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Biology of callose (β-1,3-glucan) turnover at plasmodesmata

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Abstract

The turnover of callose (β-1,3-glucan) within cell walls is an essential process affecting many developmental, physiological and stress related processes in plants. The deposition and degradation of callose at the neck region of plasmodesmata (Pd) is one of the cellular control mechanisms regulating Pd permeability during both abiotic and biotic stresses. Callose accumulation at Pd is controlled by callose synthases (CalS; EC 2.4.1.34), endogenous enzymes mediating callose synthesis, and by β-1,3-glucanases (BG; EC 3.2.1.39), hydrolytic enzymes which specifically degrade callose. Transcriptional and posttranslational regulation of some CalSs and BGs are strongly controlled by stress signaling, such as that resulting from pathogen invasion. We review the role of Pd-associated callose in the regulation of intercellular communication during developmental, physiological, and stress response processes. Special emphasis is placed on the involvement of Pd-callose in viral pathogenicity. Callose accumulation at Pd restricts virus movement in both compatible and incompatible interactions, while its degradation promotes pathogen spread. Hence, studies on mechanisms of callose turnover at Pd during viral cell-to-cell spread are of importance for our understanding of host mechanisms exploited by viruses in order to successfully spread within the infected plant.

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Abbreviations

BG:

β-1,3-glucanase; β-1,3-glucan hydrolase

CalS:

Callose synthase

ER:

Endoplasmic reticulum

GSL:

Glucan synthase-like

MP:

Movement protein

Pd:

Plasmodesmata

PR:

Pathogenesis related

SAR:

Systemic acquired resistance

SEL:

Size exclusion limit

References

  • Agudelo-Romero P, Carbonell P, de la Iglesia F, Carrera J, Rodrigo G, Jaramillo A, Perez-Amador MA, Elena SF (2008) Changes in the gene expression profile of Arabidopsis thaliana after infection with Tobacco etch virus. Virol J 5:92

    PubMed  Google Scholar 

  • Aist JR (1976) Papillae and related wound plugs of plant cells. Annu Rev Phytopathol 14:145–163

    Google Scholar 

  • Allison AV, Shalla TA (1974) The ultrastructure of local lesions induced by Potato virus X: a sequence of cytological events in the course of infection. Phytopathology 64:784–793

    Google Scholar 

  • Ascencio-Ibanez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148(1):436–454

    CAS  PubMed  Google Scholar 

  • Avisar D, Prokhnevsky AI, Dolja VV (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82(6):2836–2843

    CAS  PubMed  Google Scholar 

  • Babu M, Griffiths JS, Huang TS, Wang A (2008) Altered gene expression changes in Arabidopsis leaf tissues and protoplasts in response to Plum pox virus infection. BMC Genomics 9:325

    PubMed  Google Scholar 

  • Bayer E, Thomas C, Maule A (2008) Symplastic domains in the Arabidopsis shoot apical meristem correlate with PDLP1 expression patterns. Plant Signal Behav 3(10):853–855

    PubMed  Google Scholar 

  • Beffa R, Meins F (1996) Pathogenesis-related functions of plant beta-1, 3-glucanases investigated by antisense transformation—a review. Gene 179(1):97–103

    CAS  PubMed  Google Scholar 

  • Beffa RS, Hofer RM, Thomas M, Meins F Jr (1996) Decreased susceptibility to viral disease of beta-1, 3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8(6):1001–1011

    CAS  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Jackson D (2009) Redox homeostasis regulates plasmodesmal communication in Arabidopsis meristems. Plant Signal Behav 4(7):655–659

    CAS  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106(9):3615–3620

    CAS  PubMed  Google Scholar 

  • Bol JF, Linthorst HJM, Cornelissen BJC (1990) Plant pathogenesis-related proteins induced by virus infection. Annu Rev Phytopathol 28:113–138

    CAS  Google Scholar 

  • Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53(372):1367–1376

    CAS  PubMed  Google Scholar 

  • Borner GH, Sherrier DJ, Stevens TJ, Arkin IT, Dupree P (2002) Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A genomic analysis. Plant Physiol 129(2):486–499

