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Vacuolar membrane structures and their roles in plant–pathogen interactions

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Short review focussing on the role and targeting of vacuolar substructure in plant immunity and pathogenesis.

Abstract

Plants lack specialized immune cells, therefore each plant cell must defend itself against invading pathogens. A typical plant defense strategy is the hypersensitive response that results in host cell death at the site of infection, a process largely regulated by the vacuole. In plant cells, the vacuole is a vital organelle that plays a central role in numerous fundamental processes, such as development, reproduction, and cellular responses to biotic and abiotic stimuli. It shows divergent membranous structures that are continuously transforming. Recent technical advances in visualization and live-cell imaging have significantly altered our view of the vacuolar structures and their dynamics. Understanding the active nature of the vacuolar structures and the mechanisms of vacuole-mediated defense responses is of great importance in understanding plant-pathogen interactions. In this review, we present an overview of the current knowledge about the vacuole and its internal structures, as well as their role in plant–microbe interactions. There is so far limited information on the modulation of the vacuolar structures by pathogens, but recent research has identified the vacuole as a possible target of microbial interference.

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References

  • Ahmad et al (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol 157:317–327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    CAS  PubMed  Google Scholar 

  • Banasiak J, Biała W, Staszków A, Swarcewicz B, Kępczyńska E, Figlerowicz M, Jasiński M (2013) A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. J Exp Bot 64:1005–1015

    CAS  PubMed  Google Scholar 

  • Beebo A et al (2009) Life with and without AtTIP1; 1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles. Plant Mol Biol 70:193–209

    CAS  PubMed  Google Scholar 

  • Bewley JD, Black M (1994) Seeds: physiology of development and germination, 2nd edn. Plenum Press, New York

    Google Scholar 

  • Boller T, Kende H (1979) Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol 63:1123–1132

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bottanelli F, Foresti O, Hanton S, Denecke J (2011) Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell 23:3007–3025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boursiac Y, Chen S, Luu D-T, Sorieul M, Van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bowles DJ, Marcus SE, Pappin D, Findlay J, Eliopoulos E, Maycox PR, Burgess J (1986) Posttranslational processing of concanavalin A precursors in jackbean cotyledons. J Cell Biol 102:1284–1297

    CAS  PubMed  Google Scholar 

  • Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu CH, Cano LM, Kamoun S (2015) Rerouting of plant late endocytic trafficking toward a pathogen interface. Traffic 16:204–226

    CAS  PubMed  Google Scholar 

  • Broekaert WF, Terras FRG, Cammue BPA (2000) Induced and preformed antimicrobial proteins. In: Slusarenko AJ, Fraser RSS, van Loon LC (eds) Mechanisms of resistance to plant diseases. Kluwer Academic Publishers, Dordrecht, pp 371–477

    Google Scholar 

  • Caillaud MC, Piquerez SJ, Fabro G, Steinbrenner J, Ishaque N, Beynon J, Jones JD (2012) Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J 69:252–265

    CAS  PubMed  Google Scholar 

  • De Angeli A, Monachello D, Ephritikhine G, Frachisse J, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939

    PubMed  Google Scholar 

  • Emans N, Zimmermann S, Fischer R (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. Plant Cell 14:71–86

    CAS  PubMed  PubMed Central  Google Scholar 

  • Endler A et al (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141:196–207

    CAS  PubMed  PubMed Central  Google Scholar 

  • Epimashko S, Meckel T, Fischer-Schliebs E, Lüttge U, Thiel G (2004) Two functionally different vacuoles for static and dynamic purposes in one plant mesophyll leaf cell. Plant J 37:294–300

    PubMed  Google Scholar 

  • Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K (2003) High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15:1507–1523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foresti O, Luis L, Denecke J (2006) Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 18:2275–2293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman BC, Beattie GA (2008) An overview of plant defenses against pathogens and herbivores. Plant Health Instr 149

