1932

Abstract

Plant-associated bacteria face multiple selection pressures within their environments and have evolved countless adaptations that both depend on and shape bacterial phenotype and their interaction with plant hosts. Explaining bacterial adaptation and evolution therefore requires considering each of these forces independently as well as their interactions. In this review, we examine how bacteriophage viruses (phages) can alter the ecology and evolution of plant-associated bacterial populations and communities. This includes influencing a bacterial population's response to both abiotic and biotic selection pressures and altering ecological interactions within the microbiome and between the bacteria and host plant. We outline specific ways in which phages can alter bacterial phenotype and discuss when and how this might impact plant-microbe interactions, including for plant pathogens. Finally, we highlight key open questions in phage-bacteria-plant research and offer suggestions for future study.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080417-045858
2018-08-25
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/phyto/56/1/annurev-phyto-080417-045858.html?itemId=/content/journals/10.1146/annurev-phyto-080417-045858&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Adriaenssens EM, Van Vaerenbergh J, Vandenheuvel D, Dunon V, Ceyssens P-J et al. 2012. T4-related bacteriophage LIMEstone isolates for the control of soft rot on potato caused by ‘Dickeya solani. .’ PLOS ONE 7:e33227
    [Google Scholar]
  2. 2.  Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST et al. 2016. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLOS Biol 14:e1002352
    [Google Scholar]
  3. 3.  Ahmad AA, Askora A, Kawasaki T, Fujie M, Yamada T 2014. The filamentous phage XacF1 causes loss of virulence in Xanthomonas axonopodis pv. citri, the causative agent of citrus canker disease. Front. Microbiol. 5:e321
    [Google Scholar]
  4. 4.  Alsohim AS, Taylor TB, Barrett GA, Gallie J, Zhang XX et al. 2014. The biosurfactant viscosin produced by Pseudomonas fluorescens SBW25 aids spreading motility and plant growth promotion. Environ. Microbiol. 16:2267–81
    [Google Scholar]
  5. 5.  Arnold DL, Pitman A, Jackson RW 2003. Pathogenicity and other genomic islands in plant pathogenic bacteria. Mol. Plant Pathol. 4:407–20
    [Google Scholar]
  6. 6.  Ashelford KE, Day MJ, Bailey MJ, Lilley AK, Fry JC 1999. In situ population dynamics of bacterial viruses in a terrestrial environment. Appl. Environ. Microbiol. 65:169–74
    [Google Scholar]
  7. 7.  Ashelford KE, Norris SJ, Fry JC, Bailey MJ, Day MJ 2000. Seasonal population dynamics and interactions of competing bacteriophages and their host in the rhizosphere. Appl. Environ. Microbiol. 66:4193–99
    [Google Scholar]
  8. 8.  Azegami K 2013. Suppressive effect of bacteriophage on bacterial palea browning of rice caused by Pantoea ananatis. J. Gen. . Plant Pathol 79:145–54
    [Google Scholar]
  9. 9.  Balogh B, Canteros BI, Stall RE, Jones JB 2008. Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis 92:1048–52
    [Google Scholar]
  10. 10.  Balogh B, Jones J, Momol M, Olson S, Obradovic A et al. 2003. Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis 87:949–54
    [Google Scholar]
  11. 11.  Barksdale L, Garmise L, Horibata K 1960. Virulence, toxinogeny, and lysogeny in Corynebacterium diphtheriae. Ann. NY Acad. Sci. 88:1093–108
    [Google Scholar]
  12. 12.  Beattie GA, Lindow SE 1999. Bacterial colonization of leaves: a spectrum of strategies. Phytopathology 89:353–59
    [Google Scholar]
  13. 13.  Beumer A, Robinson JB 2005. A broad-host-range, generalized transducing phage (SN-T) acquires 16S rRNA genes from different genera of bacteria. Appl. Environ. Microbiol. 71:8301–4
    [Google Scholar]
  14. 14.  Bikard D, Marraffini LA 2012. Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr. Opin. Immunol. 24:15–20
    [Google Scholar]
  15. 15.  Bobay L-M, Rocha EP, Touchon M 2012. The adaptation of temperate bacteriophages to their host genomes. Mol. Biol. Evol. 30:737–51