    CAS  PubMed  Google Scholar 

  • Borner GH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132(2):568–577

    CAS  PubMed  Google Scholar 

  • Botha CEJ, Cross RHN (2000) Towards reconciliation of structure with function in plasmodesmata—who is the gatekeeper? Micron 31(6):713–721

    CAS  PubMed  Google Scholar 

  • Brownfield L, Doblin MS, Fincher GB, Bacic A (2009) Biochemical and molecular properties of biosynthetic enzymes for (1,3)-beta-glucans in embryophytes, chlorophytes and rhodophytes. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides. London Academic Press, pp 283–326

  • Bucciaglia PA, Zimmermann E, Smith AG (2003) Functional analysis of a beta-1, 3-glucanase gene (Tag1) with anther-specific RNA and protein accumulation using antisense RNA inhibition. J Plant Physiol 160(11):1367–1373

    CAS  PubMed  Google Scholar 

  • Bucher GL, Tarina C, Heinlein M, Di Serio F, Meins F Jr, Iglesias VA (2001) Local expression of enzymatically active class I beta-1, 3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28(3):361–369

    CAS  PubMed  Google Scholar 

  • Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141(2):446–455

    CAS  PubMed  Google Scholar 

  • Castresana C, de Carvalho F, Gheysen G, Habets M, Inzé D, Van Montague M (1990) Tissue-specific and pathogen-induced regulation of a Nicotiana plumbaginifolia beta-1, 3-glucanase gene. Plant Cell 2:1131–1143

    CAS  PubMed  Google Scholar 

  • Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signal Behav 4(6):489–492

    CAS  PubMed  Google Scholar 

  • Chen XY, Liu L, Lee E, Han X, Rim Y, Chu H, Kim SW, Sack F, Kim JY (2009) The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiol 150(1):105–113

    CAS  PubMed  Google Scholar 

  • Choi CW (1999) Modified plasmodesmata in sorghum (Sorghum bicolor L. Moench) leaf tissues infected by Maize dwarf mosaic virus. J Plant Biol 42(1):63–70

    Google Scholar 

  • Delp G, Palva ET (1999) A novel flower-specific Arabidopsis gene related to both pathogen-induced and developmentally regulated plant beta-1, 3-glucanase genes. Plant Mol Biol 39(3):565–575

    CAS  PubMed  Google Scholar 

  • Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3(1):61–72

    CAS  PubMed  Google Scholar 

  • Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42(3):315–328

    CAS  PubMed  Google Scholar 

  • Dong X, Hong Z, Chatterjee J, Kim S, Verma DP (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229(1):87–98

    CAS  PubMed  Google Scholar 

  • Doxey AC, Yaish MW, Moffatt BA, Griffith M, McConkey BJ (2007) Functional divergence in the Arabidopsis beta-1, 3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 24(4):1045–1055

    CAS  PubMed  Google Scholar 

  • Elortza F, Nuhse TS, Foster LJ, Stensballe A, Peck SC, Jensen ON (2003) Proteomic analysis of glycosylphosphatidylinositol-anchored membrane proteins. Mol Cell Proteomics 2(12):1261–1270

    CAS  PubMed  Google Scholar 

  • Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE (2005) Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 58(3):333–349

    CAS  PubMed  Google Scholar 

  • Epel BL (2009) Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host beta-1, 3-glucanases. Semin Cell Dev Biol 20(9):1074–1081

    CAS  PubMed  Google Scholar 

  • Flors V, Ton J, van Doorn R, Jakab G, Garcia-Agustin P, Mauch-Mani B (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54(1):81–92

    CAS  PubMed  Google Scholar 

  • Furch AC, Hafke JB, Schulz A, van Bel AJ (2007) Ca2+-mediated remote control of reversible sieve tube occlusion in Vicia faba. J Exp Bot 58(11):2827–2838