  • Fuji K, Shirakawa M, Shimono Y, Kunieda T, Fukao Y, Koumoto Y, Takahashi H, Hara-Nishimura I, Shimada T (2016) The adaptor complex AP-4 regulates vacuolar protein sorting at trans-Golgi network by interacting with VACUOLAR SORTING RECEPTOR 1. Plant Physiol 170:211–219

    CAS  PubMed  Google Scholar 

  • Gaffal KP, Friedrichs GJ, El-Gammal S (2007) Ultrastructural evidence for a dual function of the phloem and programmed cell death in the floral nectary of Digitalis purpurea. Ann Bot 99:593–607

    PubMed  PubMed Central  Google Scholar 

  • Gao C, Zhao Q, Jiang L (2015) Vacuoles protect plants from high magnesium stress. Proc Natl Acad Sci USA 112:2931–2932

    CAS  PubMed  Google Scholar 

  • Gattolin S, Sorieul M, Hunter PR, Khonsari RH, Frigerio L (2009) In vivo imaging of the tonoplast intrinsic protein family in Arabidopsis roots. BMC Plant Biol 9:133

    PubMed  PubMed Central  Google Scholar 

  • Grolig F, Pierson ES (2000) Cytoplasmic streaming: from flow to track. In: Actin: a dynamic framework for multiple plant cell functions, vol 89. Springer, New York, pp 165–190

    Google Scholar 

  • Grotewold E (2006) The genetics and biochemistry of floral pigments. Ann Rev Plant Biol 57:761–780

    CAS  Google Scholar 

  • Grubb CD, Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100

    CAS  PubMed  Google Scholar 

  • Gunawardena AH (2007) Programmed cell death and tissue remodelling in plants. J Exp Bot 59:445–451

    PubMed  Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Ann Rev Plant Biol 57:303–333

    CAS  Google Scholar 

  • Han SW, Alonso JM, Rojas-Pierce M (2015) REGULATOR OF BULB BIOGENESIS1 (RBB1) is involved in vacuole bulb formation in Arabidopsis. PLoS ONE 10:e0125621

    PubMed  PubMed Central  Google Scholar 

  • Handrick V et al (2016) Biosynthesis of 8-o-methylated benzoxazinoid defense compounds in maize. Plant Cell 28:1682–1700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochem 55:481–504

    CAS  Google Scholar 

  • Hatsugai N, Hara-Nishimura I (2010) Two vacuole-mediated defense strategies in plants. Plant Signal Behav 5:1568–1570

    PubMed  PubMed Central  Google Scholar 

  • Hatsugai N et al (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858

    CAS  PubMed  Google Scholar 

  • Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–911

    CAS  PubMed  Google Scholar 

  • Hatsugai N et al (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23:2496–2506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hawes C, Saint-Jore CM, Brandizzi F, Zheng H, Andreeva AV, Boevink P (2001) Cytoplasmic illuminations: in planta targeting of fluorescent proteins to cellular organelles. Protoplasma 215:77–88

    CAS  PubMed  Google Scholar 

  • Hedrich R (2012) Ion channels in plants. Physiol Rev 92:1777–1811

    CAS  PubMed  Google Scholar 

  • Hicks GR, Rojo E, Hong S, Carter DG, Raikhel NV (2004) Geminating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol 134:1227–1239

    CAS  PubMed  PubMed Central  Google Scholar 

  • Higaki T, Kutsuna N, Okubo E, Sano T, Hasezawa S (2006) Actin microfilaments regulate vacuolar structures and dynamics: dual observation of actin microfilaments and vacuolar membrane in living tobacco BY-2 cells. Plant Cell Physiol 47:839–852

    CAS  PubMed  Google Scholar 

  • Higaki T et al (2007) Elicitor-induced cytoskeletal rearrangement relates to vacuolar dynamics and execution of cell death: in vivo imaging of hypersensitive cell death in tobacco BY-2 cells. Plant Cell Physiol 48:1414–1425

    CAS  PubMed  Google Scholar 

  • Higaki T, Kutsuna N, Sano T, Hasezawa S (2008) Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biol 8:80

