1932

Abstract

Flowers at times host abundant and specialized communities of bacteria and fungi that influence floral phenotypes and interactions with pollinators. Ecological processes drive variation in microbial abundance and composition at multiple scales, including among plant species, among flower tissues, and among flowers on the same plant. Variation in microbial effects on floral phenotype suggests that microbial metabolites could cue the presence or quality of rewards for pollinators, but most plants are unlikely to rely on microbes for pollinator attraction or reproduction. From a microbial perspective, flowers offer opportunities to disperse between habitats, but microbial species differ in requirements for and benefits received from such dispersal. The extent to which floral microbes shape the evolution of floral traits, influence fitness of floral visitors, and respond to anthropogenic change is unclear. A deeper understanding of these phenomena could illuminate the ecological and evolutionary importance of floral microbiomes and their role in the conservation of plant–pollinator interactions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-011720-013401
2020-11-02
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/51/1/annurev-ecolsys-011720-013401.html?itemId=/content/journals/10.1146/annurev-ecolsys-011720-013401&mimeType=html&fmt=ahah

Literature Cited

  1. Adler LS. 2000. The ecological significance of toxic nectar. Oikos 91:409–20
    [Google Scholar]
  2. Alexander HM, Antonovics J. 1988. Disease spread and population dynamics of anther-smut infection of Silene alba caused by the fungus Ustilago violacea. J. Ecol 76:91–104
    [Google Scholar]
  3. Alvarez-Perez S, Herrera CM, de Vega C 2012. Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol. Ecol. 80:3591–602
    [Google Scholar]
  4. An S-Q, Potnis N, Dow M, Vorhölter F-J, He Y-Q et al. 2020. Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol. Rev 44:1–32
    [Google Scholar]
  5. Bartlewicz J, Pozo MI, Honnay O, Lievens B, Jacquemyn H 2016. Effects of agricultural fungicides on microorganisms associated with floral nectar: susceptibility assays and field experiments. Environ. Sci. Pollut. Res. 23:1919776–86
    [Google Scholar]
  6. Batra LR, Batra SWT, Bohart G 1973. The mycoflora of domesticated and wild bees (Apoidea). Mycopathol. Mycol. Appl. 49:13–44
    [Google Scholar]
  7. Belisle M, Peay KG, Fukami T 2012. Flowers as islands: spatial distribution of nectar-inhabiting microfungi among plants of Mimulus aurantiacus, a hummingbird-pollinated shrub. Microb. Ecol. 63:711–18
    [Google Scholar]
  8. Biere A, Honders SC. 2006. Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia. . New Phytol 169:719–27
    [Google Scholar]
  9. Boachon B, Lynch JH, Ray S, Yuan J, Caldo KMP et al. 2019. Natural fumigation as a mechanism for volatile transport between flower organs. Nat. Chem. Biol. 15:583–88
    [Google Scholar]
  10. Boutroux L. 1884. Sur la conservation des ferments alcooliques dans la nature. Ann. Sci. Nat. Sér. IV Bot. 17:145–209
    [Google Scholar]
  11. Brysch-Herzberg M. 2004. Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiol. Ecol. 50:87–100
    [Google Scholar]
  12. Burdon RC, Junker RR, Scofield DG, Parachnowitsch AL 2018. Bacteria colonising Penstemon digitalis show volatile and tissue-specific responses to a natural concentration range of the floral volatile linalool. Chemoecology 28:11–19
    [Google Scholar]
  13. Canto A, Herrera CM, Medrano M, Perez R, Garcia IM 2008. Pollinator foraging modifies nectar sugar composition in Helleborus foetidus (Ranunculaceae): an experimental test. Am. J. Bot. 95:315–20
