Mutualistic ants as an indirect defence against leaf pathogens

New Phytologist

Volumn 202, Issue 2, 2014, Pages 640-650

  González Teuber, Marcia ^a,b   Kaltenpoth, Martin ^a   Boland, Wilhelm ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b DEPARTAMENTO DE BIOLOGÍA   (Chile)

Author keywords

Ant protection; Ant plant mutualisms; Epiphytic bacterial communities; Indirect defence; Leaf pathogens

Indexed keywords

ANT; BACTERIUM; EPIPHYTE; LEGUME; MICROBIAL COMMUNITY; MUTUALISM; PLANT DEFENSE;

ACACIA; ACACIA HINDSII; BACTERIA (MICROORGANISMS); FABACEAE; FORMICIDAE; OTUS;

ACACIA; ANIMAL; ANT; ANT PROTECTION; ANT-PLANT MUTUALISMS; ARTICLE; BACTERIUM; EPIPHYTIC BACTERIAL COMMUNITIES; HERBIVORY; INDIRECT DEFENCE; LEAF PATHOGENS; MICROBIOLOGY; MICROFLORA; PLANT DISEASE; PLANT LEAF; SYMBIOSIS;

ANT PROTECTION; ANT-PLANT MUTUALISMS; EPIPHYTIC BACTERIAL COMMUNITIES; INDIRECT DEFENCE; LEAF PATHOGENS;

ACACIA; ANIMALS; ANTS; BACTERIA; HERBIVORY; MICROBIOTA; PLANT DISEASES; PLANT LEAVES; SYMBIOSIS;

EID: 84896545073     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12664     Document Type: Article

References (71)