    PubMed  PubMed Central  Google Scholar 

  • Higaki T, Kurusu T, Hasezawa S, Kuchitsu K (2011) Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants. J Plant Res 124:315–324

    PubMed  Google Scholar 

  • Hirakawa Y, Nomura T, Hasezawa S, Higaki T (2015) Simplification of vacuole structure during plant cell death triggered by culture filtrates of Erwinia carotovora. J Integr Plant Biol 57:127–135

    CAS  PubMed  Google Scholar 

  • Höglund A-S, Lenman M, Falk A, Rask L (1991) Distribution of myrosinase in rapeseed tissues. Plant Physiol 95:213–221

    PubMed  PubMed Central  Google Scholar 

  • Höglund A-S, Lenman M, Rask L (1992) Myrosinase is localized to the interior of myrosin grains and is not associated to the surrounding tonoplast membrane. Plant Sci 85:165–170

    Google Scholar 

  • Hoh B, Hinz G, Jeong B-K, Robinson DG (1995) Protein storage vacuoles form de novo during pea cotyledon development. J Cell Sci 108:299–310

    CAS  PubMed  Google Scholar 

  • Hopkins RJ, van Dam NM, van Loon JJ (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Ann Rev Entomol 54:57–83

    CAS  Google Scholar 

  • Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145:1371–1382

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inada N, Ueda T (2014) Membrane trafficking pathways and their roles in plant-microbe interactions. Plant Cell Physiol 55:672–686

    CAS  PubMed  Google Scholar 

  • Jaquinod M, Villiers F, Kieffer-Jaquinod S, Hugouvieux V, Bruley C, Garin J, Bourguignon J (2007) A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol Cell Proteomics 6:394–412

    CAS  PubMed  Google Scholar 

  • Jauh G-Y, Phillips TE, Rogers JC (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11:1867–1882

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150:755–769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson KD, Herman EM, Chrispeels MJ (1989) An abundant, highly conserved tonoplast protein in seeds. Plant Physiol 91:1006–1013

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kamiya T, Akahori T, Ashikari M, Maeshima M (2006) Expression of the vacuolar Ca2+/H+ exchanger, OsCAX1a, in rice: cell and age specificity of expression, and enhancement by Ca2+. Plant Cell Physiol 47:96–106

    CAS  PubMed  Google Scholar 

  • Kasaras A, Melzer M, Kunze R (2012) Arabidopsis senescence-associated protein DMP1 is involved in membrane remodeling of the ER and tonoplast. BMC Plant Biol 12:54

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katsuta J, Hashiguchi Y, Shibaoka H (1990) The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. J Cell Sci 95:413–422

    Google Scholar 

  • Kim DH et al (2001) Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 13:287–301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kissen R, Rossiter JT, Bones AM (2009) The ‘mustard oil bomb’: not so easy to assemble?! Localization, expression and distribution of the components of the myrosinase enzyme system. Phytochem Rev 8:69–86

    CAS  Google Scholar 

  • Kluge C et al (2004) Subcellular distribution of the V-ATPase complex in plant cells, and in vivo localisation of the 100 kDa subunit VHA-a within the complex. BMC Cell Biol 5:29

    PubMed  PubMed Central  Google Scholar 

  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    CAS  PubMed  Google Scholar 

  • Kovar DR, Staiger CJ, Weaver EA, McCurdy DW (2000) AtFim1 is an actin filament crosslinking protein from Arabidopsis thaliana. Plant J 24:625–636

    CAS  PubMed  Google Scholar 

  • Kovermann P et al (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–1180

    CAS  PubMed  Google Scholar 

  • Koyano T, Kurusu T, Hanamata S, Kuchitsu K (2014) Regulation of vacuole-mediated programmed cell death during innate immunity and reproductive development in plants. In: Sawada H, Inoue N, Iwano M (eds) Sexual reproduction in animals and plants. Springer, Tokyo, pp 431–440

    Google Scholar 

  • Küfner I, Koch W (2008) Stress regulated members of the plant organic cation transporter family are localized to the vacuolar membrane. BMC Res Notes 1:43