    [Google Scholar]
  14. Carter C, Graham RA, Thornburg RW 1999. Nectarin I is a novel, soluble germin-like protein expressed in the nectar of Nicotiana sp. Plant Mol. Biol. 41:207–16
    [Google Scholar]
  15. Chanbusarakum L, Ullman D. 2008. Characterization of bacterial symbionts in Frankliniella occidentalis (Pergande), Western flower thrips. J. Invertebr. Pathol. 99:318–25
    [Google Scholar]
  16. Chappell CR, Fukami T. 2018. Nectar yeasts: a natural microcosm for ecology. Yeast 35:417–23
    [Google Scholar]
  17. Corby-Harris V, Maes P, Anderson KE 2014. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLOS ONE 9:e95056
    [Google Scholar]
  18. Danforth BN, Minckley RL, Neff JL, Fawcett F 2019. The Solitary Bees: Biology, Evolution, Conservation Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  19. de Vega C, Herrera CM 2013. Microorganisms transported by ants induce changes in floral nectar composition of an ant-pollinated plant. Am. J. Bot. 100:792–800
    [Google Scholar]
  20. de Vega C, Herrera CM, Johnson S 2009. Yeasts in floral nectar of some South African plants: quantification and associations with pollinator type and sugar concentration. South Afr. J. Bot. 75:798–806
    [Google Scholar]
  21. Dhami MK, Hartwig T, Fukami T 2016. Genetic basis of priority effects: insights from nectar yeast. Proc. R. Soc. B 283:20161455
    [Google Scholar]
  22. Dhami MK, Hartwig T, Letten AD, Banf M, Fukami T 2018. Genomic diversity of a nectar yeast clusters into metabolically, but not geographically, distinct lineages. Mol. Ecol. 27:2067–76
    [Google Scholar]
  23. Dobson HEM. 2006. Relationship between floral fragrance composition and type of pollinator. Biology of Floral Scent N Dudareva, E Pichersky 147–98 Boca Raton, FL: CRC Press
    [Google Scholar]
  24. Durrer S, Schmid-Hempel P. 1994. Shared use of flowers leads to horizontal pathogen transmission. Proc. R. Soc. B. 258:299–302
    [Google Scholar]
  25. Eastgate JA. 2000. Erwinia amylovora: the molecular basis of fireblight disease. Mol. Plant Pathol. 1:325–29
    [Google Scholar]
  26. Eisikowitch D, Lachance MA, Kevan PG, Willis S, Collins-Thompson DL 1990. The effect of the natural assemblage of microorganisms and selected strains of the yeast Metschnikowia reukaufii in controlling the germination of pollen of the common milkweed Asclepias syriaca. Can. J. Bot 68:51163–65
    [Google Scholar]
  27. Engel P, Martinson VG, Moran NA 2012. Functional diversity within the simple gut microbiota of the honey bee. PNAS 109:11002–7
    [Google Scholar]
  28. Farré-Armengol G, Filella I, Llusia J, Peñuelas J 2016. Bidirectional interaction between phyllospheric microbiotas and plant volatile emissions. Trends Plant Sci 21:10854–60
    [Google Scholar]
  29. Figueroa LL, Blinder M, Grincavitch C, Jelinek A, Mann EK et al. 2019. Bee pathogen transmission dynamics: deposition, persistence and acquisition on flowers. Proc. R. Soc. B 286:20190603
    [Google Scholar]
  30. Finkel OM, Castrillo G, Paredes SH, González IS, Dangl JL 2017. Understanding and exploiting plant beneficial microbes. Curr. Opin. Plant Biol. 38:155–63
    [Google Scholar]
  31. Fokkema NJ. 1971. The effect of pollen in the phyllosphere of rye on colonization by saprophytic fungi and on infection by Helminthosporium sativum and other leaf pathogens. Neth. J. Plant Pathol. 77:1–60
    [Google Scholar]
  32. Fridman S, Izhaki I, Gerchman Y, Halpern M 2012. Bacterial communities in floral nectar. Environ. Microbiol. Rep. 4:97–104
    [Google Scholar]
  33. Fouks B, Lattorff HMG. 2011. Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLOS ONE 6:10e26328
    [Google Scholar]