    CAS  PubMed  Google Scholar 

  • Furch AC, Hafke JB, van Bel AJ (2008) Plant- and stimulus-specific variations in remote-controlled sieve-tube occlusion. Plant Signal Behav 3(10):858–861

    PubMed  Google Scholar 

  • Furch AC, Zimmermann MR, Will T, Hafke JB, van Bel AJ (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61(13):3697–3708

    CAS  PubMed  Google Scholar 

  • Golinowski W, Grundler FMW, Sobczak M (1996) Changes in the structure of Arabidopsis thaliana during female development of the plant parasitic nematode Heterodera schachtii. Protoplasma 194:103–116

    Google Scholar 

  • Grover A, Gowthaman R (2003) Strategies for development of fungus-resistant transgenic plants. Curr Sci 84(3):330–340

    Google Scholar 

  • Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL (2008) Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant Microb Interact 21(3):335–345

    CAS  Google Scholar 

  • Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, Kanaoka MM, Hong Z, Torii KU (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8). Development 137(10):1731–1741

    CAS  PubMed  Google Scholar 

  • Heinlein M, Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol 235:93–164

    CAS  PubMed  Google Scholar 

  • Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN (1998) Changing patterns of localization of the Tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10(7):1107–1120

    CAS  PubMed  Google Scholar 

  • Hennig J, Dewey RE, Cutt JR, Klessig DF (1993) Pathogen, salicylic acid and developmental dependent expression of a beta-1, 3-glucanase/GUS gene fusion in transgenic tobacco plants. Plant J 4(3):481–493

    CAS  PubMed  Google Scholar 

  • Hinrichs-Berger J, Harfold M, Breger S, Buchenauer H (1999) Cytological responses of susceptible and extremely resistant potato plants to inoculation with Potato virus Y. Physiol Mol Plant Pathol 55:143–150

    Google Scholar 

  • Hird DL, Worrall D, Hodge R, Smartt S, Paul W, Scott R (1993) The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6 gene displays similarity to beta-1, 3-glucanases. Plant J 4(6):1023–1033

    CAS  PubMed  Google Scholar 

  • Hofmann J, Youssef-Banora M, de Almeida-Engler J, Grundler FM (2010) The role of callose deposition along plasmodesmata in nematode feeding sites. Mol Plant Microb Interact 23(5):549–557

    CAS  Google Scholar 

  • Hoj PB, Rodriguez EB, Stick RV, Stone BA (1989) Differences in active site structure in a family of beta-glucan endohydrolases deduced from the kinetics of inactivation by epoxyalkyl beta-oligoglucosides. J Biol Chem 264(9):4939–4947

    CAS  PubMed  Google Scholar 

  • Hong ZL, Delauney AJ, Verma DPS (2001a) A cell plate specific callose synthase and its interaction with phragmoplastin. Plant Cell 13(4):755–768

    CAS  PubMed  Google Scholar 

  • Hong ZL, Zhang Z, Olson JM, Verma DPS (2001b) A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13(4):769–779

    CAS  PubMed  Google Scholar 

  • Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA (2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol 137(3):1147–1159

    CAS  PubMed  Google Scholar 

  • Huang L, Chen XY, Rim Y, Han X, Cho WK, Kim SW, Kim JY (2009) Arabidopsis glucan synthase-like 10 functions in male gametogenesis. J Plant Physiol 166(4):344–352

    CAS  PubMed  Google Scholar 

  • Hull R (2002) Matthews’ plant virology, 4th edn. London Academic Press

  • Iglesias VA, Meins F Jr (2000) Movement of plant viruses is delayed in a beta-1, 3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21(2):157–166

    CAS  PubMed  Google Scholar 

  • Iriti M, Faoro F (2008) Abscisic acid is involved in chitosan-induced resistance to Tobacco necrosis virus (TNV). Plant Physiol Biochem 46(12):1106–1111

    CAS  PubMed  Google Scholar 

  • Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15(11):2503–2513

    CAS  PubMed  Google Scholar 

  • Jelitto-Van Dooren EP, Vidal S, Denecke J (1999) Anticipating endoplasmic reticulum stress. A novel early response before pathogenesis-related gene induction. Plant Cell 11(10):1935–1944