    PubMed  PubMed Central  Google Scholar 

  • Kumagai F, Hasezawa S (2001) Dynamic organization of microtubules and microfilaments during cell cycle progression in higher plant cells. Plant Biol 3:4–16

    Google Scholar 

  • Kusumi A et al (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Ann Rev Biophys Biomol Struct 34:351–378

    CAS  Google Scholar 

  • Kutsuna N, Hasezawa S (2002) Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol 43:965–973

    CAS  PubMed  Google Scholar 

  • Kutsuna N, Kumagai F, Sato MH, Hasezawa S (2003) Three-dimensional reconstruction of tubular structure of vacuolar membrane throughout mitosis in living tobacco cells. Plant Cell Physiol 44:1045–1054

    CAS  PubMed  Google Scholar 

  • Lepiniec L, Debeaujon I, Routaboul J-M, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Ann Rev Plant Biol 57:405–430

    CAS  Google Scholar 

  • Leshem Y et al (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci USA 103:18008–18013

    CAS  PubMed  Google Scholar 

  • Lillemeier BF, Pfeiffer JR, Surviladze Z, Wilson BS, Davis MM (2006) Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc Natl Acad Sci USA 103:18992–18997

    CAS  PubMed  Google Scholar 

  • Ma QH, Tian B, Li YL (2010) Overexpression of a wheat jasmonate-regulated lectin increases pathogen resistance. Biochimie 92:187–193

    CAS  PubMed  Google Scholar 

  • Madina MH, Zheng H, Germain H (2018) New insight into bulb dynamics in the vacuolar lumen of Arabidopsis cells. Botany 96:511–520

    CAS  Google Scholar 

  • Maîtrejean M et al (2011) Assembly and sorting of the tonoplast potassium channel AtTPK1 and its turnover by internalization into the vacuole. Plant Physiol 156:1783–1796

    PubMed  PubMed Central  Google Scholar 

  • Martinoia E, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Plant Biol 63:183–213

    CAS  Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11:587–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • Melan MA (1999) Overview of cell fixatives and cell membrane permeants. Methods Mol Biol 115:45–55

    CAS  PubMed  Google Scholar 

  • Minami A et al (2009) Alterations in detergent-resistant plasma membrane microdomains in Arabidopsis thaliana during cold acclimation. Plant Cell Physiol 50:341–359

    CAS  PubMed  Google Scholar 

  • Mitsuhashi N, Shimada T, Mano S, Nishimura M, Hara-Nishimura I (2000) Characterization of organelles in the vacuolar-sorting pathway by visualization with GFP in tobacco BY-2 cells. Plant Cell Physiol 41:993–1001

    CAS  PubMed  Google Scholar 

  • Morita MT, Kato T, Nagafusa K, Saito C, Ueda T, Nakano A, Tasaka M (2002) Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 14:47–56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2007) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520

    PubMed  Google Scholar 

  • Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–1141

    PubMed  PubMed Central  Google Scholar 

  • Neuhaus HE, Trentmann O (2014) Regulation of transport processes across the tonoplast. Front Plant Sci 5:460

    PubMed  PubMed Central  Google Scholar 

  • Neuhaus J-M, Sticher L, Meins F, Boller T (1991) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci USA 88:10362–10366

    CAS  PubMed  Google Scholar 

  • Niemeyer HM (2009) Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. J Agric Food Chem 57:1677–1696

    CAS  PubMed  Google Scholar 

  • Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Okubo-Kurihara E, Sano T, Higaki T, Kutsuna N, Hasezawa S (2008) Acceleration of vacuolar regeneration and cell growth by overexpression of an aquaporin NtTIP1;1 in tobacco BY-2 cells. Plant Cell Physiol 50:151–160

    PubMed  Google Scholar 

  • Opalski KS, Schultheiss H, Kogel KH, Hückelhoven R (2005) The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f. sp. hordei. Plant J 41:291–303

    CAS  PubMed  Google Scholar 

  • Otegui MS, Noh YS, Martínez DE, Vila PMG, Andrew SL, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844

