhang H-Y, Han C-Y, Wang X-C, Chen Q-J (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol  16: 144. PubMed PMC

Wassenaar TA, Ingólfsson HI, Böckmann RA, Tieleman DP, Marrink SJ (2015) Computational lipidomics with insane : a versatile tool for generating custom membranes for molecular simulations. J Chem Theory Comput  11: 2144–2155 PubMed

Welte MA, Gould AP (2017) Lipid droplet functions beyond energy storage. Biochim Biophys Acta - Mol Cell Biol Lipids  1862: 1260–1272 PubMed PMC

Wilfling F, Wang H, Haas JT, Krahmer N, Gould TJ, Uchida A, Cheng JX, Graham M, Christiano R, Fröhlich F, et al. (2013). Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev Cell  24: 384–399 PubMed PMC

Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007). An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One  2: 1–12 PubMed PMC

Xie Y, Zheng Y, Li H, Luo X, He Z, Cao S, Shi Y, Zhao Q, Xue Y, Zuo Z, et al. (2016) GPS-Lipid: a robust tool for the prediction of multiple lipid modification sites. Sci. Rep.  6: 1–9. PubMed PMC

Xing H-L, Dong L, Wang Z-P, Zhang H-Y, Han C-Y, Liu B, Wang X-C, Chen Q-J (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol  14: 327. PubMed PMC

Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell  20: 3389–3404 PubMed PMC

Yang HJ, Hsu CL, Yang JY, Yang WY (2012) Monodansylpentane as a blue-fluorescent lipid-droplet marker for multi-color live-cell imaging. PLoS One  7 PubMed PMC

Yang Y, Benning C (2018) Functions of triacylglycerols during plant development and stress. Curr Opin Biotechnol  49: 191–198 PubMed

Yu H, Liu Y, Gulbranson DR, Paine A, Rathore SS, Shen J (2016) Extended synaptotagmins are Ca2+-dependent lipid transfer proteins at membrane contact sites. Proc Natl Acad Sci USA  113: 4362–4367 PubMed PMC

Yu J, Kang L, Li Y, Wu C, Zheng C, Liu P, Huang J (2021) RING finger protein RGLG1 and RGLG2 negatively modulate MAPKKK18 mediated drought stress tolerance in Arabidopsis. J Integr Plant Biol  63: 484–493 PubMed

Zang J, Zhang T, Hussey PJ, Wang P (2020) Light microscopy of the endoplasmic reticulum–membrane contact sites in plants. J Microsc  280: 134–139 PubMed