1. Ahuja I, Kissen R, Bones AM. 2012. Phytoalexins in defense against pathogens. Trends in Plant Science 17: 73-90.
2. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
3. Arnon DI. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24: 1-15.
4. Berger S, Sinha AK, Roitsch T. 2007. Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. Journal of Experimental Botany 58: 4019-4026.
5. Bolton MD. 2009. Primary metabolism and plant defense-fuel for the fire. Molecular Plant-Microbe Interactions 22: 487-497.
6. Bolwell GP, Daudi A. 2009. Reactive oxygen species in plant-pathogen interactions. In: del Rio LA, Puppo A, eds. Reactive oxygen species in plant signaling. Berlin, Germany: Springer-Verlag, 113-133.
7. Bronstein JL. 1998. The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30: 150-161.
8. Bronstein JL. 2001. The exploitation of mutualisms. Ecology Letters 4: 277-287.
9. Brownlie JC, Johnson KN. 2009. Symbiont-mediated protection in insect hosts. Trends in Microbiology 17: 348-354.
10. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. 2010a. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267.
11. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI et al. 2010b. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
12. Chamberlain SA, Holland JN. 2009. Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90: 2384-2392.
13. Clement LW, Koppen SCW, Brand WA, Heil M. 2008. Strategies of a parasite of the ant-acacia mutualism. Behavioral Ecology and Sociobiology 62: 953-962.
14. Currie CR, Scott JA, Summerbell RC, Malloch D. 1999. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704.
15. Davidson DW, McKey D. 1993. The evolutionary ecology of symbiotic ant plant relationships. Journal of Hymenoptera Research 2: 13-83.
16. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
17. Eilmus S, Heil M. 2009. Bacterial associates of arboreal ants and their putative functions in an obligate ant-plant mutualism. Applied and Environmental Microbiology 75: 4324-4332.
18. Ercolani GL. 1991. Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microbial Ecology 21: 35-48.
19. Federle W, Maschwitz U, Fiala B. 1998. The two partner ant-plant system of Camponotus (Colobopsis) sp.1 and Macaranga puncticulata (Euphorbiaceae): natural history of the exceptional ant partner. Insectes Sociaux 45: 1-16.
20. Fonseca CR. 1994. Herbivory and the long-lived leaves of an Amazonian ant-tree. Journal of Ecology 82: 833-842.
21. Forsgren E, Olofsson TC, Vasquez A, Fries I. 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108.
22. de la Fuente MAS, Marquis RJ. 1999. The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia 118: 192-202.
23. González-Teuber M, Heil M. 2010. Pseudomyrmex ants and Acacia host plants join efforts to protect their mutualism from microbial threats. Plant Signaling and Behavior 5: 890-892.
24. Hammerschmidt R, Nuckles EM, Kuc J. 1982. Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiological Plant Pathology 20: 73-82.
25. Heil M. 2008. Indirect defence via tritrophic interactions. New Phytologist 178: 41-61.
26. Heil M, Baumann B, Andary C, Linsenmair KE, McKey D. 2002. Extraction and quantification of "condensed tannins" as valuable measure of plant anti-herbivore defence? Revisiting an old problem. Naturwissenschaften 89: 519-524.
27. Heil M, Fiala B, Boller T, Linsenmair KE. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86: 146-149.
28. Heil M, Greiner S, Meimberg H, Kruger R, Noyer JL, Heubl G, Linsenmair KE, Boland W. 2004. Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430: 205-208.
29. Heil M, McKey D. 2003. Protective ant-plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution, and Systematics 34: 425-453.
30. Heil M, Staehelin C, McKey D. 2000. Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences? Naturwissenschaften 87: 555-558.
31. Hirano CC, Upper CD. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae - a pathogen, ice nucleus, and epiphyte. Microbiology and Molecular Biology Reviews 64: 624-653.
32. Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD. 2010. Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Applied and Environmental Microbiology 76: 8117-8125.
33. Innerebner G, Knief C, Vorholt JA. 2011. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Applied and Environmental Microbiology 77: 3202-3210.
34. Ishak HD, Plowes R, Sen R, Kellner K, Meyer E, Estrada DA, Dowd SE, Mueller UG. 2011. Bacterial diversity in Solenopsis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 pyrosequencing. Microbial Ecology 61: 821-831.
35. Janzen DH. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20: 249-275.
36. Janzen DH. 1974. Swollen-thorn Acacias of Central America. Washington, DC, USA: Smithsonian Institution Press.
37. Janzen DH. 1975. Pseudomyrmex nigropilosa: a parasite of a mutualism. Science 188: 936-937.
38. Kadivar H, Stapleton AE. 2003. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microbial Ecology 45: 353-361.
39. Kaltenpoth M. 2009. Actinobacteria as mutualists: general healthcare for insects? Trends in Microbiology 17: 529-535.
40. Kaltenpoth M, Gottler W, Herzner G, Strohm E. 2005. Symbiotic bacteria protect wasp larvae from fungal infestation. Current Biology 15: 475-479.
41. Kautz S, Lumbsch HT, Ward PS, Heil M. 2009. How to prevent chaeting: a digestive specialization ties mutualistic plant-ants to their ant-plant partners. Evolution 63: 839-853.
42. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48: 251-275.
43. Letourneau DK. 1998. Ants, stem-borers, and fungal pathogens: experimental tests of a fitness advantage in Piper ant-plants. Ecology 79: 593-603.
44. Li WZ, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
45. Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Applied and Environmental Microbiology 69: 1875-1883.
46. Loake G, Grant M. 2007. Salicylic acid in plant defence - the players and protagonists. Current Opinion in Plant Biology 10: 466-472.
47. van Loon LC, Rep M, Pieterse CMJ. 2006. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44: 135-162.
48. van Loon LC, van Strien EA. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55: 85-97.
49. Mannanov RN, Sattarova RK. 2001. Antibiotics produced by Bacillus bacteria. Chemistry of Natural Compounds 37: 117-123.
50. Miller TEX. 2007. Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 116: 500-512.
51. Morgan ED. 2008. Chemical sorcery for sociality: exocrine secretions of ants (Hymenoptera: Formicidae). Myrmecological News 11: 79-90.
52. Ness JH, Morris WF, Bronstein JL. 2006. Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87: 912-921.
53. Oliver KM, Russell JA, Moran NA, Hunter MS. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences, USA 100: 1803-1807.
54. Porra RJ, Thompson WA, Kriedemann PE. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 107: 176-179.
55. Raine NE, Gammans N, Macfadyen IJ, Scrivner GK, Stone GN. 2004. Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant-plant. Ecological Entomology 29: 345-352.
56. de Roman M, Fernandez I, Wyatt T, Sahrawy M, Heil M, Pozo MJ. 2011. Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. Journal of Ecology 99: 36-45.
57. Rouse DI, Nordheim EV, Hirano SS, Upper CD. 1985. A model relating the probability of foliar disease incidence to the population frequencies of bacterial plant pathogens. Phytopathology 75: 505-509.
58. Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI. 2004. Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. Fems Microbiology Letters 239: 319-323.
59. Schmelzer E. 2002. Cell polarization, a crucial process in fungal defence. Trends in Plant Science 7: 411-415.
60. Schulze B, Lauchli R, Sonwa MM, Schmidt A, Boland W. 2006. Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Analytical Biochemistry 348: 269-283.
61. Seigler DS, Ebinger JE. 1995. Taxonomic revision of the ant-acacias (Fabaceae, Mimosoideae; Acacia, series Gummiferae) of the new world. Annals of the Missouri Botanical Garden 82: 117-138.
62. Skwarra E. 1935. Ökologie der Lebensgemeinschaften mexikanischer Ameisenpflanzen. Zeitschrift für Morphologie und Ökologie der Tiere 29: 306-373.
63. Stromberg KD, Kinkel LL, Leonard KJ. 1999. Relationship between phyllosphere population sizes of Xanthomonas translucens pv translucens and bacterial leaf streak severity on wheat seedlings. Phytopathology 89: 131-135.
64. Suda W, Nagasaki A, Shishido M. 2009. Powdery mildew-infection changes bacterial community composition in the phyllosphere. Microbes and Environment 24: 217-223.
65. Sun Y, Wolcott RD, Dowd SE. 2011. Tag-encoded FLX amplicon pyrosequencing for the elucidation of microbial and functional gene diversity in any environment. Methods in Molecular Biology 733: 129-141.
66. Visser R, Holzapfel WH. 1992. Lactic acid bacteria in the control of plant pathogens. In: Wood BJB, ed. The lactic acid bacteria, vol. 1. London, UK: Elsevier Science Publishers, 193-210.
67. Visser R, Holzapfel WH, Bezuidenhout JJ, Kotzé JM. 1986. Antagonism of lactic acid bacteria against phytopathogenic bacteria. Applied and Environmental Microbiology 52: 552-555.
68. Vorholt JA. 2012. Microbial life in the phyllosphere. Nature Reviews Microbiology 10: 828-840.
69. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261-5267.
70. Ward PS. 1993. Systematic studies on Pseudomyrmex acacia-ants (Hymenoptera: Formicidae: Pseudomyrmecinae). Journal of Hymenoptera Research 2: 117-168.
71. Yang C-H, Crowley DE, Borneman J, Keen NT. 2001. Microbial phyllosphere populations are more complex than previously realized. Proceedings of the National Academy of Sciences, USA 98: 3889-3894.