    [Google Scholar]
  16. 16.  Bohannan BJ, Lenski RE 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3:362–77
    [Google Scholar]
  17. 17.  Bono LM, Gensel CL, Pfennig DW, Burch CL 2012. Competition and the origins of novelty: experimental evolution of niche-width expansion in a virus. Biol. Lett. 9:20120616
    [Google Scholar]
  18. 18.  Borah P, Jindal J, Verma J 2000. Integrated management of bacterial leaf spot of mungbean with bacteriophages of Xav and chemicals. J. Mycol. Plant Pathol. 30:19–21
    [Google Scholar]
  19. 19.  Boulé J, Sholberg P, Lehman S, O'Gorman D, Svircev A 2011. Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia, Canada. Can. J. Plant Pathol. 33:308–17
    [Google Scholar]
  20. 20.  Bowatte S, Newton PC, Takahashi R, Kimura M 2010. High frequency of virus-infected bacterial cells in a sheep grazed pasture soil in New Zealand. Soil Biol. Biochem. 42:708–12
    [Google Scholar]
  21. 21.  Boyd EF, Brüssow H 2002. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol 10:521–29
    [Google Scholar]
  22. 22.  Bradley DE, Douglas CJ, Peschon J 1984. Flagella-specific bacteriophages of Agrobacterium tumefaciens: demonstration of virulence of nonmotile mutants. Can. J. Microbiol. 30:676–81
    [Google Scholar]
  23. 23.  Brockhurst MA, Buckling A, Rainey PB 2005. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa. Proc. R. Soc. B 272:1385–91
    [Google Scholar]
  24. 24.  Brown SP, Le Chat L, De Paepe M, Taddei F 2006. Ecology of microbial invasions: Amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 16:2048–52
    [Google Scholar]
  25. 25.  Buée M, De Boer W, Martin F, van Overbeek L, Jurkevitch E 2009. The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212
    [Google Scholar]
  26. 26.  Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. PNAS 100:10181–86
    [Google Scholar]
  27. 27.  Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J et al. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403
    [Google Scholar]
  28. 28.  Burdman S, Bahar O, Parker JK, De La Fuente L 2011. Involvement of type IV pili in pathogenicity of plant pathogenic bacteria. Genes 2:706–35
    [Google Scholar]
  29. 29.  Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J et al. 2017. Research priorities for harnessing plant microbiomes in sustainable agriculture. PLOS Biol 15:e2001793
    [Google Scholar]
  30. 30.  Buttimer C, McAuliffe O, Ross RP, Hill C, O'Mahony J, Coffey A 2017. Bacteriophages and bacterial plant diseases. Front. Microbiol. 8:e34
    [Google Scholar]
  31. 31.  Campbell JI, Albrechtsen M, Sørensen J 1995. Large Pseudomonas phages isolated from barley rhizosphere. FEMS Microbiol. Ecol. 18:63–74
    [Google Scholar]
  32. 32.  Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67:238–76
    [Google Scholar]
  33. 33.  Chan BK, Abedon ST, Loc-Carrillo C 2013. Phage cocktails and the future of phage therapy. Future Microbiol 8:769–83
    [Google Scholar]
  34. 34.  Chen J, Carpena N, Quiles-Puchalt N, Ram G, Novick RP, Penadés JR 2015. Intra- and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages. ISME J 9:1260–63
    [Google Scholar]
  35. 35.  Chen J, Novick RP 2009. Phage-mediated intergeneric transfer of toxin genes. Science 323:139–41
    [Google Scholar]
  36. 36.  Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K et al. 2007. Comparative analysis of the complete genome sequence of the plant growth–promoting bacterium Bacillus amyloliquefaciens FZB42. Nat. Biotechnol. 25:1007–14
    [Google Scholar]
  37. 37.  Chowdhury C, Jagannadham MV 2013. Virulence factors are released in association with outer membrane vesicles of Pseudomonas syringae pv. tomato T1 during normal growth. Biochim. Biophys. Acta 1834:231–39
    [Google Scholar]
  38. 38.  Civerolo E, Keil H 1969. Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59:1966–67
    [Google Scholar]
  39. 39.  Czajkowski R, Smolarska A, Ozymko Z 2017. The viability of lytic bacteriophage ΦD5 in potato-associated environments and its effect on Dickeya solani in potato (Solanum tuberosum L.) plants. PLOS ONE 12:e0183200
