Skip to main content

Pathobiomes Revealed that Pseudomonas fuscovaginae and Sarocladium oryzae Are Independently Associated with Rice Sheath Rot


Rice sheath rot has been mainly associated with the bacterial pathogen Pseudomonas fuscovaginae and in some cases to the fungal pathogen Sarocladium oryzae; it is yet unclear if they are part of a complex disease. The bacterial and fungal community associated with rice sheath rot symptomatic and asymptomatic rice plants was determined/studied with the main aim to shed light on the pathogen(s) causing rice sheath rot. Plant samples were collected from different rice varieties in two locations (highland and lowland) in two rice-growing seasons (wet and dry season) in Burundi. Our results showed that the bacterial Pseudomonas genus was prevalent in highland in both rice-growing seasons and was not affected by rice plant varieties. Pseudomonas sequence reads displayed a significant high similarity to Pseudomonas fuscovaginae indicating that it is the causal agent of rice sheath rot as previously reported. The fungal Sarocladium genus was on the other hand prevalent in lowland only in the wet season; the sequence reads were most significantly similar to Sarocladium oryzae. These studies showed that plant microbiome analysis is very useful in determining the microorganisms involved in a plant disease. P. fuscovaginae and S. oryzae were prevalent in symptomatic samples in highland and lowland respectively being present independently and hence are not part of a complex disease. The significant presence of other bacterial and fungal taxa in symptomatic samples is also discussed possibly making this disease more complex. Finally, we also report the microbial communities that are associated with the plant sheath in symptomatic and asymptomatic plants from the same rice fields.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6



operational taxonomic unit


internal transcribed spacer


polymerase chain reaction


  1. 1.

    Tanii A, Miyajima K, Akita T (1976) The sheath brown rot disease of Rice Plant and its causal bacterium, Pseudomonas fuscovaginae A. Tanii, K. Miyajima et T. Akita sp. nov. Japanese J Phytopathol 42:540–548.

    Article  Google Scholar 

  2. 2.

    Duveiller E, Miyajima K, Snacken F, Autrique A, Maraite H (1988) Characterization of Pseudomonas fuscovaginae and differentiation from other fluorescent Pseudomonads occurring on rice in Burundi. J. Phytopathol. 122:97–107.

    Article  Google Scholar 

  3. 3.

    Rott P (1989) Identification and characterization of Pseudomonas fuscovaginae, the causal agent of bacterial sheath brown rot of rice, from Madagascar and other countries. Plant Dis. 73:133–137.

    Article  Google Scholar 

  4. 4.

    Zeigler RS (1987) Bacterial sheath brown rot of rice caused by Pseudomonas fuscovaginae in Latin America. Plant Dis. 71:592–597.

    Article  Google Scholar 

  5. 5.

    Cother EJ, Stodart B, Noble DH, Reinke R, van de Ven RJ (2009) Polyphasic identification of Pseudomonas fuscovaginae causing sheath and glume lesions on rice in Australia. Australas Plant Pathol. 38:247–261.

    Article  Google Scholar 

  6. 6.

    Kim J, Choi O, Kim WI (2015) First report of sheath brown rot of rice caused by Pseudomonas fuscovaginae in Korea. Plant Dis. 99:1033.

    Article  Google Scholar 

  7. 7.

    Cottyn B, Cerez MT, Mew TW (1994) Chapter 7: bacteria. In: Mew TW, Mistra JK (eds) A manual of seed health testing. IRRI, Manila, pp 322–328

    Google Scholar 

  8. 8.

    Bigirimana V d P, GKH H, Nyamangyoku OI, Hòfte M (2015) Rice sheath rot: an emerging ubiquitous destructive disease complex. Front Plant Sci. 6:1066.

    Article  PubMed Central  Google Scholar 

  9. 9.

    Ballio A, Bossa F, Camoni L, di Giorgio D, Flamand MC, Maraite H, Nitti G, Pucci P, Scaloni A (1996) Structure of fuscopeptins, phytotoxic metabolites of Pseudomonas fuscovaginae. FEBS Lett. 381:213–216.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Patel HK, Matiuzzo M, Bertani I, Bigirimana VP, Ash GJ, Höfte M, Venturi V (2014) Identification of virulence associated loci in the emerging broad host range plant pathogen Pseudomonas fuscovaginae. BMC Microbiol. 14:1–13.

    Article  Google Scholar 

  11. 11.

