Abstract
The bacterial pathogen of oily spot disease, a major threat to pomegranate growers, was isolated from infected plant parts of pomegranate collected from orchards in Maharashtra, India. The pathogen was identified as Xanthomonas axonopodis pv. punicae (Xap) following phenotypic and molecular characterization by 16S rRNA gene sequencing. It produced pectinase, cellulase, xylanase in medium and in experimentally inoculated tissues with pathogen where pectinase activity was maximum (32.2 U/g). Pearson correlation analysis showed a perfect positive correlation (P < 0.05) between enzyme activity and disease rating scale. This indicates the co-synthesis of hydrolytic enzymes that aid in tissue degradation and suggests their role as virulence factors. Out of 150 indigenously isolated lactic acid bacteria (LAB), Lactococcus lactis subsp. cremoris PB6, Lactobacillus brevis PFR77 and L. lactis subsp. cremoris PFL9, the potent antagonists of Xap, were used in the management of bacterial blight. Under laboratory conditions, cell formulation of PB6, PFR77 and PFL9 were equally effective (P > 0.05) and significantly (P < 0.05) reduced the infection in fruits. Under field conditions, the disease severity index for the treatments where plants received a spray of PB6 with streptocycline, was lowest (4.61%) as compared to cells (15.74%), culture supernatant (20.66%) and their integrated treatments (21.38%), and streptocycline (15.37%) treatments. However, no significant difference (P > 0.05) was noticed between cells and streptocycline treatments, thus, indicating the effectiveness of LAB in treating bacterial blight. This is the first report on the use of antagonistic LAB for the control of oily spot disease of pomegranate.
Similar content being viewed by others
References
Kumar R, Shamarao Jahagirdar MR, Yenjerappa ST, Patil HB (2009) Epidemiology and management of bacterial blight of pomegranate caused by Xanthomonas axonopodis pv. punicae. Acta Hort 818:291–296. https://doi.org/10.17660/ActaHortic.2009.818.43
Whipps JM (2001) Microbial interactions and biocontrol in rhizosphere. J Exp Bot 52:487–511. https://doi.org/10.1093/jexbot/52.suppl_1.487
Chavan N, Pandey R, Nawani N, Nanda R, Tandon G, Khetmalas M (2016) Biocontrol potential of actinomycetes against Xanthomonas axonopodis pv. punicae, a causative agent for oily spot disease of pomegranate. Biocontrol Sci Technol 26(3):351–372. https://doi.org/10.1080/09583157.2015.1116057
De Vuyst L, Leroy F (2007) Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microbiol Biotechnol 13:194–199. https://doi.org/10.1159/000104752
Gajbhiye MH, Kapadnis BP (2016) Antifungal-activity producing lactic acid bacteria as biocontrol agents in plants. Biocontrol Sci Technol 26:1451–1470. https://doi.org/10.1080/09583157.2016.1213793
Gao Z, Daliri EBM, Wang J, Liu D, Chen S, Ye X, Ding T (2019) Inhibitory effect of lactic acid bacteria on foodborne pathogens: a review. J Food Prot 82:441–453. https://doi.org/10.4315/0362-028X.JFP-18-303
Mu W, Yu S, Zhu L, Zhang T, Jiang B (2012) Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound. Appl Microbiol Biotechnol 95:1155–1163. https://doi.org/10.1007/s00253-012-4269-8
Gajbhiye M, Prakash D, Jagdale S, Ahiwale S, Patil N, Kapadnis B (2012) Pomegranate borne fungicidal lactic acid bacteria and their biodiversity. Pro Natl Acad Sci India B 82:413–419. https://doi.org/10.1007/s40011-012-0055-8
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428
Li JG, Dong YH (2013) Effect of a rock dust treatment on disease severity of tomato bacterial wilt. Antonie Van Leeuwenhoek 103:11–22. https://doi.org/10.1007/s10482-012-9781-4
Hingorani MK, Mehta PP (1952) Bacterial leaf spot of pomegranate. Indian Phytopathol 5:55–56
Hingorani MK, Singh NJ (1960) Xanthomonas punicae sp. nov. on Punica granatum L. Indian J Agric Sci 29:45–48
Sohi HS, Jain SS, Sharma SL, Verma BR (1964) New records of plant diseases from Himachal Pradesh. Indian Phytopathol 17:35–41
Kanwar ZS (1976) A note on bacterial disease of pomegranate (Punica granatum L.) in Haryana. Haryana J Hortic Sci 5:171–180
Dhasandar DG, Nallathambi P, Rawat RD, Sawant DM (2004) Bacterial leaf and fruit spot: a new threat to pomegranate orchards in Maharashtra. J Myco Plant Pathol 34:971
Petersen Y, Mansvelt EL, Venter E, Langenhoven WE (2010) Detection of Xanthomonas axonopodis pv. punicae causing bacterial blight on pomegranate in South Africa. Austral Plant Pathol 39(6):544–546. https://doi.org/10.1071/AP10034
Akhtar MA, Bhatti MR (1992) Occurrence of bacterial leaf spot of pomegranate in Pakistan. Pak J Agric Res 13(1):95–97
Jagdale SB, Sonawane MS, Kapadnis BP (2018) A new bacterial blight of pomegranate caused by Pseudomonas sp. in Maharashtra India. Austral Plant Dis Notes 13:27. https://doi.org/10.1007/s13314-018-0311-8
Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions. Front Plant Sci 5:1–8. https://doi.org/10.3389/fpls.2014.00228
