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Polyamines levels increase in smut teliospores after contact with sugarcane glycoproteins as a plant defensive mechanism

  • Elena Sánchez-Elordi
  • Laura Morales de los Ríos
  • Carlos VicenteEmail author
  • María-Estrella Legaz
Regular Paper
  • 29 Downloads

Abstract

Previous studies have already highlighted the correlation between Sporisorium scitamineum pathogenicity and sugarcane polyamine accumulation. It was shown that high infectivity correlates with an increase in the amount of spermidine, spermine and cadaverine conjugated to phenols in the sensitive cultivars whereas resistant plants mainly produce free putrescine. However, these previous studies did not clarify the role of these polyamides in the disorders caused to the plant. Therefore, the purpose of this research is to clarify the effect of polyamines on the development of smut disease. In this paper, commercial polyamines were firstly assayed on smut teliospores germination. Secondly, effects were correlated to changes in endogenous polyamines after contact with defense sugarcane glycoproteins. Low concentrations of spermidine significantly activated teliospore germination, while putrescine had no activating effect on germination. Interestingly, it was observed that the diamine caused nuclear decondensation and breakage of the teliospore cell wall whereas the treatment of teliospores with spermidine did not induce nuclear decondensation or cell wall breakdown. Moreover, the number of polymerized microtubules increased in the presence of 7.5 mM spermidine but it decreased with putrescine which indicates that polyamines effects on Sporisorium scitamineum teliospore germination could be mediated through microtubules interaction. An increased production of polyamines in smut teliospores has been related to sugarcane resistance to the disease. Teliospores incubation with high molecular mass glycoproteins (HMMG) from the uninoculated resistant variety of sugarcane, Mayari 55-14, caused an increase of the insoluble fraction of putrescine, spermidine and spermine inside the teliospore cells. Moreover, the level of the soluble fraction of spermidine (S fraction) increased inside teliospores and the excess was released to the medium. The HMMG glycoproteins purified from Mayarí 55-14 plants previously inoculated with the pathogen significantly increased the levels of both retained and secreted soluble putrescine and spermidine. Polyamines levels did not increase in teliospores after incubation with HMMG produced by non resistant variety Barbados 42231 which could be related to the incapacity of these plants to defend themselves against smut disease. Thus, a hypothesis about the role of polyamines in sugarcane-smut interaction is explained.

Keywords

Microtubules Putrescine Smut Spermidine Spermine Sugarcane Teliospores 

Abbreviations

B 42231

Barbados 42231 cv.

cv

Cultivar

DAPI

4,6-diamidino-2-phenylindole

EGTA

Ethylene glycol-bis(2-aminoethylether)-N,N,N′,N′-tetraacetic acid

HMMG

High molecular mass glycoproteins

HMPB

High Molarity Pipes Buffer

MMMG

Mid molecular mass glycoproteins

MT

Microtubules;

My 55-14

Mayarí 55-14 cv.

ODH

Ornithine decarboxylase

PA

Polyamine

PBS

Phosphate saline buffer

PH

Insoluble conjugated polyamine fraction

PIPES

Piperazine-N,N′-bis(2-ethanesulfonic acid)