    [Google Scholar]
  40. 40.  da Silva AR, Ferro JA, Reinach F, Farah C, Furlan L et al. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–63
    [Google Scholar]
  41. 41.  Das M, Bhowmick TS, Ahern SJ, Young R, Gonzalez CF 2015. Control of Pierce's disease by phage. PLOS ONE 10:e0128902
    [Google Scholar]
  42. 42.  Davies EV, James CE, Williams D, O'Brien S, Fothergill JL et al. 2016. Temperate phages both mediate and drive adaptive evolution in pathogen biofilms. PNAS 113:8266–71
    [Google Scholar]
  43. 43.  Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B et al. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. PNAS 106:16428–33
    [Google Scholar]
  44. 44.  de Mello Varani A, Souza RC, Nakaya HI, De Lima WC, de Almeida LGP et al. 2008. Origins of the Xylella fastidiosa prophage-like regions and their impact in genome differentiation. PLOS ONE 3:e4059
    [Google Scholar]
  45. 45.  Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK et al. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. PNAS 112:E911–20
    [Google Scholar]
  46. 46.  Ellis RJ, Thompson IP, Bailey MJ 1999. Temporal fluctuations in the pseudomonad population associated with sugar beet leaves. FEMS Microbiol. Ecol. 28:345–56
    [Google Scholar]
  47. 47.  Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A et al. 2017. Communication between viruses guides lysis-lysogeny decisions. Nature 541:488–93
    [Google Scholar]
  48. 48.  Evans TJ, Ind A, Komitopoulou E, Salmond GPC 2010. Phage‐selected lipopolysaccharide mutants of Pectobacterium atrosepticum exhibit different impacts on virulence. J. Appl. Microbiol. 109:505–14
    [Google Scholar]
  49. 49.  Fineran P, Petty N, Salmond G 2009. Transduction: host DNA transfer by bacteriophages. Encyclopedia of Microbiology M Schaechter 666–79 Oxford, UK: Academic. , 3rd ed..
    [Google Scholar]
  50. 50.  Fujiwara A, Fujisawa M, Hamasaki R, Kawasaki T, Fujie M, Yamada T 2011. Biocontrol of Ralstonia solanacearum by treatment with lytic bacteriophages. Appl. Environ. Microbiol. 77:4155–62
    [Google Scholar]
  51. 51.  Gaba S, Ebert D 2009. Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol. Evol. 24:226–32
    [Google Scholar]
  52. 52.  Garcia-Doval C, van Raaij MJ 2012. Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers. PNAS 109:9390–95
    [Google Scholar]
  53. 53.  Gill J, Svircev A, Smith R, Castle A 2003. Bacteriophages of Erwinia amylovora. Appl. Environ. . Microbiol 69:2133–38
    [Google Scholar]
  54. 54.  Gómez P, Buckling A 2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106–9
    [Google Scholar]
  55. 55.  Haefele DM, Lindow SE 1987. Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl. Environ. Microbiol. 53:2528–33
    [Google Scholar]
  56. 56.  Hammad AMM 1998. Evaluation of alginate-encapsulated Azotobacter chroococcum as a phage-resistant and an effective inoculum. J. Basic Microbiol. 38:9–16
    [Google Scholar]
  57. 57.  Harrison E, Brockhurst MA 2017. Ecological and evolutionary benefits of temperate phage: What does or doesn't kill you makes you stronger. BioEssays 39:1700112
    [Google Scholar]
  58. 58.  Herron PR 1995. Phage ecology and genetic exchange in soil. Molecular Microbial Ecology Manual GA Kowalchuk, F de Bruijn, IM Head, AJ Van der Zijpp, JD van Elsas 427–38 Dordrecht, Neth.: Springer
    [Google Scholar]
  59. 59.  Hirano SS, Upper CD 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64:624–53
    [Google Scholar]
  60. 60.  Höfte M, Seong KY, Jurkevitch E, Verstraete W 1991. Pyoverdin production by the plant growth beneficial Pseudomonas strain 7NSK2: ecological significance in soil. Iron Nutrition and Interactions in Plants Y Chen, Y Hadar 289–97 Dordrecht, Neth.: Springer
    [Google Scholar]
  61. 61.  Hong YH, Huang C, Wang KC, Chu TH, Li CH et al. 2014. Mutations in Ralstonia solanacearum loci involved in lipopolysaccharide biogenesis, phospholipid trafficking and peptidoglycan recycling render bacteriophage infection. Arch. Microbiol. 196:667–74
    [Google Scholar]
