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Bacterial antagonists and their cell-free cultures efficiently suppress canker disease in citrus lime

  • Natthida Sudyoung
  • Shinji Tokuyama
  • Sukhumaporn Krajangsang
  • Onanong Pringsulaka
  • Siriruk SarawaneeyarukEmail author
Original Article
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Abstract

Proliferation of citrus canker disease caused by Xanthomonas citri subsp. citri (Xcc) has increasingly become a serious threat and has resulted in a significant loss in citrus production worldwide. This research aimed to identify efficient antagonistic bacteria for the biological control of canker disease in Citrus aurantifolia cultivar Pan (Pan-lime) and their antagonistic characteristics by experimental analysis. With the dual culture method, twenty isolates inhibited Xcc. Eight out of over fifty isolates showed clear inhibition zones and were further analyzed for plant growth-promoting characteristics. After the screening process, Bacillus velezensis isolate SWUA08 and Pseudomonas aeruginosa isolate SWUC02 were selected for further analysis of bacterial canker resistance in Pan-lime seedlings and trees. Experimental results show that both antagonists increased canker disease resistance. Furthermore, their cell-free cultures reduced canker disease severity index in Pan-lime tree. Our experimental results demonstrating that the antagonists offer an alternative perspective to evaluate a method of canker disease inhibition.

Keywords

Canker disease Antagonist Xanthomonad Biocontrol Citrus 
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Notes

Acknowledgements

This work was supported by Srinakharinwirot University [Grant Numbers 762/2558].

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

41348_2019_295_MOESM1_ESM.pdf (14 kb)
Supplementary material 1 (PDF 13 kb)
41348_2019_295_MOESM2_ESM.pdf (101 kb)
Supplementary material 2 (PDF 101 kb)