PVP

Polyvinylpyrrolidone

PUT

Putrescine

SPD

Spermidine

SPM

Spermine

S

Soluble, free polyamine fraction

SH

Soluble conjugated polyamine fraction

Notes

References

  1. Arce L, Ríos A, Valcárcel M (1997) Selective and rapid determination of biogenicamines by capillary zone electrophoresis. Chromatographia 46:170–176CrossRefGoogle Scholar
  2. Benevenuto J, Teixeira-Silva NS, Kuramae EE, Croll D, Monteiro-Vitorello CB (2018) Comparative genomics of smut pathogens: insights from orphans and positively selected genes into host specialization. Front Plant Sci 9:660CrossRefGoogle Scholar
  3. Brauc S, de Vooght E, Claeys M, Geuns JMC, Höfte M, Angenon G (2012) Overexpression of arginase in Arabidopsis thaliana influences defence responses against Botrytis cinerea. Plant Biol 14:39–45CrossRefGoogle Scholar
  4. Carvalho G, Quecine MC, Longatto DP, Peters LP, Almeida JR, Shyton TG, Silva MML, Crestana GS, Crete S, Monteiro-Vitorello CB (2016) Sporisorium scitamineum colonisation of sugarcane genotypes susceptible and resistant to smut revealed by GFP-tagged strains. Annal Appl Biol 169:329–341CrossRefGoogle Scholar
  5. Castoldi M, Popov AV (2003) Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr Purif 32:83–88CrossRefGoogle Scholar
  6. Charnay D, Nari J, Noat G (1992) Regulation of plant cell-wall pectin methyl esterase by polyamines—Interactions with the effects of metal ions. Eur J Biochem 205:711–714CrossRefGoogle Scholar
  7. Fontaniella B, Márquez A, Rodríguez CW, Piñón D, Solas MT, Vicente C, Legaz ME (2002) A role for sugarcane glycoproteins in the resistance of sugarcane to Ustilago scitaminea. Plant Physiol Biochem 40:881–889CrossRefGoogle Scholar
  8. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33CrossRefGoogle Scholar
  9. Grant NJ, Oriol-Audit C, Dickens MJ (1983) Supramolecular forms of actin induced by polyamines; an electron microscopic study. Eur J Cell Biol 30:67–73Google Scholar
  10. Guevara-Olvera L, Xoconostle-Cázares B, Ruiz-Herrera J (1997) Cloning and disruption of the ornithine decarboxylase gene of Ustilago maydis: evidence for a role of polyamines in its dimorphic transition. Microbiology 143:2237–2245CrossRefGoogle Scholar
  11. Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35:2015–2036CrossRefGoogle Scholar
  12. Kadotani N, Nakayashiki H, Tosa Y, Mayama S (2003) RNA Silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol Plant Microb Interact 16:769–776CrossRefGoogle Scholar
  13. Khatri M, Rajam MV (2007) Targeting polyamines of Aspergillus nidulans by siRNA specific to fungal ornithine decarboxylase gene. Med Mycol 45:211–220CrossRefGoogle Scholar
  14. Legaz ME, Pedrosa MM, Martínez M, Vicente C (1995) Soluble glycoproteins from sugarcane juice analyzed by SE-HPLC and fluorescence emission. J Chromatogr 697:329–335CrossRefGoogle Scholar
  15. Legaz ME, de Armas R, Piñón D, Vicente C (1998a) Relationships between phenolics-conjugated polyamines and sensitivity of sugarcane to smut (Ustilago scitaminea). J Exp Bot 49:1723–1728CrossRefGoogle Scholar
  16. Legaz ME, Pedrosa MM, de Armas R, Rodríguez CW, de los Ríos V, Vicente C (1998b) Separation of soluble glycoproteins from sugarcane juice by capillary electrophoresis. Anal Chim Acta 372:201–208CrossRefGoogle Scholar
  17. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  18. Marques JPR, Appezzato-da-Glória B, Pipebring M, Massola N, Monteiro-Vitorello CB, Vieira MLC (2017) Sugarcane smut: shedding light on the development of the whip shaped sorus. Ann Bot 11:815–827Google Scholar
  19. Marques JP, Hoy JW, Appezzato-da-Glória B, Viveros AF, Vieira ML, Baisakh N (2018) Sugarcane cell wall-associated defense responses to infection by Sporisorium scitamineum. Front Plant Sci 9:698CrossRefGoogle Scholar
  20. Mechulam A, Chernov KG, Mucher E, Hamon L, Curmi PA, Pastré D (2009) Polyamine sharing between tubulin dimers favours microtubule nucleation and elongation via facilitated diffusion. PLoS Comput Biol 5:e1000255CrossRefGoogle Scholar
  21. Millanes AM, Fontaniella B, Legaz ME, Vicente C (2005) Glycoproteins from sugarcane plants regulate cell polarity of Ustilago scitaminea teliospores. J Plant Physiol 162:253–265CrossRefGoogle Scholar
  22. Piñón D, de Armas R, Vicente C, Legaz ME (1999) Role of polyamines in the infection of sugarcane buds by Ustilago scitaminea spores. Plant Physiol Biochem 37:57–64CrossRefGoogle Scholar