    CAS  PubMed  Google Scholar 

  • Ji C, Kuc J (1995) Purification and characterization of an acidic beta-1, 3-glucanase from cucumber and its relationship to systemic disease resistance induced by Colletotrichum lagenarium and Tobacco necrosis virus. Mol Plant Microb Interact 8(6):899–905

    CAS  Google Scholar 

  • Jurgens G, Geldner N (2002) Protein secretion in plants: from the trans-Golgi network to the outer space. Traffic 3(9):605–613

    CAS  PubMed  Google Scholar 

  • Kathiria P, Sidler C, Golubov A, Kalischuk M, Kawchuk LM, Kovalchuk I (2010) Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol 153(4):1859–1870

    CAS  PubMed  Google Scholar 

  • Kauffmann S, Legrand M, Geoffroy P, Fritig B (1987) Biological function of pathogenesis-related proteins: four PR proteins of tobacco have 1, 3-beta-glucanase activity. EMBO J 6(11):3209–3212

    CAS  PubMed  Google Scholar 

  • Kauss H (1985) Callose biosynthesis as a Ca2+-regulated process and possible relations to the induction of other metabolic changes. J Cell Sci Suppl 2:89–103

    CAS  PubMed  Google Scholar 

  • Kauss H (1996) Callose synthesis. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. BIOS Scientific, Oxford, pp 77–92

    Google Scholar 

  • Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC (2002) Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development 129:1261–1272

    CAS  PubMed  Google Scholar 

  • Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121(5):749–759

    CAS  PubMed  Google Scholar 

  • Krasavina MS, Malyshenko SI, Raldugina GN, Burmistrova NA, Nosov AV (2002) Can salicylic acid affect the intercellular transport of the Tobacco mosaic virus by changing plasmodesmal permeability? Russ J Plant Physiol 49(1):71–77

    Google Scholar 

  • Kunze I, Kunze G, Broker M, Manteuffel R, Meins F Jr, Muntz K (1998) Evidence for secretion of vacuolar alpha-mannosidase, class I chitinase, and class I beta-1, 3-glucanase in suspension cultures of tobacco cells. Planta 205(1):92–99

    CAS  PubMed  Google Scholar 

  • Lartey RT, Ghoshroy K, Ghoshroy S (2008) Association of selective deposition of (1-3)-beta-glucan in floral tissues with restricted movement of Turnip vein-clearing virus in Arabidopsis: a possible mechanism for non-seed transmission. Plant Pathol J 7(2):120–130

    CAS  Google Scholar 

  • Lehesranta SJ, Lichtenberger R, Helariutta Y (2010) Cell-to-cell communication in vascular morphogenesis. Curr Opin Plant Biol 13(1):59–65

    CAS  PubMed  Google Scholar 

  • Leubner-Metzger G (2001) Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways. Planta 213(5):758–763

    CAS  PubMed  Google Scholar 

  • Leubner-Metzger G (2002) Seed after-ripening and over-expression of class I beta-1, 3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215(6):959–968

    CAS  PubMed  Google Scholar 

  • Leubner-Metzger G (2005) beta-1, 3-Glucanase gene expression in low-hydrated seeds as a mechanism for dormancy release during tobacco after-ripening. Plant J 41(1):133–145

    CAS  PubMed  Google Scholar 

  • Leubner-Metzger G, Meins F (1999) Functions and regulation of plant beta-1, 3-glucanases (PR-2). In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC, Boca Raton, pp 49–76

    Google Scholar 

  • Leubner-Metzger G, Meins F Jr (2000) Sense transformation reveals a novel role for class I beta-1, 3-glucanase in tobacco seed germination. Plant J 23(2):215–221

    CAS  PubMed  Google Scholar 

  • Leubner-Metzger G, Meins F Jr (2001) Antisense-transformation reveals novel roles for class I beta-1, 3-glucanase in tobacco seed after-ripening and photodormancy. J Exp Bot 52(362):1753–1759