    CAS  PubMed  Google Scholar 

  • Ovečka M, Lang I, Baluška F, Ismail A, Illeš P, Lichtscheidl I (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226:39–54

    PubMed  Google Scholar 

  • Owens T, Poole RJ (1979) Regulation of cytoplasmic and vacuolar volumes by plant cells in suspension culture. Plant Physiol 64:900–904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ozolina N, Nesterkina I, Nurminsky V, Stepanov A, Kolesnikova E, Gurina V, Salyaev R (2011) Recognition of lipid-protein rafts in vacuolar membrane. Biochem Biophys Mol Biol 438:120–122

    CAS  Google Scholar 

  • Paris N, Stanley CM, Jones RL, Rogers JC (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85:563–572

    CAS  PubMed  Google Scholar 

  • Parton R, Fischer-Parton S, Watahiki M, Trewavas A (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114:2685–2695

    CAS  PubMed  Google Scholar 

  • Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2 + -activated channel TPC1 regulates germination and stomatal movement. Nature 434:404

    CAS  PubMed  Google Scholar 

  • Rajniak J, Barco B, Clay NK, Sattely ES (2015) A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence. Nature 525:376–379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rask L, Andréasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol 42:93–114

    CAS  PubMed  Google Scholar 

  • Reisen D, Marty F, Leborgne-Castel N (2005) New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol 5:1

    Google Scholar 

  • Robinson DG, Hoh B, Hinz G, Jeong B-K (1995) One vacuole or two vacuoles: do protein storage vacuoles arise de novo during pea cotyledon development? J Plant Physiol 145:654–664

    CAS  Google Scholar 

  • Ruthardt N, Gulde N, Spiegel H, Fischer R, Emans N (2005) Four-dimensional imaging of transvacuolar strand dynamics in tobacco BY-2 cells. Protoplasma 225:205–215

    CAS  PubMed  Google Scholar 

  • Saito C (2003) A “bulb” subregion in the vacuolar membrane. Plant Morphol 15:60–67

    Google Scholar 

  • Saito C et al (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29:245–255

    PubMed  Google Scholar 

  • Saito C, Morita MT, Kato T, Tasaka M (2005) Amyloplasts and vacuolar membrane dynamics in the living graviperceptive cell of the Arabidopsis inflorescence stem. Plant Cell 17:548–558

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saito C et al (2011) The occurrence of ‘bulbs’, a complex configuration of the vacuolar membrane, is affected by mutations of vacuolar SNARE and phospholipase in Arabidopsis. Plant J 68:64–73

    CAS  PubMed  Google Scholar 

  • Sansebastiano GPD, Barozzi F, Piro G, Denecke J, Lousa CDM (2017) Trafficking routes to the plant vacuole: connecting alternative and classical pathways. J Exp Bot 69:79–90

    PubMed  Google Scholar 

  • Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, Von Wirén N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540

    CAS  PubMed  Google Scholar 

  • Schnell U, Dijk F, Sjollema KA, Giepmans BN (2012) Immunolabeling artifacts and the need for live-cell imaging. Nat Methods 9:152–158

    CAS  PubMed  Google Scholar 

  • Schultheiss H, Dechert C, Kiraly L, Fodor J, Michel K, Kogel KH, Hückelhoven R (2003) Functional assessment of the pathogenesis-related protein PR-1b in barley. Plant Sci 165:1275–1280

    CAS  Google Scholar 

  • Segami S, Makino S, Miyake A, Asaoka M, Maeshima M (2014) Dynamics of vacuoles and H + -pyrophosphatase visualized by monomeric green fluorescent protein in Arabidopsis: artifactual bulbs and native intravacuolar spherical structures. Plant Cell 26:3416–3434

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sheahan MB, Rose RJ, McCurdy DW (2007) Actin-filament-dependent remodeling of the vacuole in cultured mesophyll protoplasts. Protoplasma 230:141–152

    PubMed  Google Scholar 

  • Shimada C, Lipka V, O’Connell R, Okuno T, Schulze-Lefert P, Takano Y (2006) Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant-Microbe Interact 19:270–279