References

  1. Bedoya JC, Dealis ML, Silva CS et al (2019) Enhanced production of target bioactive metabolites produced by Pseudomonas aeruginosa LV strain. Biocatal Agric Biotechnol 17:545–556CrossRefGoogle Scholar
  2. Behlau F, Canteros BI, Minsavage GV, Jones JB, Graham JH (2011) Molecular characterization of copper resistance genes from Xanthomonas citri subsp. citri and Xanthomonas alfalfae subsp. citrumelonis. Appl Environ Microbiol 77:4089–4096CrossRefGoogle Scholar
  3. Castric PA (1975) Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21:613–618CrossRefGoogle Scholar
  4. Chun J, Bae KS (2000) Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA sequences. Ant van Leeuwen 78:123–127CrossRefGoogle Scholar
  5. Cubero J, Graham JH (2002) Genetic relationship among worldwide strains of Xanthomonas causing canker in citrus species and design of new primers for their identification by PCR. Appl Environ Microbiol 68:1257–1264CrossRefGoogle Scholar
  6. Das AK (2003) Citrus canker-a review. J Appl Hort 5:52–60Google Scholar
  7. De Oliveira AG, Spago FR, Simionato AS et al (2016) Bioactive organocopper compound from Pseudomonas aeruginosa inhibits the grow of Xanthomonas citri subsp. citri. Front Microbiol 7:113PubMedPubMedCentralGoogle Scholar
  8. El-Fouly MZ, Sharaf AM, Shahin AAM, El-Bialy HA, Omara AMA (2015) Biosynthesis of pyocyanin pigment by Pseudomonas aeruginosa. J Radiat Res Appl Sci 8:36–48CrossRefGoogle Scholar
  9. Fan B, Wang C, Song X et al (2018) Bacillus velezensis FZB42 in 2018: the gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol 9:2491CrossRefGoogle Scholar
  10. Ference CM, Gochez AM, Behlau F, Wang N, Graham JH, Jones JB (2018) Recent advances in the understanding of Xanthomonas citri ssp. citri pathogenesis and citrus canker disease management. Mol Plant Pathol 19:1302–1318CrossRefGoogle Scholar
  11. Fill TP, Pallini HF, Amaral LDS et al (2016) Copper and manganese cations alter secondary metabolism in the fungus Penicillium brasilianum. J Braz Chem Soc 27:1444–1451Google Scholar
  12. Gionco B, Tavares ER, De Oliveira AG et al (2017) New insights about antibiotic production by Pseudomonas aeruginosa: a gene expression analysis. Front Chem 5:66CrossRefGoogle Scholar
  13. Huang TP, Tzeng DDS, Wong ACL et al (2012) DNA polymorphisms and biocontrol of Bacillus antagonistic to citrus bacterial canker with indication of the interference of phyllosphere biofilms. PLoS ONE 7:e42124CrossRefGoogle Scholar
  14. International Standards for Phytosanitary Measures (ISPM) (2014) ISPM 27 Diagnostic protocols, DP 6: Xanthomonas citri subsp. citri. IPPC, FAO, RomeGoogle Scholar
  15. Jacobson CB, Pasternak JJ, Glick BR (1994) Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 40:1019–1025CrossRefGoogle Scholar
  16. Kumar S, Stecher G, Tamura K (2016) Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  17. Lee YA, Sung AN, Liu TF, Lee YS (2009) Combination of chromogenic differential medium and estA-specific PCR for isolation and detection of phytopathogenic Xanthomonas spp. Appl Environ Microbiol 75:6831–6838CrossRefGoogle Scholar
  18. Leifert C, Waites WM (1992) Bacterial growth in plant tissue culture media. J Appl Microbiol 72:460–466Google Scholar
  19. McGuire RG, Jones JB, Sasser M (1986) Tween media for semiselective isolation of Xanthomonas campestris pv. vesicatoria from soil and plant material. Plant Dis 70:887–891CrossRefGoogle Scholar
  20. Michavila G, Adler C, De Gregorio PR et al (2017) Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biol 19:608–617CrossRefGoogle Scholar
  21. Nandi M, Selin C, Brawerman G, Fernando WGD, De Kievit T (2017) Hydrogen cyanide, which contributes to Pseudomonas chlororaphis strain PA23 biocontrol, is upregulated in the presence of glycine. Biol Control 108:47–54CrossRefGoogle Scholar
  22. Naz SA, Jabeen N, Sohail M, Rasool SA (2015) Production and purification of pyocin from a soil associated Pseudomonas aeruginosa strain SA 188. Pak J Agri Sci 52:873–879Google Scholar
  23. Palazzini JM, Dunlap CA, Bowman MJ, Chulze SN (2016) Bacillus velezensis RC 218 as a biocontrol agent to reduce Fusarium head blight and deoxynivalenol accumulation: genome sequencing and secondary metabolite cluster profiles. Microbiol Res 192:30–36CrossRefGoogle Scholar
  24. Park DS, Hyun JW, Park YJ, Kim JS, Kang HW, Hahn JH, Go SJ (2006) Sensitive and specific detection of Xanthomonas axonopodis pv. citri by PCR using pathovar specific primers based on hrpW gene sequences. Microbiol Res 161:145–149CrossRefGoogle Scholar
  25. Richard D, Boyer C, Vernière C, Canteros BI, Lefeuvre P, Pruvost O (2017a) Complete genome sequences of six copper-resistant Xanthomonas citri pv. citri strains causing Asiatic citrus canker, obtained using long-read technology. Genome Announc 5:e00010–e00017PubMedPubMedCentralGoogle Scholar
  26. Richard D, Tribot N, Boyer C et al (2017b) First report of copper-resistant Xanthomonas citri pv. citri pathotype A causing Asiatic citrus canker in Réunion, France. Plant Dis 101:503CrossRefGoogle Scholar
  27. Sasirekha B, Shivakumar S, Sullia SB (2012) Statistical optimization for improved indole-3-acetic acid (IAA) production by Pseudomonas aeruginosa and demonstration of enhanced plant growth promotion. J Soil Sci Plant Nutr 12:863–873Google Scholar
  28. Vasconcellos FCS, De Oliveira AG, Lopes-Santos L et al (2014) Evaluation of antibiotic activity produced by Pseudomonas aeruginosa LV strain against Xanthomonas arboricola pv. pruni. Agric Sci 5:71–76Google Scholar
  29. Zhou L, Jiang HX, Sun S, Yang DD, Jin KM, Zhang W, He YW (2016) Biotechnological potential of a rhizosphere Pseudomonas aeruginosa strain producing phenazine-1-carboxylic acid and phenazine-1-carboxamide. World J Microbiol Biotechnol 32:1–12CrossRefGoogle Scholar

Copyright information

© Deutsche Phytomedizinische Gesellschaft 2019

Authors and Affiliations

  • Natthida Sudyoung
    • 1
  • Shinji Tokuyama
    • 2
  • Sukhumaporn Krajangsang
    • 3
  • Onanong Pringsulaka
    • 3
  • Siriruk Sarawaneeyaruk
    • 3
    Email author
  1. 1.Department of Biology, Faculty of ScienceSrinakharinwirot UniversityWatthanaThailand
  2. 2.Department of Applied Biological Chemistry, Graduate School of AgricultureShizuoka UniversityShizuokaJapan
  3. 3.Department of Microbiology, Faculty of ScienceSrinakharinwirot UniversityWatthanaThailand

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