  34. Fukami T. 2015. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46:1–23
    [Google Scholar]
  35. Galen C, Kaczorowski R, Todd SL, Geib J, Raguso RA 2011. Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. Am. . Nat 177:258–72
    [Google Scholar]
  36. Golonka AM, Johnson BO, Freeman J, Hinson DW 2014. Impact of nectarivorous yeasts on Silene caroliniana’s scent. East. Biol. 3:1–26
    [Google Scholar]
  37. González-Teuber M, Heil M. 2009. Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal. Behav. 4:809–13
    [Google Scholar]
  38. Groen SC, Jiang S, Murphy AM, Cunniffe NJ, Westwood JH et al. 2016. Virus infection of plants alters pollinator preference: a payback for susceptible hosts. ? PLOS Pathog 12:8e1005790
    [Google Scholar]
  39. Helletsgruber C, Dötterl S, Ruprecht U, Junker RR 2017. Epiphytic bacteria alter floral scent emissions. J. Chem. Ecol. 43:1073–77
    [Google Scholar]
  40. Herrera CM. 2020. Flower traits, habitat, and phylogeny as predictors of pollinator service: a plant community perspective. Ecol. Monogr. 90:e01402
    [Google Scholar]
  41. Herrera CM, Canto A, Pozo MJ, Bazaga P 2010. Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc. R. Soc. B 277:747–54
    [Google Scholar]
  42. Herrera CM, Garcia IM, Perez R 2008. Invisible floral larcenies: Microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–76
    [Google Scholar]
  43. Herrera CM, Pozo MI, Medrano M 2013. Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94:273–79
    [Google Scholar]
  44. Herrera CM, Vega C, Canto A, Pozo MJ 2009. Yeasts in floral nectar: a quantitative survey. Ann. Bot. 103:1415–23
    [Google Scholar]
  45. Hinton D, Bacon C. 1985. The distribution and ultrastructure of the endophyte of toxic tall fescue. Can. J. Bot. 63:36–42
    [Google Scholar]
  46. Hodgson S, de Cates C, Hodgson J, Morley NJ, Sutton BC, Gange AC 2014. Vertical transmission of fungal endophytes is widespread in forbs. Ecol. Evol. 4:1199–208
    [Google Scholar]
  47. Hua SST, Beck JJ, Sarreal SBL, Gee W 2014. The major volatile compound 2-phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergillus flavus. . Mycotoxin Res 30:71–78
    [Google Scholar]
  48. Huang HC, Kokko EG. 1985. Infection of alfalfa pollen by Verticillium albo-atrum. . Phytopathology 75:7859–65
    [Google Scholar]
  49. Huang M, Sanchez‐Moreiras AM, Abel C, Sohrabi R, Lee S et al. 2012. The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)‐β‐caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008
    [Google Scholar]
  50. Inouye DW, Gill DE, Dudash MR, Fenster CB 1994. A model and lexicon for pollen fate. Am. J. Bot. 81:1517–30
    [Google Scholar]
  51. Junker RR, Keller A. 2015. Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMS Microbiol. Ecol. 91:fiv097
    [Google Scholar]
  52. Junker RR, Kuppler J, Amo L, Blande JD, Borges RM et al. 2018. Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications. New Phytol 220:739–49
    [Google Scholar]
  53. Junker RR, Loewel C, Gross R, Dötterl S, Keller A, Blüthgen N 2011. Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol 13:918–24
    [Google Scholar]
  54. Junker RR, Tholl D. 2013. Volatile organic compound mediated interactions at the plant-microbe interface. J. Chem. Ecol. 39:7810–25
    [Google Scholar]
  55. Kearns L, Hale C. 1995. Incidence of bacteria inhibitory to Erwinia amylovora from blossoms in New Zealand apple orchards. Plant Pathol 44:918–24
    [Google Scholar]
  56. Khan MA, Zhao YF, Korban SS 2012. Molecular mechanisms of pathogenesis and resistance to the bacterial pathogen Erwinia amylovora, causal agent of fire blight disease in Rosaceae. Plant Mol. Biol. Rep. 30:247–60
    [Google Scholar]