  23. Pohjanpelto P, Virtanen I, Hölttä E (1981) Polyamine starvation causes disappearance of actin filaments and microtubules in polyamine-auxotrophic CHO cells. Nature 293:475–477CrossRefGoogle Scholar
  24. Que Y, Xu L, Wu Q, Liu Y, Ling H, Liu Y, Zhang Y, Guo J, Su Y, Chen J, Wang S, Zhang C (2014) Genome sequencing of Sporisorium scitamineum provides insights into the pathogenic mechanisms of sugarcane smut. BMC genom 15:1CrossRefGoogle Scholar
  25. Rajam MV, Galston AW (1985) The effects of some polyamine biosynthetic inhibitors on growth and morphology of phytopathogenic fungi. Plant Cell Physiol 26:683–692CrossRefGoogle Scholar
  26. Rajam MV, Weinstein LH, Galston AW (1985) Prevention of a plant disease by specific inhibition of fungal polyamine biosynthesis. Proc Nat Acad Sci 82:6874–6878CrossRefGoogle Scholar
  27. Sánchez-Elordi E, de los Ríos LM, Vicente C, Legaz ME (2015) Sugarcane arginase competes with the same fungal enzyme as a false quorum signal against smut teliospores. Phytochem Lett 14:115–122CrossRefGoogle Scholar
  28. Sánchez-Elordi E, Baluska F, Echevarría C, Vicente C, Legaz ME (2016a) Defence sugarcane glycoproteins disorganize microtubules and prevent nuclear polarization and germination of Sporisorium scitamineum teliospores. J Plant Physiol 200:111–123CrossRefGoogle Scholar
  29. Sánchez-Elordi E, Vicente-Manzanares M, Díaz E, Legaz ME, Vicente C (2016b) Plant-pathogen interactions: sugarcane glycoproteins induce chemotaxis of smut teliospores by cyclic contraction and relaxation of the cytoskeleton. South Afr J Bot 105:66–78CrossRefGoogle Scholar
  30. Sánchez-Elordi E, Contreras R, de Armas R, Benito MC, Alarcón B, de Oliveira E, del Mazo C, Díaz-Peña EM, Santiago R, Vicente C, Legaz ME (2108) Differential expression of SofDIR16 and SofCAD genes in smut resistant and susceptible sugarcane cultivars in response to Sporisorium scitamineum. J Plant Physiol 226:103–113CrossRefGoogle Scholar
  31. Savarin P, Barbet A, Delga S, Joshi V, Hamon L, Lefevre J, Nakib S, de Bandt JP, Moinard C, Curmi PA, Pastré D (2010) A central role for polyamines in microtubule assembly in cells. Biochem J 430:151–159CrossRefGoogle Scholar
  32. Takao K, Rickhag M, Hegardt C, Oredsson S, Persson L (2006) Induction of apoptotic cell death by putrescine. Int J Biochem Cell Biol 38:621–628CrossRefGoogle Scholar
  33. Trione EJ (1990) Growth and sporulation of Ustilago scitaminea, in vivo and in vitro. Mycol Res 94:489–493CrossRefGoogle Scholar
  34. Valdés-Santiago L, Cervantes-Chávez JA, Ruiz-Herrera J (2009) Ustilago maydis spermidine synthase is encoded by a chimeric gene, required for morphogenesis, and indispensable for survival in the host. FEMS Yeast Res 9:923–935CrossRefGoogle Scholar
  35. Valdés-Santiago L, Guzmán de Peña D, Ruiz-Herrera J (2010) Life without putrescine: disruption of the gene-encoding polyamine oxidase in Ustilago maydis odc mutants. FEMS Yeast Res 10:928–940CrossRefGoogle Scholar
  36. Valdés-Santiago L, Cervantes-Chávez JA, Geraldine León-Ramírez C, Ruiz-Herrera J (2012) Polyamine metabolism in fungi with emphasis on phytopathogenic species. J Amino Acids.  https://doi.org/10.1155/2012/837932 Google Scholar
  37. Waller JM (1970) Sugarcane smut (Ustilago scitaminea) in Kenya: infection and resistance. Trans Br Mycol Soc 54:405–414CrossRefGoogle Scholar
  38. Walters DR (1995) Inhibition of polyamine biosynthesis in fungi. Mycol Res 199:129–139CrossRefGoogle Scholar
  39. Walters D (2003) Research review: Resistance to plant pathogens: possible roles for free polyamines and polyamine catabolism. New Phytol 159:109–115CrossRefGoogle Scholar
  40. West HM, Walters DR (1989) Effects of polyamine biosynthesis inhibitors on growth of Pyrenophora teres, Gaeumannomyces graminis, Fusarium culmorum and Septoria nodorum in vitro. Mycol Res 92:453–457CrossRefGoogle Scholar
  41. Wojtasik W, Kulma A, Namysł K, Preisner M, Szopa J (2015) Polyamine metabolism in flax in response to treatment with pathogenic and non-pathogenic Fusarium strains. Front Plant Sci 6:291CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Elena Sánchez-Elordi
    • 1
  • Laura Morales de los Ríos
    • 1
  • Carlos Vicente
    • 1
    Email author
  • María-Estrella Legaz
    • 1
  1. 1.Team of Cell Interactions in Plant Symbioses, Faculty of BiologyComplutense UniversityMadridSpain

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