  62. 62.  Hosseinidoust Z, Tufenkji N, Van De Ven TG 2013. Predation in homogeneous and heterogeneous phage environments affects virulence determinants of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 79:2862–71
    [Google Scholar]
  63. 63.  Howard-Varona C, Hargreaves KR, Abedon ST, Sullivan MB 2017. Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J 11:1511–20
    [Google Scholar]
  64. 64.  Høyland-Kroghsbo NM, Mærkedahl RB, Svenningsen SL 2013. A quorum-sensing-induced bacteriophage defense mechanism. mBio 4:e00362–12
    [Google Scholar]
  65. 65.  Hu J, Wei Z, Weidner S, Friman VP, Xu YC et al. 2017. Probiotic Pseudomonas communities enhance plant growth and nutrient assimilation via diversity-mediated ecosystem functioning. Soil Biol. Biochem. 113:122–29
    [Google Scholar]
  66. 66.  Icho T, Iino T 1978. Isolation and characterization of motile Escherichia coli mutants resistant to bacteriophage chi. J. Bacteriol. 134:854–60
    [Google Scholar]
  67. 67.  Iriarte F, Balogh B, Momol M, Smith L, Wilson M, Jones J 2007. Factors affecting survival of bacteriophage on tomato leaf surfaces. Appl. Environ. Microbiol. 73:1704–11
    [Google Scholar]
  68. 68.  Jackson RW, Vinatzer B, Arnold DL, Dorus S, Murillo J 2011. The influence of the accessory genome on bacterial pathogen evolution. Mobile Genet. Elem. 1:55–65
    [Google Scholar]
  69. 69.  Jaiswal AK, Elad Y, Paudel I, Graber ER, Cytryn E, Frenkel O 2017. Linking the belowground microbial composition, diversity and activity to soilborne disease suppression and growth promotion of tomato amended with biochar. Sci. Rep. 7:44382
    [Google Scholar]
  70. 70.  Julio SM, Heithoff DM, Mahan MJ 2000. ssrA (tmRNA) plays a role in Salmonella enterica serovar Typhimurium pathogenesis. J. Bacteriol. 182:1558–63
    [Google Scholar]
  71. 71.  Kamoun S, Kado CI 1990. Phenotypic switching affecting chemotaxis, xanthan production, and virulence in Xanthomonas campestris. Appl. Environ. Microbiol. 56:3855–60
    [Google Scholar]
  72. 72.  Kembel SW, O'Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL 2014. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. PNAS 111:13715–20
    [Google Scholar]
  73. 73.  Khokhani D, Lowe-Power TM, Tran TM, Allen C 2017. A single regulator mediates strategic switching between attachment/spread and growth/virulence in the plant pathogen Ralstonia solanacearum. . mBio 8:e00895–17
    [Google Scholar]
  74. 74.  Kidambi SP, Ripp S, Miller RV 1994. Evidence for phage-mediated gene transfer among Pseudomonas aeruginosa strains on the phylloplane. Appl. Environ. Microbiol. 60:496–500
    [Google Scholar]
  75. 75.  Kim S, Rahman M, Seol SY, Yoon SS, Kim J 2012. Pseudomonas aeruginosa bacteriophage PA1Ø requires type IV pili for infection and shows broad bactericidal and biofilm removal activities. Appl. Environ. Microbiol. 78:6380–85
    [Google Scholar]
  76. 76.  Kleczkowska J 1950. A study of phage-resistant mutants of Rhizobium trifolii. . Microbiology 4:298–310
    [Google Scholar]
  77. 77.  Koskella B 2013. Phage-mediated selection on microbiota of a long-lived host. Curr. Biol. 23:1256–60
    [Google Scholar]
  78. 78.  Koskella B, Brockhurst MA 2014. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38:916–31
    [Google Scholar]
  79. 79.  Koskella B, Lin DM, Buckling A, Thompson JN 2012. The costs of evolving resistance in heterogeneous parasite environments. Proc. R. Soc. B 279:1896–903
    [Google Scholar]
  80. 80.  Koskella B, Meaden S 2013. Understanding bacteriophage specificity in natural microbial communities. Viruses 5:806–23
    [Google Scholar]
  81. 81.  Koskella B, Meaden S, Crowther WJ, Leimu R, Metcalf CJE 2017. A signature of tree health? Shifts in the microbiome and the ecological drivers of horse chestnut bleeding canker disease. New Phytol 215:737–46
    [Google Scholar]
  82. 82.  Koskella B, Taylor TB 2015. The potential role of bacteriophages in shaping plant-bacterial interactions. Bacteria-Plant Interactions: Advanced Research and Future Trends J Murillo, BA Vinatzer, RW Jackson, DL Arnold 199–220 Dorset, UK: Caister Acad.
