Plant Biotechnology Reports

, Volume 13, Issue 2, pp 105–110 | Cite as

The dark side of organic vegetables: interactions of human enteropathogenic bacteria with plants

  • Sung Hee Jo
  • Jeong Mee ParkEmail author


Many recent studies reported that several pathogenic bacteria rely on multiple hosts during their life cycle. Specifically, Gram-negative enteropathogenic bacteria, such as Salmonella or Escherichia coli O157:H7, infect both human and plant hosts. These multi-kingdom pathogenic bacteria cause food-associated outbreaks in human by active invasion of the host. In the current review, we cover the interactions between human enteropathogenic bacteria and plants. In particular, we describe the current state of knowledge on the mechanisms of adhesion, invasion, and colonization of the plant hosts by human enteropathogenic bacteria, and describe plant innate immune responses to virulence factors produced by these bacteria.


Enteropathogenic bacteria Alternative host Food-borne disease Innate immune responses 



This work was supported by the KRIBB Initiative Program and the Basic Research Program of National Research Foundation of Korea (NRF-2017R1A2B4012820 to J.M.P.) funded by the Ministry of Science and ICT.


  1. Asai S, Shirasu K (2015) Plant cells under siege: plant immune system versus pathogen effectors. Curr Opin Plant Biol 28:1–8CrossRefGoogle Scholar
  2. Barak JD, Gorski L, Naraghi-Arani P, Charkowski AO (2005) Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl Environ Microbiol 71:5685–5691CrossRefGoogle Scholar
  3. Barak JD, Jahn CE, Gibson DL, Charkowski AO (2007) The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol Plant Microbe Interact 20:1083–1091CrossRefGoogle Scholar
  4. Berger CN, Shaw RK, Brown DJ, Mather H, Clare S, Dougan G, Pallen MJ, Frankel G (2009) Interaction of Salmonella enterica with basil and other salad leaves. ISME J 3:261–265CrossRefGoogle Scholar
  5. Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, Frankel G (2010) Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 12:2385–2397CrossRefGoogle Scholar
  6. Bhavsar AP, Brown NF, Stoepel J, Wiermer M, Martin DD, Hsu KJ, Imami K, Ross CJ, Hayden MR, Foster LJ, Li X, Hieter P, Finlay BB (2013) The Salmonella type III effector SspH2 specifically exploits the NLR co-chaperone activity of SGT1 to subvert immunity. PLoS Pathog 9:e1003518CrossRefGoogle Scholar
  7. Cevallos-Cevallos JM, Gu G, Danyluk MD, van Bruggen AH (2012) Adhesion and splash dispersal of Salmonella enterica Typhimurium on tomato leaflets: effects of rdar morphotype and trichome density. Int J Food Microbiol 160:58–64CrossRefGoogle Scholar
  8. Cooley MB, Miller WG, Mandrell RE (2003) Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by Enterobacter asburiae. Appl Environ Microbiol 69:4915–4926CrossRefGoogle Scholar
  9. Dong Y, Iniguez AL, Ahmer BM, Triplett EW (2003) Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl Environ Microbiol 69:1783–1790CrossRefGoogle Scholar
  10. Erickson MC, Webb CC, Diaz-Perez JC, Phatak SC, Silvoy JJ, Davey L, Payton AS, Liao J, Ma L, Doyle MP (2010) Infrequent internalization of Escherichia coli O157:H7 into field-grown leafy greens. J Food Prot 73:500–506CrossRefGoogle Scholar
  11. Garcia AV, Charrier A, Schikora A, Bigeard J, Pateyron S, de Tauzia-Moreau ML, Evrard A, Mithofer A, Martin-Magniette ML, Virlogeux-Payant I, Hirt H (2014) Salmonella enterica flagellin is recognized via FLS2 and activates PAMP-triggered immunity in Arabidopsis thaliana. Mol Plant 7:657–674CrossRefGoogle Scholar
  12. Golberg D, Kroupitski Y, Belausov E, Pinto R, Sela S (2011) Salmonella Typhimurium internalization is variable in leafy vegetables and fresh herbs. Int J Food Microbiol 145:250–257CrossRefGoogle Scholar