Gajbhiye M, Sathe S, Shinde V, Kapadnis B (2016) Morphological and molecular characterization of pomegranate fruit rot pathogen, Chaetomella raphigera, and its virulence factors. Indian J Microbiol 56(1):99–102. https://doi.org/10.1007/s12088-015-0554-4
Huang X, Zhai J, Luo Y, Rudolph K (2008) Identification of a highly virulent strain of Xanthomonas axonopodis pv. malvacearum. Eur J Plant Pathol 122(4):461–469. https://doi.org/10.1007/s10658-008-9312-3
Ray SK, Rajeshwari R, Sonti RV (2000) Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathways are virulence deficient and unable to secrete xylanase. Mol Plant-Microbe Interact 13:394–401. https://doi.org/10.1094/MPMI.2000.13.4.394
Thowthampitak J, Shaffer BT, Prathuangwong S, Loper JE (2008) Role of rpfF in virulence and exoenzyme production of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean. Phytopathology 98(12):1252–1260. https://doi.org/10.1094/PHYTO-98-12-1252
Wang L, Rong W, He C (2008) Two Xanthomonas extracellular polygalacturonases, PghAxc and PghBxc, are regulated by type III secretion regulators HrpX and HrpG and are required for virulence. Mol Plant-Microbe Interact 21(5):555–563. https://doi.org/10.1094/MPMI-21-5-0555
Gajbhiye M, Kapadnis B (2018) Bio-efficiency of antifungal lactic acid bacterial isolates for pomegranate fruit rot management. Proc Natl Acad Sci India B 88:1477–1488. https://doi.org/10.1007/s40011-017-0891-7
Perez RH, Zendo T, Sonomoto K (2014) Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb Cell Fact 13(Suppl 1):S3. https://doi.org/10.1186/1475-2859-13-S1-S3
Trias R, Baneras L, Badosa E, Montesinos E (2008) Bioprotection of golden delicious apples and iceberg lettuce against foodborne bacterial pathogens by lactic acid bacteria. Int J Food Microbiol 123(1):50–60. https://doi.org/10.1016/j.ijfoodmicro.2007.11.065
Alegre I, Vinas I, Usall J, Anguera M, Abadias M (2011) Microbiological and physicochemical quality of fresh-cut apple enriched with the probiotic strain Lactobacillus rhamnosus GG. Food Microbiol 28:59–66. https://doi.org/10.1016/j.fm.2010.08.006
Cizeikiene D, Juodeikiene G, Paskevicius A, Bartkiene E (2013) Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control 31(2):539–545. https://doi.org/10.1016/j.foodcont.2012.12.004
Siroli L, Patrignani F, Serrazanetti DI, Vanninia L, Salvetti E, Torriani S, Gardini F, Lanciotti R (2016) Use of a nisin-producing Lactococcus lactis strain, combined with natural antimicrobials, to improve the safety and shelf-life of minimally processed sliced apples. Food Microbiol 54:11–19. https://doi.org/10.1016/j.fm.2015.11.004
Cabrefiga J, Bonaterra A, Montesinos E (2007) Mechanisms of antagonism of Pseudomonas fluorescens EPS62e against Erwinia amylovora, the causal agent of fire blight. Int Microbiol 10:123–132. https://doi.org/10.2436/20.1501.01.18
Ji GH, Wei LF, He YQ, Wu YP, Bai XH (2008) Biological control of rice bacterial blight by Lysobacter antibioticus strain 13–1. Biol Control 45(3):288–296. https://doi.org/10.1016/j.biocontrol.2008.01.004
Meng Q, Hao JJ (2017) Optimizing the application of Bacillus velezensis BAC03 in controlling the disease caused by Streptomyces scabies. Biocontrol 62:535–544. https://doi.org/10.1007/s10526-017-9799-7
Trias R, Baneras L, Montesinos E, Badosa E (2008) Lactic acid bacteria from fresh fruit and vegetables as biocontrol agents of phytopathogenic bacteria and fungi. Int Microbiol 11:231–236. https://doi.org/10.2436/20.1501.01.66
Roselló G, Bonaterra A, Francés J, Montesinos L, Badosa E, Montesinos E (2013) Biological control of fire blight of apple and pear with antagonistic Lactobacillus plantarum. Eur J Plant Pathol 137:621–633. https://doi.org/10.1007/s10658-013-0275-7
Shrestha A, Kim BS, Park DH (2014) Biological control of bacterial spot disease and plant growth-promoting effects of lactic acid bacteria on pepper. Biocontrol Sci Technol 24:763–779. https://doi.org/10.1080/09583157.2014.894495
Daranas N, Roselló G, Cabrefiga J, Donati I, Francés J, Badosa E, Spinelli F, Montesinos E, Bonaterra A (2019) Biological control of bacterial plant diseases with Lactobacillus plantarum strains selected for their broad-spectrum activity. Ann Appl Biol 174:92–105. https://doi.org/10.1111/aab.12476
Acknowledgements
The authors are grateful to Dr. M. K. Kokare for making the pomegranate farm available for sampling purposes and field studies.
Author information
Authors and Affiliations
Contributions
MH Gajbhiye performed the experiments, collected the data and prepared the first draft of the manuscript. AV Bankar assisted in data analysis and construction of tables and figures. BP Kapadnis assisted in the construction of this manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gajbhiye, M.H., Bankar, A.V. & Kapadnis, B.P. Lactic Acid Bacteria in the Management of Oily Spot Disease of Pomegranate. Curr Microbiol 80, 19 (2023). https://doi.org/10.1007/s00284-022-03113-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-022-03113-y