Xanthomonas perforans colonization influences Salmonella enterica in the tomato phyllosphere

Applied and Environmental Microbiology

Volumn 80, Issue 10, 2014, Pages 3173-3180

  Potnis, Neha ^a   Soto Arias, José Pablo ^b   Cowles, Kimberly N ^b   van Bruggen, Ariena H C ^a   Jones, Jeffrey B ^a   Barak, Jeri D ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; FRUITS; GENES; PATHOGENS; PLANTS (BOTANY);

AGGREGATE FORMATION; MIXED AGGREGATES; PATHOGEN-ASSOCIATED MOLECULAR PATTERNS; PHYLLOSPHERES; PLANT PATHOGEN; RESISTANT CULTIVARS; SALMONELLA ENTERICA; UNDAMAGED PLANTS;

SALMONELLA;

BACTERIUM; FRUIT; GENE; HERB; HOST-PATHOGEN INTERACTION; IMMUNITY; INOCULATION; PATHOGENICITY; POPULATION STRUCTURE;

GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MICROBIOLOGY; PLANT DISEASE; PLANT LEAF; SALMONELLA ENTERICA; TOMATO; XANTHOMONAS;

LYCOPERSICON ESCULENTUM; PLANT DISEASES; PLANT LEAVES; SALMONELLA ENTERICA; XANTHOMONAS;

EID: 84899051501     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00345-14     Document Type: Article

References (41)

1. Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, Griffin PM. 2013. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008. Emerg. Infect. Dis. 19:407-415. http://dx.doi.org/10.3201/eid1903.111866.
2. Ottesen A, Pena A, White J, Pettengill J, Li C, Allard S, Rideout S, Allard M, Hill T, Evans P, Strain E, Musser S, Knight R, Brown E. 2013. Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiol. 13:114. http://dx.doi.org/10.1186/1471-2180-13-114.
3. Barak JD, Schroeder BK. 2012. Interrelationships of food safety and plant pathology: the life cycle of human pathogens on plants. Annu. Rev. Phy-topathol. 50:241-266. http://dx.doi.org/10.1146/annurev-phyto-081211-172936.
4. Teplitski M, Barak JD, Schneider KR. 2009. Human enteric pathogens in produce: un-answered ecological questions with direct implications for food safety. Curr. Opin. Biotechnol. 20:166-171. http://dx.doi.org/10.1016/j.copbio.2009.03.002.
5. O'Brien RD, Lindow SE. 1989. Effect of plant species and environmental conditions on epiphytic population sizes of Pseudomonas syringae and other bacteria. Phytopathology 79:619-627. http://dx.doi.org/10.1094/Phyto-79-619.
6. Brandl MT, Mandrell RE. 2002. Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl. Environ. Microbiol. 68: 3614-3621. http://dx.doi.org/10.1128/AEM.68.7.3614-3621.2002.
7. Islam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang X. 2004. Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl. Environ. Microbiol. 70:2497-2502. http://dx.doi.org/10.1128/AEM.70.4.2497-2502.2004.
8. Islam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang X. 2004. Persistence of Salmonella enterica serovar Typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathog. Dis. 1:27-35. http://dx.doi.org/10.1089/153531404772914437.
9. Barak JD, Liang AS. 2008. Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS One 3:e1657. http://dx.doi.org/10.1371/journal.pone.0001657.
10. Poza-Carrion C, Suslow T, Lindow S. 2013. Resident bacteria on leaves enhance survival of immigrant cells of Salmonella enterica. Phytopathology 103:341-351. http://dx.doi.org/10.1094/PHYTO-09-12-0221-FI.
11. Wells JM, Butterfield JE. 1997. Salmonella contamination associated with bacterial soft rot of fresh fruits and vegetables in the marketplace. Plant Dis. 81:867-872. http://dx.doi.org/10.1094/PDIS.1997.81.8.867.
12. Wells JM, Butterfield JE. 1999. Incidence of Salmonella on fresh fruits and vegetables affected by fungal rots or physical injury. Plant Dis. 83:722-726. http://dx.doi.org/10.1094/PDIS.1999.83.8.722.
13. Toth IK, Birch PRJ. 2005. Rotting softly and stealthily. Curr. Opin. Plant Biol. 8:424-429. http://dx.doi.org/10.1016/j.pbi.2005.04.001.
14. Rico A, Jones R, Preston GM. 2009. Adaptation to the plant apoplast by plant pathogenic bacteria, p 63-89. In JacksonRW(ed), Plant pathogenic bacteria: genomics and molecular biology. Caister Academic Press, Norwich, United Kingdom.
15. Alfano JR, Collmer A. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683-1698.
16. Meng F, Altier C, Martin GB. 2013. Salmonella colonization activates the plant immune system and benefits from association with plant pathogenic bacteria. Environ. Microbiol. 15:2418-2430. http://dx.doi.org/10.1111/1462-2920.12113.
17. Miller WG, Leveau JH, Lindow SE. 2000. Improved gfp and inaZ broadhost- range promoter-probe vectors. Mol. Plant Microbe Interact. 13: 1243-1250. http://dx.doi.org/10.1094/MPMI.2000.13.11.1243.
18. Zhang Y, Callaway E, Jones J, Wilson M. 2009. Visualisation of hrp gene expression in Xanthomonas euvesicatoria in the tomato phyllosphere. Eur. J. Plant Pathol. 124:379-390. http://dx.doi.org/10.1007/s10658-008-9423-x.
19. Miller JH. 1972. Experiments in molecular genetics, p 466. Cold Spring Harbor Laboratory. Cold Spring Harbor, NY.
20. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
21. Astua-Monge G, Minsavage GV, Stall RE, Davis MJ, Bonas U, Jones JB. 2000. Resistance of tomato and pepper to T3 strains of Xanthomonas campestris pv. vesicatoria is specified by a plant-inducible avirulence gene. Mol. Plant Microbe Interact. 13:911-921. http://dx.doi.org/10.1094/MPMI.2000.13.9.911.
22. Somodi GC, Jones JB, Scott JW. 1991. Populations of Xanthomonas campestris pv. vesicatoria in lesions of susceptible and resistant tomato genotypes. Plant Dis. 75:357-360. http://dx.doi.org/10.1094/PD-75-0357.
23. Cevallos-Cevallos JM, Gu G, Danyluk MD, van Bruggen AHC. 2012. Adhesion and splash dispersal of Salmonella enterica Typhimurium on tomato leaflets: effects of rdar morphotype and trichome density. Int. J. Food Microbiol. 160:58-64. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.09.021.
24. Barak JD, Kramer LC, Hao L. 2011. Plant cultivar alters Salmonella enterica colonization of tomato and type I trichomes are preferential colonization sites. Appl. Environ. Microbiol. 77:498-504. http://dx.doi.org/10.1128/AEM.01661-10.
25. Monier JM, Lindow SE. 2003. Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc. Natl. Acad. Sci. U. S. A. 100:15977-15982. http://dx.doi.org/10.1073/pnas.2436560100.
26. Yamazaki A, Li J, Hutchins WC, Wang L, Ma J, Ibekwe AM, Yang C-H. 2011. Commensal effect of pectate lyases secreted from Dickeya dadantii on proliferation of Escherichia coli O157:H7 EDL933 on lettuce leaves. Appl. Environ. Microbiol. 77:156-162. http://dx.doi.org/10.1128/AEM.01079-10.
27. Kwan G, Charkowski AO, Barak JD. 2013. Salmonella enterica suppresses Pectobacterium carotovorum subsp. carotovorum population and soft rot progression by acidifying the microaerophilic environment. mBio 4:e00557-12. http://dx.doi.org/10.1128/mBio.00557-12.
28. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323- 329. http://dx.doi.org/10.1038/nature05286.
29. Sonnewald S, Priller JPR, Schuster J, Glickmann E, Hajirezaei M-R, Siebig S, Mudgett MB, Sonnewald U. 2012. Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors. PLoS One 7:e51763. http://dx.doi.org/10.1371/journal.pone.0051763.
30. Biemelt S, Sonnewald U. 2006. Plant-microbe interactions to probe regulation of plant carbon metabolism. J. Plant Physiol. 163:307-318. http://dx.doi.org/10.1016/j.jplph.2005.10.011.
31. Humphries EC, Wheeler AW. 1963. The physiology of leaf growth. Annu. Rev. Plant Physiol. 14:385-410. http://dx.doi.org/10.1146/annurev.pp.14.060163.002125.
32. Abou Hadid AF, El-Beltagy AS, Smith AR, Hall MA. 1986. The influence of leaf position and age upon the production of stress ethylene in tomatoes. Acta Hort. 190:397-404.
33. Monier JM, Lindow SE. 2005. Spatial organization of dual-species bacterial aggregates on leaf surfaces. Appl. Environ. Microbiol. 71:5484- 5493. http://dx.doi.org/10.1128/AEM.71.9.5484-5493.2005.
34. Gu G, Cevallos-Cevallos JM, Vallad GE, van Bruggen AHC. 2013. Organically managed soils reduce internal colonization of tomato plants by Salmonella enterica serovar Typhimurium. Phytopathology 103:381- 388. http://dx.doi.org/10.1094/PHYTO-04-12-0072-FI.
35. Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D, Granot D, Sela S. 2009. Internalization of Salmonella in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl. Environ. Microbiol. 75:6076-6086. http://dx.doi.org/10.1128/AEM.01084-09.
36. Gudesblat GE, Torres PS, Vojnov AA. 2009. Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-tocell signal-regulated virulence factor. Plant Physiol. 149:1017-1027. http://dx.doi.org/10.1104/pp.108.126870.
37. Thomma BPHJ, Nurnberger T, Joosten MHAJ. 2011. Of PAMPS and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4-15. http://dx.doi.org/10.1105/tpc.110.082602.
38. Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, van Bruggen AHC. 2011. Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS One 6:e27340. http://dx.doi.org/10.1371/journal.pone.0027340.
39. Graves AS, Alexander SA. 2002. Managing bacterial speck and spot of tomato with acibenzolar-S-methyl in Virginia. Plant Health Prog.. http://dx.doi.org/10.1094/PHP-2002-0220-01-RS.
40. Cummings K, Barrett E, Mohle-Boetani JC, Brooks JT, Farrar J, Hunt T, Fiore A, Komatsu K, Werner SB, Slutsker L. 2001. A multistate outbreak of Salmonella enterica serotype Baildon associated with domestic raw tomatoes. Emerg. Infect. Dis. 7:1046-1048. http://dx.doi.org/10.3201/eid0706.010625.
41. Staskawicz BJ, Dahlbeck D, Keen N, Napoli C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.