  13. Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011CrossRefGoogle Scholar
  14. Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, van Bruggen AH (2011) Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS One 6:e27340CrossRefGoogle Scholar
  15. Hussain MA, Dawson CO (2013) Economic impact of food safety outbreaks on food businesses. Foods 2:585–589CrossRefGoogle Scholar
  16. Irvine WN, Gillespie IA, Smyth FB, Rooney PJ, McClenaghan A, Devine MJ, Tohani VK, Outbreak Control T (2009) Investigation of an outbreak of Salmonella enterica serovar Newport infection. Epidemiol Infect 137:1449–1456CrossRefGoogle Scholar
  17. Jayaraman D, Valdes-Lopez O, Kaspar CW, Ane JM (2014) Response of Medicago truncatula seedlings to colonization by Salmonella enterica and Escherichia coli O157:H7. PLoS One 9:e87970CrossRefGoogle Scholar
  18. Kalily E, Hollander A, Korin B, Cymerman I, Yaron S (2016) Mechanisms of resistance to linalool in Salmonella Senftenberg and their role in survival on basil. Environ Microbiol 18:3673–3688CrossRefGoogle Scholar
  19. Kisluk G, Kalily E, Yaron S (2013) Resistance to essential oils affects survival of Salmonella enterica serovars in growing and harvested basil. Environ Microbiol 15:2787–2798Google Scholar
  20. Klerks MM, Franz E, van Gent-Pelzer M, Zijlstra C, van Bruggen AH (2007) Differential interaction of Salmonella enterica serovars with lettuce cultivars and plant-microbe factors influencing the colonization efficiency. ISME J 1:620–631CrossRefGoogle Scholar
  21. Klerks MM, van Gent-Pelzer M, Franz E, Zijlstra C, van Bruggen AH (2007) Physiological and molecular responses of Lactuca sativa to colonization by Salmonella enterica serovar Dublin. Appl Environ Microbiol 73:4905–4914CrossRefGoogle Scholar
  22. Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D, Granot D, Sela S (2009) Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl Environ Microbiol 75:6076–6086CrossRefGoogle Scholar
  23. 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:e00557–12CrossRefGoogle Scholar
  24. Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou JM, Shao F (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315:1000–1003CrossRefGoogle Scholar
  25. Lim JA, Lee DH, Heu S (2014) The interaction of human enteric pathogens with plants. Plant Pathol J 30:109–116CrossRefGoogle Scholar
  26. Martinez-Vaz BM, Fink RC, Diez-Gonzalez F, Sadowsky MJ (2014) Enteric pathogen–plant interactions: molecular connections leading to colonization and growth and implications for food safety. Microbes Environ 29:123–135CrossRefGoogle Scholar
  27. Marvasi M, Noel JT, George AS, Farias MA, Jenkins KT, Hochmuth G, Xu Y, Giovanonni JJ, Teplitski M (2014) Ethylene signalling affects susceptibility of tomatoes to Salmonella. Microb Biotechnol 7:545–555CrossRefGoogle Scholar
  28. Meng F, Altier C, Martin GB (2013) Salmonella colonization activates the plant immune system and benefits from association with plant pathogenic bacteria. Environ Microbiol 15:2418–2430CrossRefGoogle Scholar
  29. Milillo SR, Badamo JM, Boor KJ, Wiedmann M (2008) Growth and persistence of Listeria monocytogenes isolates on the plant model Arabidopsis thaliana. Food Microbiol 25:698–704CrossRefGoogle Scholar
  30. Mootian G, Wu WH, Matthews KR (2009) Transfer of Escherichia coli O157:H7 from soil, water, and manure contaminated with low numbers of the pathogen to lettuce plants. J Food Prot 72:2308–2312CrossRefGoogle Scholar
  31. Neumann C, Fraiture M, Hernandez-Reyes C, Akum FN, Virlogeux-Payant I, Chen Y, Pateyron S, Colcombet J, Kogel KH, Hirt H, Brunner F, Schikora A (2014) The Salmonella effector protein SpvC, a phosphothreonine lyase is functional in plant cells. Front Microbiol 5:548Google Scholar