    Mattiuzzo M, Bertani I, Ferluga S, Cabrio L, Bigirimana J, Guarnaccia C, Pongor S, Maraite H, Venturi V (2011) The plant pathogen Pseudomonas fuscovaginae contains two conserved quorum sensing systems involved in virulence and negatively regulated by RsaL and the novel regulator RsaM. Environ Microbiol. 13:145–162.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Duveiller E (1989) First detection of Pseudomonas fuscovaginae on maize and sorghum in Burundi. Plant Dis. 73:514–517.

    Article  Google Scholar 

  13. 13.

    Purkayastha RP, Ghosal A (1985) Analysis of cross-reactive antigens of Acrocylindrium oryzae and rice in relation to sheath rot disease. Physiol. Plant Pathol. 27:245–252.

    Article  Google Scholar 

  14. 14.

    Bills GF, Platas G, Gams W (2004) Conspecificity of the cerulenin and helvolic acid producing “Cephalosporium caerulens”, and the hypocrealean fungus Sarocladium oryzae. Mycol. Res. 108:1291–1300.

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Sreenivasaprasad S, Johnson R, Pearce DA, et al (2001) Species concept in Sarocladium, the causal agent of sheath rot in rice and bamboo blight. In: Major fungal diseases of rice.

  16. 16.

    Desjardins AE, Plattner RD, Nelson PE (1997) Production of fumonisin B1and moniliformin by Gibberella fujikuroi from rice from various geographic areas. Appl Environ Microbiol 63(5):1838–1842

    CAS  Article  Google Scholar 

  17. 17.

    Abbas HK, Cartwright RD, Shier WT, Abouzied MM, Bird CB, Rice LG, Ross PF, Sciumbato GL, Meredith FI (1998) Natural occurrence of fumonisins in rice with Fusarium sheath rot disease. Plant Dis. 82:22–25.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Kushiro M, Saitoh H, Sugiura Y, Aoki T, Kawamoto SI, Sato T (2012) Experimental infection of Fusarium proliferatum in Oryza sativa plants; fumonisin B1 production and survival rate in grains. Int J Food Microbiol. 156:204–208.

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Aoki T, O’Donnell K, Geiser DM (2014) Systematics of key phytopathogenic Fusarium species: current status and future challenges. J Gen Plant Pathol 80:189–201.

    CAS  Article  Google Scholar 

  20. 20.

    Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ. Microbiol. 17:316–331.

    Article  PubMed  Google Scholar 

  21. 21.

    Dudenhöffer JH, Scheu S, Jousset A (2016) Systemic enrichment of antifungal traits in the rhizosphere microbiome after pathogen attack. J. Ecol. 104:1566–1575.

    CAS  Article  Google Scholar 

  22. 22.

    Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol Plant-Microbe Interact 28:212–217.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Vayssier-Taussat M, Albina E, Citti C, Cosson JF, Jacques MA, Lebrun MH, Le Loir Y, Ogliastro M, Petit MA, Roumagnac P, Candresse T (2014) Shifting the paradigm from pathogens to pathobiome new concepts in the light of meta-omics. Front. Cell. Infect. Microbiol. 4:29.

    Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One 7:e40863.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13:581–583.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42:633–642.

    CAS  Article  Google Scholar 

  27. 27.

    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618.

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Oksanen J, Blanchet FG, Friendly M, et al (2019) vegan: community ecology package. R package version 2.5-5. Community Ecol Packag

  29. 29.

    McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Team RC (2014) R core team (2014). R A Lang Environ Stat Comput R Found Stat Comput Vienna, Austria URL http//www R-project org

  31. 31.

    Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A. 106:16428–16433.

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Grady KL, Sorensen JW, Stopnisek N, Guittar J, Shade A (2019) Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat Commun. 10:4135.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Miyajima K, Tanii A, Akita T (1983) Pseudomonas fuscovaginae sp. nov., nom. rev. Int J Syst Bacteriol 33:656–657.

    Article  Google Scholar 

  35. 35.

    Sharma S, Sthapit B, Pradhanang P, Joshi K (1997) Bacterial sheath brown rot of rice caused by Pseudomonas fuscovaginae in Nepal. In: Poisson, C. y Rakotoarisoa, J. (Eds.) Rice cultivation in highland areas. Proceedings of the CIRAD conference held at Antananarivo, Madagascar, 29 March-5 April 1996. CIRAD-CA; 1997. p. 107-112

  36. 36.

    Gomes T, Pereira JA, Lino-Neto T, Bennett AE, Baptista P (2019) Bacterial disease induced changes in fungal communities of olive tree twigs depend on host genotype. Sci. Rep. 9:1–10.