    CAS  PubMed  Google Scholar 

  • Levy A, Epel BL (2009) Cytology of the (1-3)-beta-glucan (callose) in plasmodesmata and sieve plate pores. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides. London Academic Press, pp 439–463

  • Levy A, Erlanger M, Rosenthal M, Epel BL (2007a) A plasmodesmata-associated beta-1, 3-glucanase in Arabidopsis. Plant J 49(4):669–682

    CAS  PubMed  Google Scholar 

  • Levy A, Guenoune-Gelbart D, Epel BL (2007b) beta-1, 3-Glucanases: plasmodesmal gate keepers for intracellular communication. Plant Signal Behav 2(5):404–407

    PubMed  Google Scholar 

  • Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci USA 107(6):2491–2496

    CAS  PubMed  Google Scholar 

  • Liarzi O, Epel BL (2005) Development of a quantitative tool for measuring changes in the coefficient of conductivity of plasmodesmata induced by developmental, biotic, and abiotic signals. Protoplasma 225(1–2):67–76

    CAS  PubMed  Google Scholar 

  • Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139(2):935–948

    CAS  PubMed  Google Scholar 

  • Lu H, Zhao X, Wang W, Yin H, Xu J, Bai X, Du Y (2010) Inhibition effect of Tobacco mosaic virus and regulation effect on calreticulin of oligochitosan in tobacco by induced Ca2+ influx. Carbohydr Polym 82(1):136–142

    CAS  Google Scholar 

  • Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344(1):169–184

    CAS  PubMed  Google Scholar 

  • Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19(10):495–503

    CAS  PubMed  Google Scholar 

  • Lusso M, Kuc J (1996) The effect of sense and antisense expression of the PR-N gene for β-1, 3-glucanase on disease resistance of tobacco to fungi and viruses. Physiol Mol Plant Pathol 49:267–283

    CAS  Google Scholar 

  • Mac A, Krzymowska M, Barabasz A, Hennig J (2004) Transcriptional regulation of the gluB promoter during plant response to infection. Cell Mol Biol Lett 9(4B):843–853

    CAS  PubMed  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250(4983):1002–1004

    CAS  PubMed  Google Scholar 

  • Mas P, Beachy RN (1999) Replication of Tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J Cell Biol 147(5):945–958

    CAS  PubMed  Google Scholar 

  • Melchers LS, Sela-Buurlage MB, Vloemans SA, Woloshuk CP, Van Roekel JS, Pen J, van den Elzen PJ, Cornelissen BJ (1993) Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and beta-1, 3-glucanase in transgenic plants. Plant Mol Biol 21(4):583–593

    CAS  PubMed  Google Scholar 

  • Menard R, Alban S, de Ruffray P, Jamois F, Franz G, Fritig B, Yvin JC, Kauffmann S (2004) Beta-1, 3-glucan sulfate, but not beta-1, 3-glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis. Plant Cell 16(11):3020–3032

    CAS  PubMed  Google Scholar 

  • Meyer D, Pajonk S, Micali C, O’Connell R, Schulze-Lefert P (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57(6):986–999

    CAS  PubMed  Google Scholar 

  • Moore AE, Stone BA (1972a) A beta-1, 3-glucan hydrolase from Nicotiana glutinosa: II. Specificity, action pattern and inhibitor studies. Biochim Biophys Acta 258(1):248–264

    CAS  PubMed  Google Scholar 

  • Moore AE, Stone BA (1972b) Effect of infection with TMV and other viruses on the level of a beta-1, 3-glucan hydrolase in leaves of Nicotiana glutinosa. Virology 50(3):791–798

    CAS  PubMed  Google Scholar 

  • Movsesian NR, Alizade X, Musiichuk KA, Popov Iu G, Piruzian ES (2001) Transgenic tobacco plants expressing bacterial genes encoded the thermostable glucanases. Genetika 37(6):745–753

    CAS  PubMed  Google Scholar 

  • Nakashima J, Laosinchai W, Cui X, Brown RMJ (2003) New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding. Cellulose 10:369–389

    CAS  Google Scholar 

  • Nawrath C, Metraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11(8):1393–1404

    CAS  PubMed  Google Scholar 

  • Nishikawa S, Zinkl GM, Swanson RJ, Maruyama D, Preuss D (2005) Callose (beta-1, 3-glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol 5:22

    PubMed  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    CAS  PubMed  Google Scholar 

  • Northcote DH, Davey R, Lay J (1989) Use of antisera to localize callose, xylan and arabinogalactan in the cell-plate, primary and secondary cell walls of plant cells. Planta 178:353–366

    CAS  Google Scholar 

  • Ori N, Sessa G, Lotan T, Himmelhoch S, Fluhr R (1990) A major stylar matrix polypeptide (Sp41) is a member of the pathogenesis-related proteins superclass. EMBO J 9(11):3429–3436

    CAS  PubMed  Google Scholar 

  • Ostergaard L, Petersen M, Mattsson O, Mundy J (2002) An Arabidopsis callose synthase. Plant Mol Biol 49(6):559–566

    CAS  PubMed  Google Scholar 

  • Payne G, Ward E, Gaffney T, Goy PA, Moyer M, Harper A, Meins F, Ryals J (1990) Evidence for a 3rd structural class of beta-1, 3-glucanase in tobacco. Plant Mol Biol 15(6):797–808

    CAS  PubMed  Google Scholar 

  • Pennazio S, Redolfi P, Sapetti C (1981) Callose formation and permeability changes during the partly localized reaction of Gomphrena globosa to Potato virus X. Phytopathol Z 100:172–181

    Google Scholar 

  • Prokhnevsky AI, Peremyslov VV, Dolja VV (2005) Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79(22):14421–14428

    CAS  PubMed  Google Scholar 

  • Radford JE, Vesk M, Overall RL (1998) Callose deposition at plasmodesmata. Protoplasma 201(1–2):30–37

    CAS  Google Scholar 

  • Reichel C, Beachy RN (1998) Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA 95(19):11169–11174

    CAS  PubMed  Google Scholar 

  • Rinne PL, van der Schoot C (1998) Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125(8):1477–1485

    CAS  PubMed  Google Scholar 

  • Rinne PL, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26(3):249–264

    CAS  PubMed  Google Scholar 

  • Roberts AG (2005) Plasmodesmal structure and development. In: Oparka KJ (ed) Plasmodesmata. Annu Plant Rev, Vol. 18, Oxford Blackwell Publishing, pp 1–32

  • Ruan YL, Llewellyn DJ, Furbank RT (2001) The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13(1):47–60

    CAS  PubMed  Google Scholar 

  • Ruan YL, Xu SM, White R, Furbank RT (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiol 136(4):4104–4113

    CAS  PubMed  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT, Chourey PS (2005) The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered patterns of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton. J Exp Bot 56(413):977–984

    CAS  PubMed  Google Scholar 

  • Ruiz-Medrano R, Xoconostle-Cazares B, Kragler F (2004) The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses. Curr Opin Plant Biol 7(6):641–650

    CAS  PubMed  Google Scholar 

  • Sagi G, Katz A, Guenoune-Gelbart D, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. Plant Cell 17 (6):1788–1800

    Google Scholar 

  • Samuels AL, Giddings TH Jr, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130(6):1345–1357

    CAS  PubMed  Google Scholar 

  • Sanada M, Matsushita K, Shimokawa H, Itoh R (1986) Comparison of beta-1, 3-glucan hydrolase activity in some tobacco plants inoculated with Tobacco mosaic virus. Ann Phytopathol Soc Jpn 52:320–329

    CAS  Google Scholar 

  • Schuster G, Flemming M (1976) Studies on the formation of diffusion barriers in hypersensitive hosts of Tobacco mosaic virus and the role of necrotization in the formation of diffusion barriers as well as in the localization of virus infections. Phytopathol Z 87:345–352