    [Google Scholar]
  83. 83.  Koskella B, Taylor TB, Bates J, Buckling A 2011. Using experimental evolution to explore natural patterns between bacterial motility and resistance to bacteriophages. ISME J 5:1809–17
    [Google Scholar]
  84. 84.  Koskella B, Thompson JN, Preston GM, Buckling A 2011. Local biotic environment shapes the spatial scale of bacteriophage adaptation to bacteria. Am. Nat. 177:440–51
    [Google Scholar]
  85. 85.  Labrie SJ, Samson JE, Moineau S 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317–27
    [Google Scholar]
  86. 86.  Laforest-Lapointe I, Paquette A, Messier C, Kembel SW 2017. Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546:145–47
    [Google Scholar]
  87. 87.  Leonard S, Hommais F, Nasser W, Reverchon S 2017. Plant-phytopathogen interactions: bacterial responses to environmental and plant stimuli. Environ. Microbiol. 19:1689–716
    [Google Scholar]
  88. 88.  Levy A, Gonzalez IS, Mittelviefhaus M, Clingenpeel S, Paredes SH et al. 2018. Genomic features of bacterial adaptation to plants. Nat. Genet. 50:138
    [Google Scholar]
  89. 89.  Lindow SE, Brandl MT 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875–83
    [Google Scholar]
  90. 90.  Liu H, Carvalhais LC, Schenk PM, Dennis PG 2017. Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci. Rep. 7:41766
    [Google Scholar]
  91. 91.  Lu TK, Collins JJ 2009. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. PNAS 106:4629–34
    [Google Scholar]
  92. 92.  Lüneberg K, Prado B, Broszat M, Dalkmann P, Díaz D et al. 2018. Water flow paths are hotspots for the dissemination of antibiotic resistance in soil. Chemosphere 193:1198–206
    [Google Scholar]
  93. 93.  Mattick JS 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289–314
    [Google Scholar]
  94. 94.  Mavrodi DV, Loper JE, Paulsen IT, Thomashow LS 2009. Mobile genetic elements in the genome of the beneficial rhizobacterium Pseudomonas fluorescens Pf-5. BMC Microbiol 9:8
    [Google Scholar]
  95. 95.  Mazaheri Nezhad Fard R, Barton M, Heuzenroeder M 2011. Bacteriophage‐mediated transduction of antibiotic resistance in enterococci. Lett. Appl. Microbiol. 52:559–64
    [Google Scholar]
  96. 96.  Meaden S, Paszkiewicz K, Koskella B 2015. The cost of phage resistance in a plant pathogenic bacterium is context‐dependent. Evolution 69:1321–28
    [Google Scholar]
  97. 97.  Melotto M, Underwood W, Koczan J, Nomura K, He SY 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80
    [Google Scholar]
  98. 98.  Morella NM, Gomez AL, Wang G, Leung MS, Koskella B 2018. The impact of bacteriophages on phyllosphere bacterial abundance and composition. Mol. Ecol. 27:2025–38
    [Google Scholar]
  99. 99.  Mori Y, Inoue K, Ikeda K, Nakayashiki H, Higashimoto C et al. 2016. The vascular plant‐pathogenic bacterium Ralstonia solanacearum produces biofilms required for its virulence on the surfaces of tomato cells adjacent to intercellular spaces. Mol. Plant Pathol. 17:890–902
    [Google Scholar]
  100. 100.  Muniesa M, Lucena F, Jofre J 1999. Comparative survival of free Shiga toxin 2-encoding phages and Escherichia coli strains outside the gut. Appl. Environ. Microbiol. 65:5615–18
    [Google Scholar]
  101. 101.  Nanda AM, Thormann K, Frunzke J 2015. Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions. J. Bacteriol. 197:410–19
    [Google Scholar]
  102. 102.  Narulita E, Addy HS, Kawasaki T, Fujie M, Yamada T 2016. The involvement of the PilQ secretin of type IV pili in phage infection in Ralstonia solanacearum. Biochem. Biophys. Res. Commun. 469:868–72
    [Google Scholar]
  103. 103.  Nguyen S, Baker K, Padman BS, Patwa R, Dunstan RA et al. 2017. Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio 8:e01874–17
    [Google Scholar]
