Advertisement

Mycological Progress

, Volume 17, Issue 11, pp 1237–1249 | Cite as

Phylogenetics and histology provide insight into damping-off infections of ‘Poblano’ pepper seedlings caused by Fusarium wilt in greenhouses

  • Mally N. Rivera-Jiménez
  • Hilda A. Zavaleta-Mancera
  • Angel Rebollar-Alviter
  • Víctor H. Aguilar-Rincón
  • Gabino García-de-los-Santos
  • H. Vaquera-Huerta
  • Hilda Victoria Silva-Rojas
Original Article

Abstract

The ‘Poblano’ pepper crop is economically important in Mexico and throughout the world as it is used as a hot spice in food. The cultivated area of the ‘Poblano’ pepper crop is decreasing yearly for many reasons, among them a wilt disease commonly associated with Fusarium spp. This disease is a problem of field and greenhouse production plants. Moreover, it is not clear whether the pathogens that cause wilt in mature plants are the same as those involved in the damping-off symptoms and death of pepper seedlings in greenhouses. For this reason, the aim of the present study was to identify the causal agent of damping-off in pepper during seedling production, establish its relationship with the causal agent of wilting in mature plants, and determine whether histological damage in seedlings occurs. Isolates were recovered from the crown rot and stem base of 4-month-old infected ‘Poblano’ mature pepper plants and were identified using morphological and phylogenetic approaches. Fusarium oxysporum and F. solani were isolated from the crown rot and base stem, respectively. A pathogenicity test showed that both species caused damping-off in pepper seedlings. Histological studies with inoculated seedlings of both isolates showed several changes in the external cortex, epidermal cells, endodermis, Casparian strips, cell size, and xylem wall. Casparian strip rupture resulted in permeability loss and regulatory activity to maintain the cellular equilibrium inside the vascular bundles. Hence, according to these findings, producers should avoid seedling contamination by infected mature plants because the aggressiveness of Fusarium isolates can cause rapid seedling mortality.