    CAS  PubMed  Google Scholar 

  • Shimada T, Takagi J, Ichino T, Shirakawa M, Hara-Nishimura I (2018) Plant vacuoles. Ann Rev Plant Biol 69:123–145

    CAS  Google Scholar 

  • Shitan N (2016) Secondary metabolites in plants: transport and self-tolerance mechanisms. Biosci Biotechnol Biochem 80:1283–1293

    CAS  PubMed  Google Scholar 

  • Silady RA, Ehrhardt DW, Jackson K, Faulkner C, Oparka K, Somerville CR (2008) The GRV2/RME-8 protein of Arabidopsis functions in the late endocytic pathway and is required for vacuolar membrane flow. Plant J 53:29–41

    CAS  PubMed  Google Scholar 

  • Smertenko AP, Bozhkov PV, Filonova LH, Arnold S, Hussey PJ (2003) Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J 33:813–824

    CAS  PubMed  Google Scholar 

  • Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine’s defensive function in nature. PLoS Biol 2:e217

    PubMed  PubMed Central  Google Scholar 

  • Swanson SJ, Bethke PC, Jones RL (1998) Barley aleurone cells contain two types of vacuoles: characterization of lytic organelles by use of fluorescent probes. Plant Cell 10:685–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Kutsuna N, Kanazawa Y, Kondo N, Hasezawa S, Sano T (2007) Intra-vacuolar reserves of membranes during stomatal closure: the possible role of guard cell vacuoles estimated by 3-D reconstruction. Plant Cell Physiol 48:1159–1169

    CAS  PubMed  Google Scholar 

  • Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323

    CAS  PubMed  Google Scholar 

  • Thangstad O, Iversen T-H, Slupphaug G, Bones A (1990) Immunocytochemical localization of myrosinase in Brassica napus L. Planta 180:245–248

    CAS  PubMed  Google Scholar 

  • Thangstad O, Evjen K, Bones A (1991) Immunogold-EM localization of myrosinase in Brassicaceae. Protoplasma 161:85–93

    CAS  Google Scholar 

  • Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    CAS  PubMed  Google Scholar 

  • Tominaga M, Yokota E, Vidali L, Sonobe S, Hepler PK, Shimmen T (2000) The role of plant villin in the organization of the actin cytoskeleton, cytoplasmic streaming and the architecture of the transvacuolar strand in root hair cells of Hydrocharis. Planta 210:836–843

    CAS  PubMed  Google Scholar 

  • Toyooka K, Moriyasu Y, Goto Y, Takeuchi M, Fukuda H, Matsuoka K (2006) Protein aggregates are transported to vacuoles by macroautophagic mechanism in nutrient-starved plant cells. Autophagy 2:96–106

    CAS  PubMed  Google Scholar 

  • Ueda T, Yamaguchi M, Uchimiya H, Nakano A (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 20:4730–4741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda H et al (2006) AtVAM3 is required for normal specification of idioblasts, myrosin cells. Plant Cell Physiol 47:164–175

    CAS  PubMed  Google Scholar 

  • Uemura T, Yoshimura SH, Takeyasu K, Sato MH (2002) Vacuolar membrane dynamics revealed by GFP-AtVam3 fusion protein. Genes Cells 7:743–753

    CAS  PubMed  Google Scholar 

  • Van der Hoorn RA, Jones JD (2004) The plant proteolytic machinery and its role in defence. Curr Opin Plant Biol 7:400–407

    PubMed  Google Scholar 

  • Van Gestel K, Köhler R, Verbelen JP (2002) Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J Exp Bot 53:659–667

    PubMed  Google Scholar 

  • Vermeer JE et al (2006) Visualization of PtdIns3P dynamics in living plant cells. Plant J 47:687–700

    CAS  PubMed  Google Scholar 

  • Vetter J (2000) Plant cyanogenic glycosides. Toxicon 38:11–36

    CAS  PubMed  Google Scholar 

  • Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K (2006) Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J 48:296–306