    CAS  Article  Google Scholar 

  37. 37.

    Kerdraon L, Laval V, Suffert F (2019) Microbiomes and pathogen survival in crop residues, an ecotone between plant and soil. Phytobiomes J 3:246–255.

    Article  Google Scholar 

  38. 38.

    Rubio-Portillo E, Kersting DK, Linares C, Ramos-Esplá AA, Antón J (2018) Biogeographic differences in the microbiome and pathobiome of the coral Cladocora caespitosa in the Western Mediterranean Sea. Front Microbiol. 9:22.

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Lamichhane JR, Venturi V (2015) Synergisms between microbial pathogens in plant disease complexes: a growing trend. Front Plant Sci 6:385.

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Buonaurio R, Moretti C, Da Silva DP et al (2015) The olive knot disease as a model to study the role of interspecies bacterial communities in plant disease. Front Plant Sci. 6:434.

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Nadarasah G, Stavrinides J (2014) Quantitative evaluation of the host-colonizing capabilities of the enteric bacterium Pantoea using plant and insect hosts. Microbiol (United Kingdom) 160:602–615.

    CAS  Article  Google Scholar 

  42. 42.

    Walterson AM, Stavrinides J (2015) Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol. Rev. 39:968–984.

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Lanoiselet V, You MP, Li YP, Wang CP, Shivas RG, Barbetti MJ (2012) First report of Sarocladium oryzae causing sheath rot on rice (Oryza sativa) in western Australia. Plant Dis. 96:1382.

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Hittalmani S, Mahesh HB, Mahadevaiah C, Prasannakumar MK (2016) De novo genome assembly and annotation of rice sheath rot fungus Sarocladium oryzae reveals genes involved in Helvolic acid and Cerulenin biosynthesis pathways. BMC Genomics 17:1–13.

    CAS  Article  Google Scholar 

  45. 45.

    Peeters KJ, Haeck A, Harinck L, Afolabi OO, Demeestere K, Audenaert K, Höfte M (2020) Morphological, pathogenic and toxigenic variability in the rice sheath rot pathogen Sarocladium oryzae. Toxins (Basel) 12:109.

    Article  Google Scholar 

  46. 46.

    Sakthivel N, Amudha R, Muthukrishnan S (2002) Production of phytotoxic metabolites by Sarocladium oryzae. Mycol Res. 106:609–614.

    CAS  Article  Google Scholar 

  47. 47.

    Manamgoda DS, Rossman AY, Castlebury LA, Crous PW, Madrid H, Chukeatirote E, Hyde KD (2014) The genus Bipolaris. Stud Mycol. 79:221–288.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Roncero MIG, Hera C, Ruiz-Rubio M et al (2003) Fusarium as a model for studying virulence in soilborne plant pathogens. Physiol Mol Plant Pathol 62:87–98.

    Article  Google Scholar 

  49. 49.

    Summerell BA (2019) Resolving Fusarium : current status of the genus. Annu. Rev. Phytopathol. 57:323–333.

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol. 72:1–401.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Stohr SN, Dighton J (2004) Effects of species diversity on establishment and coexistence: a phylloplane fungal community model system. Microb Ecol. 48:431–438.

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Poudel R, Jumpponen A, Schlatter DC et al (2016) Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management. Phytopathology 106:1083–1096.

    CAS  Article  PubMed  Google Scholar 

Download references


We acknowledge IRRI-Burundi for laboratory financial support and providing the plant samples used in this work.


SM was supported by an ICGEB Arturo Falaschi fellowship. This work financially supported by ICGEB and in part by the grant from the Italian MAE-CI (PGR00816/PGR00927/PGR00739).

Author information




SM, JB and VV designed the experiments. SM, GH and DL performed the experiments. GH drew and adapted the rice field sites and outstation map of IRRI-Burundi. SM, DL and CB analyzed the data. MS, CB and VV drafted the manuscript. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Vittorio Venturi.

Ethics declarations

Competing Interests

The authors declare that they have no competing interests.

Electronic Supplementary Material


(PDF 1.60 mb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Musonerimana, S., Bez, C., Licastro, D. et al. Pathobiomes Revealed that Pseudomonas fuscovaginae and Sarocladium oryzae Are Independently Associated with Rice Sheath Rot. Microb Ecol 80, 627–642 (2020).

Download citation


  • Pathobiome
  • Rice sheath rot
  • Pseudomonas
  • Sarocladium
  • Phyllospheric microbiome of rice