  104. 104.  Ofek M, Voronov‐Goldman M, Hadar Y, Minz D 2014. Host signature effect on plant root‐associated microbiomes revealed through analyses of resident versus active communities. Environ. Microbiol. 16:2157–67
    [Google Scholar]
  105. 105.  O'Flaherty S, Ross RP, Coffey A 2009. Bacteriophage and their lysins for elimination of infectious bacteria. FEMS Microbiol. Rev. 33:801–19
    [Google Scholar]
  106. 106.  Panopoulos N, Schroth M 1974. Role of flagellar motility in the invasion of bean leaves. Phytopathology 64:1389–97
    [Google Scholar]
  107. 107.  Paulsen IT, Press CM, Ravel J, Kobayashi DY, Myers GS et al. 2005. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat. Biotechnol. 23:873–78
    [Google Scholar]
  108. 108.  Parikka KJ, Le Romancer M, Wauters N, Jacquet S 2017. Deciphering the virus‐to‐prokaryote ratio (VPR): insights into virus–host relationships in a variety of ecosystems. Biol. Rev. 92:1081–100
    [Google Scholar]
  109. 109.  Pirhonen M, Heino P, Helander I, Harju P, Palva ET 1988. Bacteriophage T4 resistant mutants of the plant pathogen Erwinia carotovora. Microb. Pathog. 4:359–67
    [Google Scholar]
  110. 110.  Poisot T, Bell T, Martinez E, Gougat-Barbera C, Hochberg ME 2013. Terminal investment induced by a bacteriophage in a rhizosphere bacterium. F1000Research 1:21
    [Google Scholar]
  111. 111.  Pratama AA, van Elsas JD 2018. The ‘neglected’ soil virome: potential role and impact. Trends Microbiol In press. https://doi.org/10.1016/j.tim.2017.12.004
    [Crossref]
  112. 112.  Primo ED, Ruiz F, Masciarelli O, Giordano W 2015. Biofilm formation and biosurfactant activity in plant-associated bacteria. Bacterial Metabolites in Sustainable Agroecosystem DK Maheshwari 337–49 Dordrecht, Neth.: Springer
    [Google Scholar]
  113. 113.  Quesada JM, Soriano MI, Espinosa-Urgel M 2012. Stability of a Pseudomonas putida KT2440 bacteriophage-carried genomic island and its impact on rhizosphere fitness. Appl. Environ. Microbiol. 78:6963–74
    [Google Scholar]
  114. 114.  Quiñones B, Dulla G, Lindow SE 2005. Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol. Plant Microbe Interact. 18:682–93
    [Google Scholar]
  115. 115.  Quirós P, Muniesa M 2017. Contribution of cropland to the spread of Shiga toxin phages and the emergence of new Shiga toxin-producing strains. Sci. Rep. 7:7796
    [Google Scholar]
  116. 116.  Ramey BE, Koutsoudis M, von Bodman SB, Fuqua C 2004. Biofilm formation in plant-microbe associations. Curr. Opin. Microbiol. 7:602–9
    [Google Scholar]
  117. 117.  Ravensdale M, Blom T, Gracia-Garza J, Svircev A, Smith R 2007. Bacteriophages and the control of Erwinia carotovora subsp. carotovora. Can. J. Plant Pathol. 29:121–30
    [Google Scholar]
  118. 118.  Refardt D 2011. Within-host competition determines reproductive success of temperate bacteriophages. ISME J 5:1451–60
    [Google Scholar]
  119. 119.  Regan K, Stempfhuber B, Schloter M, Rasche F, Prati D et al. 2017. Spatial and temporal dynamics of nitrogen fixing, nitrifying and denitrifying microbes in an unfertilized grassland soil. Soil Biol. Biochem. 109:214–26
    [Google Scholar]
  120. 120.  Remus-Emsermann MN, Tecon R, Kowalchuk GA, Leveau JH 2012. Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J 6:756–65
    [Google Scholar]
  121. 121.  Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J et al. 2008. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J 3:271–82
    [Google Scholar]
  122. 122.  Rodríguez-Navarro DN, Dardanelli MS, Ruíz-Saínz JE 2007. Attachment of bacteria to the roots of higher plants. FEMS Microbiol. Lett. 272:127–36
    [Google Scholar]
  123. 123.  Roine E, Raineri DM, Romantschuk M, Wilson M, Nunn DN 1998. Characterization of type IV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol. Plant Microbe Interact. 11:1048–56
    [Google Scholar]