    CAS  PubMed  Google Scholar 

  • Wada Y (2013) Vacuoles in mammals: a subcellular structure indispensable for early embryogenesis. Bioarchitecture 3:13–19

    PubMed  PubMed Central  Google Scholar 

  • Wang J, Li Y, Lo SW, Hillmer S, Sun SS, Robinson DG, Jiang L (2007) Protein mobilization in germinating mung bean seeds involves vacuolar sorting receptors and multivesicular bodies. Plant Physiol 143:1628–1639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson RE (1993) Organelle movements. Ann Rev Plant Biol 44:181–202

    Google Scholar 

  • Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270

    CAS  PubMed  Google Scholar 

  • Wormit A et al (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18:3476–3490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Ishida H, Reisen D, Hanson MR (2006) Upregulation of a tonoplast-localized cytochrome P450 during petal senescence in Petunia inflata. BMC Plant Biol 6:8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaryo Y, Dubots E, Albrieux C, Baldan B, Block MA (2008) Phosphate availability affects the tonoplast localization of PLDζ2, an Arabidopsis thaliana phospholipase D. FEBS Lett 582:685–690

    CAS  PubMed  Google Scholar 

  • Yoshida K et al (2013) Studies on vacuolar membrane microdomains isolated from Arabidopsis suspension-cultured cells: local distribution of vacuolar membrane proteins. Plant Cell Physiol 54:1571–1584

    CAS  PubMed  Google Scholar 

  • Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Hicks GR, Raikhel NV (2014) Plant vacuole morphology and vacuolar trafficking. Front Plant Sci 5:476

    PubMed  PubMed Central  Google Scholar 

  • Zhou S, Richter A, Jander G (2018) Beyond defense: multiple functions of benzoxazinoids in maize metabolism. Plant Cell Physiol 59(8):1528–1537

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are very thankful to Melodie B. Plourde for critical review of the manuscript.

Funding

This work was supported by a NSERC Grant No. RGPIN/435870-2013 and Canada Research Chair number 950-231790.

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Authors and Affiliations

  1. Department of Chemistry, Biochemistry and Physics, Université du Québec à Trois-Rivières, 3351 boulevard des Forges, Trois-Rivières, QC, G9A 5H7, Canada

    Mst Hur Madina, Md Saifur Rahman & Hugo Germain

  2. Department of Biology, McGill University, 1205 Dr. Penfield Avenue, Montreal, QC, H3A 1B1, Canada

    Huanquan Zheng

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  1. Mst Hur Madina
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  2. Md Saifur Rahman
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  3. Huanquan Zheng
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  4. Hugo Germain
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Contributions

Conceptualization: MHM, HZ, HG. Data curation: MHM, MSR, HZ, HG. Funding acquisition: HG. Methodology: MHM, MSR, HG. Project administration: HZ, HG. Resources: HG. Software: MSR, HG. Supervision: HZ, HG. Validation: MHM, MSR, HZ, HG. Visualization: MHM, HG. Writing—original draft: MHM, MSR, HG. Writing—review & editing: HZ, HG.

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Correspondence to Hugo Germain.

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Supplementary material 1 Video S1. Uneven distribution of a marker protein on the bulb surface in Arabidopsis. Video of 3-D confocal images of leaf epidermal cell expressing Mlp124357-GFP showing a clear view of an uneven protein distribution of markers on bulbs in a single cell. The Mlp124357, an effector of Melampsora larici-populina, was cloned in fusion with GFP and stably transformed into wild type (Col-0) Arabidopsis. Live-cell imaging was performed by laser scanning confocal microscopy of leaf epidermal cells of 4-days old plants. The GFP was excited at 488 nm and green fluorescence was collected at 505-525 nm. Scale bar = 10 µm. The color gradient reflect the depth. (MP4 4425 kb)

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Madina, M.H., Rahman, M.S., Zheng, H. et al. Vacuolar membrane structures and their roles in plant–pathogen interactions. Plant Mol Biol 101, 343–354 (2019). https://doi.org/10.1007/s11103-019-00921-y

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