Keywords

Capsicum annuum Casparian strips Crown rot Canker Histopathology Identification 

Notes

Acknowledgements

The authors wish to thank CONACYT for their support of this research reported through a scholarship assigned to the first author to obtain her doctoral degree. The authors also thank Greta Nanako Rosales-Saito for her assistance with the light and electron micrographs.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402CrossRefGoogle Scholar
  2. Beckman CH (1987) The nature of wilt diseases of plants. American Phytopathological Society Press, St PaulGoogle Scholar
  3. Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40:48–53CrossRefGoogle Scholar
  4. Booth C (1971) The genus Fusarium. Commonwealth Mycological Institute. Kew, Surrey, EnglandGoogle Scholar
  5. Burgess LW, Summerell BA, Bullock S, Gott KP, Backhouse D (1994) Laboratory manual for Fusarium research. The University of Sydney and The Royal Botanic Gardens, Sydney, AustraliaGoogle Scholar
  6. Chialva M, di Fossalunga AS, Daghino S, Ghignone S, Bagnaresi P, Chiapello M, Novero M, Spadaro D, Perotto S, Bonfante P (2018) Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytol.  https://doi.org/10.1111/nph.15014
  7. Collmer A, Keen NT (1986) The role of pectic enzymes in plant pathogenesis. Annu Rev Phytopathol 24:383–409CrossRefGoogle Scholar
  8. Dale J, James A, Paul JY, Khanna H, Smith M, Peraza-Echeverria S, Garcia-Bastidas F, Kema G, Waterhouse P, Mengersen K, Harding R (2017) Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4. Nat Commun 8(1):1496CrossRefGoogle Scholar
  9. Di Pietro A, Madrid MP, Caracuel Z, Delgado-Jarana J, Roncero MIG (2003) Fusarium oxysporum exploring the molecular arsenal of a vascular wilt fungus. Mol Plant Pathol 4(5):315–325CrossRefGoogle Scholar
  10. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12(1):13–15Google Scholar
  11. FAOSTAT (2015) Food and Agriculture Organization of the United Nations. Statistical, Agricultural Production. On-line [http://faostat.fao.org/site/342/default.aspx]. Accessed 10.02.2015
  12. FAOSTAT (2017) Food and agriculture organization of the united nations. Statistical, agricultural production. On-line [http://wwwfaoorg/faostat/en/#data/QC] Accessed 08.02.2018
  13. Fayzalla EA, Shabana YM, Mahmoud NS (2008) Effect of environmental conditions on wilting and root rot fungi pathogenic to solanaceous plants. Plant Pathol J 7(1):27–33CrossRefGoogle Scholar
  14. Ferniah RS, Daryono BS, Kasiamdari RS, Priyatmojo A (2014) Characterization and pathogenicity of Fusarium oxysporum as the causal agent of Fusarium wilt in chili (Capsicum annuum L.). Microbiology 8(3):121–126Google Scholar
  15. Fisher NL, Burgess LW, Toussoun TA, Nelson PE (1982) Carnation leaves as a substrate and for preserving cultures of Fusarium species. Phytopathology 72:151–153CrossRefGoogle Scholar
  16. Geiser DM, Jimenez-Gasco MM, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zheng N, Kuldau GA, O’Donnell K (2004) FUSARIUM-ID v.1.0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110(5):473–479CrossRefGoogle Scholar
  17. Geiser DM, Aoki T, Bacon CW, Baker SE, Bhattacharyya MK, Brandt ME, Brown DW, Burgess LW, Chulze S, Colemann JJ, Correll JC, Covert SF, Crous PW et al (2013) One fungus, one name: defining the genus Fusarium is a scientifically robust way that preserves longstanding use. Phytopathology 103(5):400–408CrossRefGoogle Scholar
  18. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420CrossRefGoogle Scholar
  19. Goodman NR, Király Z, Wood KR (1986) The biochemistry and physiology of plant disease. University of Missouri Press, ColumbiaGoogle Scholar
  20. Gordon TR (2017) Fusarium oxysporum and the Fusarium wilt syndrome. Annu Rev Phytophathol 55:23–39.  https://doi.org/10.1146/annurev-phyto-080615-095919 CrossRefGoogle Scholar
  21. Guadet J, Julien J, Lafay JF, Brygoo Y (1989) Phylogenetics of some Fusarium species, as determined by large-subunit rRNA sequence comparison. Mol Biol Evol 6(3):227–242PubMedGoogle Scholar
  22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  23. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755CrossRefGoogle Scholar
  24. Iwahara S, Nishihira T, Jomori T, Kuwahara M, Higuchi T (1980) Enzymatic oxidation of α,β unsaturated alcohols in the side chains of lignin-related aromatic compounds. J Ferment Technol 58:183–188Google Scholar
  25. Jones TM, Anderson AJ, Albersheim P (1972) Host-pathogen interactions IV. Studies on the polysaccharide degrading enzymes secreted by Fusarium oxysporum f. sp. lycopersici. Physiol Plant Pathol 2(2):153–166CrossRefGoogle Scholar
  26. Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing Professional, AmesCrossRefGoogle Scholar
  27. Lievens B, Rep M, Thomma BPHJ (2008) Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. Pest Manag Sci 64(8):781–788CrossRefGoogle Scholar