  124. 124.  Romanenko AS, Lomovatskaya LA, Shafikova TN, Borovskii GB, Krivolapova NV 2003. Potato cell plasma membrane receptors to ring rot pathogen extracellular polysaccharides. J. Phytopathol. 151:1–6
    [Google Scholar]
  125. 125.  Romantschuk M, Bamford DH 1985. Function of pili in bacteriophage Ø6 penetration. J. Gen. Virol. 66:2461–69
    [Google Scholar]
  126. 126.  Romero-Suarez S, Jordan B, Heinemann JA 2012. Isolation and characterization of bacteriophages infecting Xanthomonas arboricola pv. juglandis, the causal agent of walnut blight disease. World J. Microbiol. Biotechnol. 28:1917–27
    [Google Scholar]
  127. 127.  Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S et al. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. . Nature 415:497–502
    [Google Scholar]
  128. 128.  Samuel AD, Pitta TP, Ryu WS, Danese PN, Leung EC, Berg HC 1999. Flagellar determinants of bacterial sensitivity to χ-phage. PNAS 96:9863–66
    [Google Scholar]
  129. 129.  Scanlan PD, Bischofberger AM, Hall AR 2016. Modification of Escherichia coli–bacteriophage interactions by surfactants and antibiotics in vitro. FEMS Microbiol. Ecol. 93:fiw211
    [Google Scholar]
  130. 130.  Scanlan PD, Buckling A 2012. Co-evolution with lytic phage selects for the mucoid phenotype of Pseudomonas fluorescens SBW25. ISME J 6:1148–58
    [Google Scholar]
  131. 131.  Scharf BE, Hynes MF, Alexandre GM 2016. Chemotaxis signaling systems in model beneficial plant–bacteria associations. Plant Mol. Biol. 90:549–59
    [Google Scholar]
  132. 132.  Scholl D 2017. Phage tail–like bacteriocins. Annu. Rev. Virol. 4:453–67
    [Google Scholar]
  133. 133.  Schwarczinger I, Nagy JK, Künstler A, Szabó L, Geider K et al. 2017. Characterization of Myoviridae and Podoviridae family bacteriophages of Erwinia amylovora from Hungary: potential of application in biological control of fire blight. Eur. J. Plant Pathol. 149:639–52
    [Google Scholar]
  134. 134.  Schwinghamer EA, Brockwell J 1978. Competitive advantage of bacteriocin and phage-producing strains of Rhizobium trifolii in mixed culture. Soil Biol. Biochem. 10:383–87
    [Google Scholar]
  135. 135.  Secor PR, Sweere JM, Michaels LA, Malkovskiy AV, Lazzareschi D et al. 2015. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 18:549–59
    [Google Scholar]
  136. 136.  Sharma RS, Mohmmed A, Babu CR 2002. Diversity among rhizobiophages from rhizospheres of legumes inhabiting three ecogeographical regions of India. Soil Biol. Biochem. 34:965–73
    [Google Scholar]
  137. 137.  Simpson AJG, Reinach FC, Arruda P, Abreu FA, Acencio M et al. 2000. The genome sequence of the plant pathogen Xylella fastidiosa. . Nature 406:151–57
    [Google Scholar]
  138. 138.  Sistrom M, Park D, O'Brien HE, Wang Z, Guttman DS et al. 2015. Genomic and gene-expression comparisons among phage-resistant type-IV pilus mutants of Pseudomonas syringae pathovar phaseolicola. . PLOS ONE 10:e0144514
    [Google Scholar]
  139. 139.  Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480:241–44
    [Google Scholar]
  140. 140.  Smit E, Wolters AC, Lee H, Trevors JT, Van Elsas JD 1996. Interactions between a genetically marked Pseudomonas fluorescens strain and bacteriophage ΦR2f in soil: effects of nutrients, alginate encapsulation, and the wheat rhizosphere. Microb. Ecol. 31:125–40
    [Google Scholar]
  141. 141.  Stacey G, Paau AS, Noel KD, Maier RJ, Silver LE, Brill WJ 1982. Mutants of Rhizobium japonicum defective in nodulation. Arch. Microbiol. 132:219–24
    [Google Scholar]
  142. 142.  Stephens PM, O'Sullivan M, O'Gara F 1987. Effect of bacteriophage on colonization of sugarbeet roots by fluorescent Pseudomonas spp. Appl. Environ. Microbiol. 53:1164–67
    [Google Scholar]
  143. 143.  Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW 1995. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. PNAS 92:8985–89