  57. Kim D-R, Cho G, Jeon C-W, Weller DM, Thomashow LS et al. 2019. A mutualistic interaction between Streptomyces bacteria, strawberry plants and pollinating bees. Nat. Commun. 10:4802
    [Google Scholar]
  58. Koch H, Woodward J, Langat MK, Brown MJF, Stevenson PC 2019. Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite. Curr. Biol. 29:3494–500.e5
    [Google Scholar]
  59. Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF, Janzen DH 2001. Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1:1–8
    [Google Scholar]
  60. Lara C, Ornelas JF. 2003. Hummingbirds as vectors of fungal spores in Moussonia deppeana (Gesneriaceae): taking advantage of a mutualism. ? Am. J. Bot. 90:262–69
    [Google Scholar]
  61. Laviad-Shitrit S, Izhaki I, Whitman WB, Shapiro N, Woyke T et al. 2020. Draft genome of Rosenbergiella nectarea strain 8N4T provides insights into the potential role of this species in its plant host. PeerJ 8:e8822
    [Google Scholar]
  62. Lenaerts M, Goelen T, Paulussen C, Herrera-Malaver B, Steensels J et al. 2017. Nectar bacteria affect life history of a generalist aphid parasitoid by altering nectar chemistry. Funct. Ecol. 31:2061–69
    [Google Scholar]
  63. Lindow SE, Suslow TV. 2003. Temporal dynamics of the biocontrol agent Pseudomonas fluorescens strain A506 in flowers in inoculated pear trees. Phytopathology 93:727–37
    [Google Scholar]
  64. Manirajan BA, Ratering S, Rusch V, Schwiertz A, Geissler-Plaum R et al. 2016. Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environ. Microbiol. 18:5161–74
    [Google Scholar]
  65. Martínez del Rio C. 1990. Sugar preferences in hummingbirds: the influence of subtle chemical differences on food choice. Condor 92:1022–30
    [Google Scholar]
  66. Massoni J, Bortfeld-Miller M, Jardillier L, Salazar G, Sunagawa S, Vorholt JA 2019. Consistent host and organ occupancy of phyllosphere bacteria in a community of wild herbaceous plant species. ISME J 14:245–58
    [Google Scholar]
  67. McArt SH, Koch H, Irwin RE, Adler LS 2014. Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol. Lett. 17:5624–36
    [Google Scholar]
  68. McArt SH, Miles TD, Rodriguez-Saona C, Schilder A, Adler LS, Grieshop MJ 2016. Floral scent mimicry and vector-pathogen associations in a pseudoflower-inducing plant pathogen system. PLOS ONE 11:e0165761
    [Google Scholar]
  69. McFrederick QS, Thomas JM, Neff JL, Vuong HQ, Russell KA et al. 2017. Flowers and wild megachilid bees share microbes. Microb. Ecol. 73:188–200
    [Google Scholar]
  70. McFrederick QS, Wcislo WT, Taylor DR, Ishak HD, Dowd SE, Mueller UG 2012. Environment or kin: Whence do bees obtain acidophilic bacteria. ? Mol. Ecol. 21:1754–68
    [Google Scholar]
  71. Mittelbach M, Yurkov AM, Stoll R, Begerow D 2016. Inoculation order of nectar-borne yeasts opens a door for transient species and changes nectar rewarded to pollinators. Fungal Ecol 22:90–97
    [Google Scholar]
  72. Morris M, Frixione N, Burkert A, Dinsdale E, Vannette RL 2020. Microbial abundance, composition, and function in nectar are shaped by flower visitor identity. FEMS Microbiol. Ecol. 96:fiaa003
    [Google Scholar]
  73. Naqvi SS, Harper A, Carter C, Ren G, Guirgis A et al. 2005. Nectarin IV, a potent endoglucanase inhibitor secreted into the nectar of ornamental tobacco plants. Isolation, cloning, and characterization. Plant Physiol 139:1389–400
    [Google Scholar]
  74. O'Garro L, Charlemange E. 1994. Comparison of bacterial growth and activity of glucanase and chitinase in pepper leaf and flower tissue infected with Xanthomonas campestris pv. vesicatoria. Physiol. Mol. Plant Pathol. 45:181–88
    [Google Scholar]
  75. Palmer‐Young EC, Farrell IW, