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Effects of the Papaya meleira virus on papaya latex structure and composition

  • Biotic and Abiotic Stress
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Abstract

Spontaneous latex exudation is the main symptom of papaya sticky (meleira) disease caused by the Papaya meleira virus (PMeV), a double-stranded RNA (dsRNA) virus. This paper describes different effects of PMeV on papaya latex. Latex samples were subjected to different histochemical tests to evaluate their chemical composition. Additionally, the integrity of the latex particles was assessed by transmission and scanning electron microscopy analysis. Biochemical and micro- and macro-element measurements were performed. PMeV dsRNA extraction was performed to evaluate the interaction of the virus with the latex particles. Sticky diseased latex was positive for alkaloid biosynthesis and showed an accumulation of calcium oxalate crystals. PMeV also increased H2O2 synthesis within sticky diseased laticifers. The protein, sugar and water levels were altered, probably due to chemical changes. The morphology of the latex particles was further altered; PMeV particles seemed to be bound to the latex particles. The alkaloid and H2O2 biosynthesis in the papaya laticifers indicate a papaya defense response against PMeV. However, such efforts failed, as the virus affected the plant latex. The effects described here suggest some advantages of the infection process, including facilitating the movement of the virus within the papaya plant.

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References

  • An T, Huang H, Yang Z, Zhang D, Li G, Yao Y, Gao J (2001) Alkaloids from Cynanchum komarovii with inhibitory activity against the Tobacco mosaic virus. Phytochemistry 58:1267–1269

    Article  PubMed  CAS  Google Scholar 

  • Araújo MMM, Tavares ET, Silva FR, Marinho VLA, Souza Júnior MT (2007) Molecular detection of Papaya meleira virus in the latex of Carica papaya by RT-PCR. J Virol Methods 146:305–310

    Article  PubMed  Google Scholar 

  • Azarkan M, Dibiani R, Baulard C, Baeyens-Volant D (2006) Effects of mechanical wounding on Carica papaya cysteine endopeptidases accumulation and activity. Int J Biol Macromol 38:216–224

    Article  PubMed  CAS  Google Scholar 

  • Borchert R (1986) Calcium acetate induces calcium uptake and formation of calcium-oxalate crystals in isolated leaflets of Gleditsia triacanthos L. Planta 168:571–578

    Article  CAS  Google Scholar 

  • Bouteau F, Lacrotte R, Cornel D, Monestiez M, Bousquet U, Pennarun AM, Rona JP (1991) Electrogenic active proton pump in Hevea brasiliensis laticiferous cells its role in activating sucrose/H+ and glucose/H+ symports at the plasma membrane. Bioelectrochem Bioenerg 26:223–236

    Article  CAS  Google Scholar 

  • Bouteau F, Bousquet U, Pennarun AM, Convert M, Dellis O, Cornel D, Ronal JP (1996) Time dependent K+ currents through plasmalemma of laticifer protoplasts from Hevea brasiliensis. Physiol Plant 98:97–104

    Article  CAS  Google Scholar 

  • Bouteau F, Dellis O, Bousquet U, Rona JP (1999) Evidence of multiple sugar uptake across the plasma membrane of laticifer protoplasts from Hevea. Bioelectrochem Bioenerg 48:135–139

    Article  PubMed  CAS  Google Scholar 

  • Bravo LM, Hermosilla J, Salas CE (1994) A biochemical comparison between latex from Carica candamarcensis and C. Papaya. Braz J Med Biol Res 27:2831–2842

    PubMed  CAS  Google Scholar 

  • Calvin M (1987) Fuel oils from euphorbs and other plants. Bot J Linn Soc 94:97–110

    Article  Google Scholar 

  • Chaykin S, Law J, Philipis AH, Tchen TT, Bloch K (1958) Phosphorylated intermediates in the synthesis of squalene. Proc Natl Acad Sci USA 44:998–1004

    Article  PubMed  CAS  Google Scholar 

  • Chow KS, Wan KL, Isa MNM, Baharil A, Tan SH, Harikrishna K, Yeang HY (2007) Insights into rubber biosynthesis from transcriptome analysis of Hevea brasiliensis latex. J Exp Bot 58:2429–2440

    Article  PubMed  CAS  Google Scholar 

  • Da Cunha M, Gomes VM, Xavier-Filho J, Attias M, Souza W, Miguens FC (2000) The laticifer system of Chamaesyce thymifolia: a closed host environment for plant Trypanosomatids. Biocell 24:123–132

    PubMed  CAS  Google Scholar 

  • Davis MJ, Kramer JB, Ferwerda FH, Brunner BR (1996) Association of a bacterium and not a phytoplasm with papaya bunchy top disease. Phytopathology 86:102–109

    Article  Google Scholar 

  • El Moussaoui A, Nijs M, Paul C, Wintjens R, Vincentelli J, Azarkan M, Looze Y (2001) Revisiting the enzymes stored in the laticifers of Carica papaya in the context of their possible participation in the plant defense mechanism. Cell Mol Life Sci 58:556–570

    Article  CAS  Google Scholar 

  • Esaú K (1976) Anatomía Vegetal, 3rd edn. Ediciones Omega, Barcelona

    Google Scholar 

  • Ferrar PH, Walker JRL (1993) o-Diphenol oxidase inhibition—an additional role for oxalic acid in the phytopathogenic arsenal of Sclerotinia sclerotiorum and Sclerotium rolfsii. Physiol Mol Plant Pathol 43:415–422

    Article  CAS  Google Scholar 

  • Gidrol X, Chrestin H, Tan H, Kush A (1994) Hevein, a lectin-like protein from Hevea brasiliensis (rubber tree) is involved in the coagulation of latex. J Biol Chem 269:9278–9283

    PubMed  CAS  Google Scholar 

  • Guimarães RL, Stotz HU (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 136:3703–3711

    Article  PubMed  Google Scholar 

  • Hunter JR (1994) Reconsidering the functions of latex. Trees 9:1–5

    Article  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry, principles and practice. W.H. Freeman, San Francisco

    Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Kitajima EW, Rodrigues C, Silveira J, Alves FL, Ventura JA, Aragão FJL, Oliveira LHR (1993) Association of isometric vírus-like particles, restricted to laticifers, with “meleira” (“sticky disease”) of papaya (Carica papaya). Fitopatol Bras 18:118–122

    Google Scholar 

  • Kraus JE, Arduin M (1997) Manual básico de métodos em morfologia vegetal. EDUR, Seropédica

    Google Scholar 

  • Kronberg K, Vogel F, Rutten T, Hajirezaei MR, Sonnewald U, Hofius D (2007) The silver lining of a viral agent: increasing seed yield and harvest index in Arabidopsis by ectopic expression of the potato leaf roll virus movement protein. Plant Physiol 145:905–918

    Article  PubMed  CAS  Google Scholar 

  • Lane BG (1994) Oxalate, germin, and extracellular matrix of higher plants. FASEB J 5:12239–12242

    Google Scholar 

  • Lane BG (2002) Oxalate, germins, and higher-plant pathogens. IUBMB Life 53:67–75

    Article  PubMed  CAS  Google Scholar 

  • Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a marker protein of early plant growth, is an oxalate oxidase. J Biol Chem 268:12239–12242

    PubMed  CAS  Google Scholar 

  • Lebaudy A, Véry AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Ma Y, Zhou T, Hong Y, Fan Z, Li H (2008) Decreased level of ferredoxin I in Tobacco mosaic virus-infected tobacco is associated with development of the mosaic symptom. doi:10.1016/j.pmpp.2008.05.004

  • Miller RO (1997) Nitric-perchloric acid wet digestion in an open vessel. In: Kalra YP (ed) Soil and plant analysis. CRC Press, Edmonton

    Google Scholar 

  • Moutim V, Silva LG, Lopes MTP, Wilson Fernandes G, Salas CE (1999) Spontaneous processing of peptides during coagulation of latex from Carica papaya. Plant Sci 142:115–121

    Article  CAS  Google Scholar 

  • Nawrot R, Kalinowski A, Gozdzicka-Jozefiak A (2007) Proteomic analysis of Chelidonium majus milky sap using two-dimensional gel electrophoresis and tandem mass spectrometry. Phytochemistry 68:1612–1622

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cárdenas ML, Ryan C (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and system in via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557

    Article  PubMed  Google Scholar 

  • Pickard WF (2008) Laticifers and secretory ducts: two other tube systems in plants. New Phytol 177:877–888

    Article  PubMed  Google Scholar 

  • Purvis MJ, Collier DC, Walls D (1964) Laboratory techniques in botany. Butterwoths, London

    Google Scholar 

  • Radwan DE, Fayez KA, Mahmoud SY, Hamad A, Lu G (2007) Physiological and metabolic changes of Cucurbita pepo leaves in response to zucchini yellow mosaic virus (ZYMV) infection and salicylic acid treatments. Plant Physiol Biochem 45:480–489

    Article  PubMed  CAS  Google Scholar 

  • Rinne PL, van den Boogaard R, Mensink MG, Kopperud C, Kormelink R, Goldbach R, van der Schoot C (2005) Tobacco plants respond to the constitutive expression of the tospovirus movement protein NS(M) with a heat-reversible sealing of plasmodesmata that impairs development. Plant J 43:688–707

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues CH, Ventura JA, Marin SLD (1989) Ocorrência e sintomas da meleira do mamoeiro (Carica papaya) no Estado do Espírito Santo. Fitopatol Bras 14:118

    Google Scholar 

  • Rodrigues SP, Galvão OP, Andrade JS, Ventura JA, Fernandes PMB (2005) Simple molecular method to papaya sticky disease detection from latex and tissues samples. Summa Phytopatol 31:273–275

    Google Scholar 

  • Sajnani C, Zurita JL, Roncel M, Ortega JM, Baron M, Ducruet JM (2007) Changes in photosynthetic metabolism induced by tobamovirus infection in Nicotiana benthamiana studied in vivo by thermoluminescence. New phytol 175:120–130

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Alcantara J, Bourgault R, Zulak KG, Facchini PJ (2006) The role of phloem sieve elements and laticifers in biosynthesis and accumulation of alkaloids in opium. Plant J 47:547–563

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Hedrich R, Fernandez JM (1984) Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312:361–362

    Article  CAS  Google Scholar 

  • Scott TA Jr, Melvin EH (1953) Determination of dextran with anthrone. Anal Chem 11:1656–1661

    Article  Google Scholar 

  • Stuart NW (1936) Adaptation of the micro-Kjedahl method for the determination of nitrogen in plant tissues. Plant Physiol 11:173–179

    Article  PubMed  CAS  Google Scholar 

  • Ventura JA, Costa H, Tatagiba JS (2001) Sintomatologia da meleira do mamoeiro e sua importância para o “roguing”. Fitopatol Bras 26:536

    Google Scholar 

  • Ventura JA, Costa H, Tatagiba J, da S (2004) Papaya diseases and integrated control. In: Naqvi SAH (ed) Diseases of fruits and vegetables: diagnosis and management. Kluwer, London

    Google Scholar 

  • Wititsuwannakul R, Pasitkul P, Kanokwiroon K, Wititsuwannakul D (2008a) A role for a Hevea latex lectin-like protein in mediating rubber particle aggregation and latex coagulation. Phytochemistry 69:339–347

    Article  PubMed  CAS  Google Scholar 

  • Wititsuwannakul R, Rukseree K, Kanokwiroon K, Wititsuwannakul D (2008b) A rubber particle protein specific for Hevea latex lectin binding involved in latex coagulation. Phytochemistry 69:1111–1118

    Article  PubMed  CAS  Google Scholar 

  • Wititsuwannakul R, Pasitkul P, Jewtragoon P, Wititsuwannakul D (2008c) Hevea latex lectin binding protein in C-serum as an anti-latex coagulating factor and its role in a proposed new model for latex coagulation. Phytochemistry 69:656–662

    Article  PubMed  CAS  Google Scholar 

  • Yasue T (1969) Histochemical identification of calcium oxalate. Acta Histochem Cytochem 2:83–95

    CAS  Google Scholar 

  • Zambolim EM, Alonso SK, Matsuoka K, Carvalho MG, Zerbini FM (2003) Purification and some properties of Papaya meleira virus, a novel virus infecting papayas in Brazil. Plant Pathol 52:389–394

    Article  Google Scholar 

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Acknowledgments

This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Financiadora de Estudos e Projetos (FINEP) and Fundação de Apoio à Ciência e Tecnologia do Estado do Espírito Santo (FAPES). We thank Prof. Antônio Alberto R. Fernandes for helpful comments on this manuscript. We also thank João G.Z. Piccin for technical assistance.

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Authors and Affiliations

  1. Núcleo de Biotecnologia, Universidade Federal do Espírito Santo, Av. Marechal Campos 1498, Vitória, ES, 29040-090, Brazil

    Silas P. Rodrigues & Patricia Machado Bueno Fernandes

  2. Instituto Capixaba de Pesquisa Assistência Técnica e Extensão Rural, Rua Afonso Sarlo 160, Vitória, ES, 29052-010, Brazil

    José A. Ventura

  3. Instituto de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego 2000, Campos dos Goytacazes, RJ, 28013-602, Brazil

    Maura Da Cunha

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  1. Silas P. Rodrigues
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  2. Maura Da Cunha
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  3. José A. Ventura
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  4. Patricia Machado Bueno Fernandes
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Correspondence to Patricia Machado Bueno Fernandes.

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Communicated by H. Judelson.

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Rodrigues, S.P., Da Cunha, M., Ventura, J.A. et al. Effects of the Papaya meleira virus on papaya latex structure and composition. Plant Cell Rep 28, 861–871 (2009). https://doi.org/10.1007/s00299-009-0673-7

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  • DOI: https://doi.org/10.1007/s00299-009-0673-7

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