  28. Llop C, Pujol I, Aguilar C, Sala J, Riba D, Guarro J (2000) Comparison of three methods of determining MICs for filamentous fungi using different end point criteria and incubation periods. Antimicrob Agents Chemother 44(2):239–242CrossRefGoogle Scholar
  29. Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10(3):311–324CrossRefGoogle Scholar
  30. Nelson PE, Toussoun TA, Marasas WFO (1983) Fusarium species: an illustrated manual for identification. The Pennsylvania State University Press, USAGoogle Scholar
  31. O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci USA 95(5):2044–2049CrossRefGoogle Scholar
  32. O’Donnell K, Sutton DA, Wiederhold N, Robert VARG, Crous PW, Geiser DM (2016) Veterinary fusarioses within the United States. J Clin Microbiol 54(11):2813–2819CrossRefGoogle Scholar
  33. Perez-Hernandez A, Serrano-Alonso Y, Aguilar-Perez MI, Gomez-Uroz R (2014) Damping-off and root rot of pepper caused by Fusarium oxysporum in Almería province, Spain. Plant Dis 98(8):159CrossRefGoogle Scholar
  34. Punja ZK, Parker M (2000) Development of Fusarium root and stem rot, a new disease on greenhouse cucumber in British Columbia, caused by Fusarium oxysporum f. sp. radicis-cucumerinum. Can J Plant Pathol 22(4):349–363CrossRefGoogle Scholar
  35. Rekah Y, Shtienberg D, Katan J (2000) Disease development following infection of tomato and basil foliage by airborne conidia of the soilborne pathogens Fusarium oxysporum f. sp. radicis-lycopersici and F. oxysporum f. sp. basilici. Phytopathology 90(12):1322–1329CrossRefGoogle Scholar
  36. Robbins NE II, Trontin C, Duan L, Dinneny JR (2014) Beyond the barrier: communication in the root through the endodermis. Plant Physiol 166:551–559CrossRefGoogle Scholar
  37. Roncero MIG, Hera C, Ruiz RM, García MFI, Madrid MP, Caracuel Z (2003) Fusarium as a model for studying virulence in soilborne plant pathogens. Physiol Mol Plant Pathol 62(2):87–98CrossRefGoogle Scholar
  38. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574CrossRefGoogle Scholar
  39. Ruzin ES (1999) Plant microtechnique and microscopy. Oxford University Press, OxfordGoogle Scholar
  40. Schreiber L, Franke RB (2011) Endodermis and exodermis in roots. In: John Wiley and Sons Ltd, Chichester  https://doi.org/10.1002/9780470015902.a0002086.pub2
  41. Schumann GL, D’Arcy CJ (2009) Essential plant pathology. The American Phytopathology Society Press, St. PaulGoogle Scholar
  42. SIAP (2017) Agrifood and fisheries information service. Statistics. Available on https://www.gob.mx/siap/acciones-y-programas/produccion-agricola-33119
  43. Singh VK, Singh HB, Upadhyay RS (2017) Role of fusaric acid in the development of Fusarium wilt symptoms in tomato: physiological, biochemical and proteomic perspectives. Plant Physiol Biochem 118:320–332CrossRefGoogle Scholar
  44. Sundaramoorthy S, Raguchander T, Ragupathi N, Samiyappan R (2012) Combinatorial effect of endophytic and plant growth promoting rhizobacteria against wilt disease of Capsicum annum L. caused by Fusarium solani. Biol Control 60(1):59–67Google Scholar
  45. Vasquez-Lopez A, Tlapal BB, Yañez-Morales MJ, Pacheco PR, Quintos EM (2009) Etiology of pepper wilt disease of ‘Chile de agua’ (Capsicum annuum L.) in Oaxaca, Mexico. Rev Fitotec Mex 32(2):127–134Google Scholar
  46. Wang C, Ulloa M, Duong T, Roberts PA (2018) QTL of multiple independent loci for resistance to Fusarium oxysporum f. sp. vasinfectum races 1 and 4 in an interspecific cotton population. Phytopathology 108(6):759–767CrossRefGoogle Scholar
  47. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  48. Yadeta AK, Thomma BPHJ (2013) The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci 4(97):1–12.  https://doi.org/10.3389/fpls.2013.00097 eCollection 2013CrossRefGoogle Scholar
  49. Zavaleta-Mancera HA, Engleman EM (1994) Anatomy of the ovule and seed of Manilkara zapota (L.) van Royen (Sapotaceae). Phytomorphology 44:169–175Google Scholar
  50. Zhang N, Geiser DM, Smart CD (2007) Macroarray detection of solanaceous plant pathogens in the Fusarium solani species complex. Plant Dis 91(12):1612–1620CrossRefGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Mally N. Rivera-Jiménez
    • 1
  • Hilda A. Zavaleta-Mancera
    • 2
  • Angel Rebollar-Alviter
    • 3
  • Víctor H. Aguilar-Rincón
    • 1
  • Gabino García-de-los-Santos
    • 1
  • H. Vaquera-Huerta
    • 4
  • Hilda Victoria Silva-Rojas
    • 1
  1. 1.Posgrado en Recursos Geneticos y ProductividadColegio de Postgraduados, Campus MontecilloTexcocoMexico
  2. 2.Posgrado en BotanicaColegio de Postgraduados, Campus MontecilloTexcocoMexico
  3. 3.Centro Regional Morelia, Universidad Autonoma ChapingoMoreliaMexico
  4. 4.Posgrado en EstadísticaColegio de Postgraduados, Campus MontecilloTexcocoMexico

Personalised recommendations