    Google Scholar 

  • Sela-Buurlage MB, Ponstein AS, Bres-Vloemans SA, Melchers LS, Van Den Elzen P, Cornelissen B (1993) Only specific tobacco (Nicotiana tabacum) chitinases and beta-1, 3-glucanases exhibit antifungal activity. Plant Physiol 101(3):857–863

    CAS  PubMed  Google Scholar 

  • Serova VV, Raldugina GN, Krasavina MS (2006) Inhibition of callose hydrolysis by salicylic acid interferes with Tobacco mosaic virus transport. Dokl Biochem Biophys 406:36–39

    CAS  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 Microb Interact 19(3):270–279

    CAS  Google Scholar 

  • Shimomura T (1979) Stimulation of callose synthesis in the leaves of Samsun NN tobacco showing systemic acquired resistance to Tobacco mosaic virus. Ann Phytopathol Soc Japan 45:299–304

    Google Scholar 

  • Shimomura T, Dijkstra J (1975) The occurrence of callose during the process of local lesion formation. Neth J Plant Pathol 81:107–121

    Google Scholar 

  • Shinshi H, Wenzler H, Neuhaus JM, Felix G, Hofsteenge J, Meins F (1988) Evidence for N-terminal and C-terminal processing of a plant defense-related enzyme—primary structure of tobacco prepro-beta-1, 3-glucanase. Proc Natl Acad Sci USA 85(15):5541–5545

    CAS  PubMed  Google Scholar 

  • Simmons CR (1994) The physiology and molecular biology of plant 1, 3-beta-d-glucanases and 1, 3;1, 4-beta-d-glucanases. Crit Rev Plant Sci 13(4):325–387

    CAS  Google Scholar 

  • Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21(2):581–594

    CAS  PubMed  Google Scholar 

  • Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z, Osawa H, Maeda T, Mori T, Volkmann D, Matsumoto H (2000) Aluminum-induced 1– > 3-beta-d-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 124:991–1006

    CAS  PubMed  Google Scholar 

  • Stass A, Horst WJ (2009) Callose in abiotic stress. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides. London Academic Press, pp 499–524

  • Stobbs LW, Manocha MS (1977) Histological changes associated with virus localization in TMV-infected Pinto bean leaves. Physiol Plant Pathol 11:87–94

    Google Scholar 

  • Stone BA, Clarke AE (1992) Chemistry and biology of 1– > 3-beta-glucans. La Trobe University Press, Victoria

    Google Scholar 

  • Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P (2009) Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc Natl Acad Sci USA 106(40):17229–17234

    CAS  PubMed  Google Scholar 

  • Thiele K, Wanner G, Kindzierski V, Jurgens G, Mayer U, Pachl F, Assaad FF (2009) The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant J 58:13–26

    CAS  Google Scholar 

  • Toller A, Brownfield L, Neu C, Twell D, Schulze-Lefert P (2008) Dual function of Arabidopsis glucan synthase-like genes GSL8 and GSL10 in male gametophyte development and plant growth. Plant J 54(5):911–923

    PubMed  Google Scholar 

  • Ton J, Mauch-Mani B (2004) Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38(1):119–130

    CAS  PubMed  Google Scholar 

  • Ueki S, Citovsky V (2002) The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nat Cell Biol 4(7):478–486

    CAS  PubMed  Google Scholar 

  • Verma DP, Hong Z (2001) Plant callose synthase complexes. Plant Mol Biol 47:693–701

    CAS  PubMed  Google Scholar 

  • Vierheilig H, Alt M, Lange J, Gut-Rella M, Wiemken A, Boller T (1995) Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vesicular–arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 61(8):3031–3034

    CAS  PubMed  Google Scholar 

  • Vogel J, Somerville S (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc Natl Acad Sci USA 97(4):1897–1902

    CAS  PubMed  Google Scholar 

  • Vogeli-Lange R, Hansengehri A, Boller T, Meins F (1988) Induction of the defense-related glucanohydrolases, beta-1, 3-glucanase and chitinase, by Tobacco mosaic virus infection of tobacco leaves. Plant Sci 54(3):171–176