  32. Ohl ME, Miller SI (2001) Salmonella: a model for bacterial pathogenesis. Annu Rev Med 52:259–274CrossRefGoogle Scholar
  33. Ongeng D, Vasquez GA, Muyanja C, Ryckeboer J, Geeraerd AH, Springael D (2011) Transfer and internalisation of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in cabbage cultivated on contaminated manure-amended soil under tropical field conditions in Sub-Saharan Africa. Int J Food Microbiol 145:301–310CrossRefGoogle Scholar
  34. Plotnikova JM, Rahme LG, Ausubel FM (2000) Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol 124:1766–1774CrossRefGoogle Scholar
  35. Prithiviraj B, Bais HP, Jha AK, Vivanco JM (2005) Staphylococcus aureus pathogenicity on Arabidopsis thaliana is mediated either by a direct effect of salicylic acid on the pathogen or by SA-dependent, NPR1-independent host responses. Plant J 42:417–432CrossRefGoogle Scholar
  36. Rossez Y, Holmes A, Wolfson EB, Gally DL, Mahajan A, Pedersen HL, Willats WG, Toth IK, Holden NJ (2014) Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants. Environ Microbiol 16:2181–2195CrossRefGoogle Scholar
  37. Roy D, Panchal S, Rosa BA, Melotto M (2013) Escherichia coli O157:H7 induces stronger plant immunity than Salmonella enterica Typhimurium SL1344. Phytopathology 103:326–332CrossRefGoogle Scholar
  38. Saldana Z, Sanchez E, Xicohtencatl-Cortes J, Puente JL, Giron JA (2011) Surface structures involved in plant stomata and leaf colonization by Shiga-toxigenic Escherichia coli O157:H7. Front Microbiol 2:119CrossRefGoogle Scholar
  39. Schikora A, Carreri A, Charpentier E, Hirt H (2008) The dark side of the salad: Salmonella typhimurium overcomes the innate immune response of Arabidopsis thaliana and shows an endopathogenic lifestyle. PLoS One 3:e2279CrossRefGoogle Scholar
  40. Schikora A, Virlogeux-Payant I, Bueso E, Garcia AV, Nilau T, Charrier A, Pelletier S, Menanteau P, Baccarini M, Velge P, Hirt H (2011) Conservation of Salmonella infection mechanisms in plants and animals. PLoS One 6:e24112CrossRefGoogle Scholar
  41. Seo S, Matthews KR (2012) Influence of the plant defense response to Escherichia coli O157:H7 cell surface structures on survival of that enteric pathogen on plant surfaces. Appl Environ Microbiol 78:5882–5889CrossRefGoogle Scholar
  42. Shirron N, Yaron S (2011) Active suppression of early immune response in tobacco by the human pathogen Salmonella Typhimurium. PLoS One 6:e18855CrossRefGoogle Scholar
  43. Solomon EB, Yaron S, Matthews KR (2002) Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Appl Environ Microbiol 68:397–400CrossRefGoogle Scholar
  44. Ustun S, Muller P, Palmisano R, Hensel M, Bornke F (2012) SseF, a type III effector protein from the mammalian pathogen Salmonella enterica, requires resistance-gene-mediated signalling to activate cell death in the model plant Nicotiana benthamiana. New Phytol 194:1046–1060CrossRefGoogle Scholar
  45. Wachtel MR, Charkowski AO (2002) Cross-contamination of lettuce with Escherichia coli O157:H7. J Food Prot 65:465–470CrossRefGoogle Scholar
  46. Xicohtencatl-Cortes J, Sanchez Chacon E, Saldana Z, Freer E, Giron JA (2009) Interaction of Escherichia coli O157:H7 with leafy green produce. J Food Prot 72:1531–1537CrossRefGoogle Scholar
  47. Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185CrossRefGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology 2019

Authors and Affiliations

  1. 1.Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)DaejeonSouth Korea
  2. 2.Department of Biosystems and Bioengineering, KRIBB School of BiotechnologyKorea University of Science and Technology (UST)DaejeonSouth Korea

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