    [Google Scholar]
  144. 144.  Sullivan JT, Ronson CW 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. PNAS 95:5145–49
    [Google Scholar]
  145. 145.  Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD et al. 2002. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 184:3086–95
    [Google Scholar]
  146. 146.  Sutherland IW, Hughes KA, Skillman LC, Tait K 2004. The interaction of phage and biofilms. FEMS Microbiol. Lett. 232:1–6
    [Google Scholar]
  147. 147.  Swanson MM, Fraser G, Daniell TJ, Torrance L, Gregory PJ, Taliansky M 2009. Viruses in soils: morphological diversity and abundance in the rhizosphere. Ann. Appl. Biol. 155:51–60
    [Google Scholar]
  148. 148.  Takahashi R, Bowatte S, Taki K, Ohashi Y, Asakawa S, Kimura M 2011. High frequency of phage-infected bacterial cells in a rice field soil in Japan. Soil Sci. Plant Nutr. 57:35–39
    [Google Scholar]
  149. 149.  Takahashi R, Saka N, Honjo H, Asakawa S, Kimura M 2013. Comparison of the frequency of visibly infected bacterial cells between the soil and the floodwater in two Japanese rice fields. Soil Sci. Plant Nutr. 59:331–36
    [Google Scholar]
  150. 150.  Tanaka H, Negishi H, Maeda H 1990. Control of tobacco bacterial wilt by an avirulent strain of Pseudomonas solanacearum M4S and its bacteriophage. Jpn. J. Phytopathol. 56:243–46
    [Google Scholar]
  151. 151.  Toth IK, Pritchard L, Birch PR 2006. Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu. Rev. Phytopathol. 44:305–36
    [Google Scholar]
  152. 152.  Torsvik V, Øvreås L, Thingstad TF 2002. Prokaryotic diversity: magnitude, dynamics, and controlling factors. Science 296:1064–66
    [Google Scholar]
  153. 153.  Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A 2015. The importance of the microbiome of the plant holobiont. New Phytol 206:1196–206
    [Google Scholar]
  154. 154.  Varani AM, Monteiro-Vitorello CB, Nakaya HI, Van Sluys MA 2013. The role of prophage in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 51:429–51
    [Google Scholar]
  155. 155.  Vasse M, Torres-Barceló C, Hochberg ME 2015. Phage selection for bacterial cheats leads to population decline. Proc. R. Soc. B 282:20152207
    [Google Scholar]
  156. 156.  Vodovar N, Vallenet D, Cruveiller S, Rouy Z, Barbe V et al. 2006. Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nat. . Biotechnol 24:673–79
    [Google Scholar]
  157. 157.  Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A 2009. Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325:833
    [Google Scholar]
  158. 158.  Wagner PL, Neely MN, Zhang X, Acheson DW, Waldor MK, Friedman DI 2001. Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J. Bacteriol. 183:2081–85
    [Google Scholar]
  159. 159.  Wagner PL, Waldor MK 2002. Bacteriophage control of bacterial virulence. Infect. Immun. 70:3985–93
    [Google Scholar]
  160. 160.  Westra ER, Swarts DC, Staals RH, Jore MM, Brouns SJ, van der Oost J 2012. The CRISPRs, they are a-changin’: how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311–39
    [Google Scholar]
  161. 161.  Yu J, Peñaloza‐Vázquez A, Chakrabarty AM, Bender CL 1999. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol. Microbiol. 33:712–20
    [Google Scholar]
  162. 162.  Yu P, Mathieu J, Yang Y, Alvarez PJ 2017. Suppression of enteric bacteria by bacteriophages: importance of phage polyvalence in the presence of soil bacteria. Environ. Sci. Technol. 51:5270–78
    [Google Scholar]
  163. 163.  Zhang QG, Buckling A 2012. Phages limit the evolution of bacterial antibiotic resistance in experimental microcosms. Evol. Appl. 5:575–82
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-080417-045858
Loading
/content/journals/10.1146/annurev-phyto-080417-045858
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error