    Google Scholar 

  • Vogeli-Lange R, Frundt C, Hart CM, Nagy F, Meins F Jr (1994) Developmental, hormonal, and pathogenesis-related regulation of the tobacco class I beta-1, 3-glucanase B promoter. Plant Mol Biol 25(2):299–311

    CAS  PubMed  Google Scholar 

  • Voigt CA, Somerville SC (2009) Callose in biotic stress (pathogenesis). In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides. London Academic Press, pp 525–562

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308(5724):1036–1040

    CAS  PubMed  Google Scholar 

  • Ward ER, Payne GB, Moyer MB, Williams SC, Dincher SS, Sharkey KC, Beck JJ, Taylor HT, Ahl-Goy P, Meins F, Ryals JA (1991) Differential regulation of beta-1, 3-glucanase messenger RNAs in response to pathogen infection. Plant Physiol 96(2):390–397

    CAS  PubMed  Google Scholar 

  • Wawrzynska A, Rodibaugh NL, Innes RW (2010) Synergistic activation of defense responses in Arabidopsis by simultaneous loss of the GSL5 callose synthase and the EDR1 protein kinase. Mol Plant Microb Interact 23(5):578–584

    CAS  Google Scholar 

  • Whitham SA, Quan S, Chang HS, Cooper B, Estes B, Zhu T, Wang X, Hou YM (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 33(2):271–283

    CAS  PubMed  Google Scholar 

  • Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of Tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246(4928):377–379

    CAS  PubMed  Google Scholar 

  • Wright KM, Wood NT, Roberts AG, Chapman S, Boevink P, Mackenzie KM, Oparka KJ (2007) Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8(1):21–31

    CAS  PubMed  Google Scholar 

  • Wrobel-Kwiatkowska M, Lorenc-Kukula K, Starzycki M, Oszmianski J, Kepczynska E, Szopa J (2004) Expression of β-1, 3-glucanase in flax causes increased resistance to fungi. Physiol Mol Plant Pathol 65(5):245–256

    CAS  Google Scholar 

  • Wu JH, Dimitman JE (1970) Leaf structure and callose formation as determinants of TMV movement in bean leaves as revealed by UV irradiation studies. Virology 40(4):820–827

    CAS  PubMed  Google Scholar 

  • Yang C, Guo R, Jie F, Nettleton D, Peng J, Carr T, Yeakley JM, Fan JB, Whitham SA (2007) Spatial analysis of Arabidopsis thaliana gene expression in response to Turnip mosaic virus infection. Mol Plant Microb Interact 20(4):358–370

    CAS  Google Scholar 

  • Ye XS, Pan SQ, Kuc J (1990) Association of pathogenesis-related proteins and activities of peroxidase, beta-1, 3-glucanase and chitinase with systemic induced resistance to blue mould of tobacco but not to systemic Tobacco mosaic virus. Physiol Mol Plant Pathol 36:523–531

    CAS  Google Scholar 

  • Zavaliev R, Sagi G, Gera A, Epel BL (2010) The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61 (1):131–142

    Google Scholar 

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Acknowledgements

The authors thank Amit Levy for providing the Fig. 2 source. BLE and RZ are supported by the Israel Science Foundation grant 723/00-17.1, and by the Manna Institute for Plant Biosciences at Tel Aviv University. VC and SU are supported by NIH grant 1059779-1-41721.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, 69978, Israel

    Raul Zavaliev & Bernard L. Epel

  2. Department of Biochemistry and Cell Biology, State University of New York at Stony Brook, Stony Brook, NY, 11794-5215, USA

    Shoko Ueki & Vitaly Citovsky

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  1. Raul Zavaliev
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  2. Shoko Ueki
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  3. Bernard L. Epel
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Correspondence to Bernard L. Epel.

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Handling Editor: Karl Oparka

Raul Zavaliev and Shoko Ueki contributed equally to this manuscript.

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Zavaliev, R., Ueki, S., Epel, B.L. et al. Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma 248, 117–130 (2011). https://doi.org/10.1007/s00709-010-0247-0

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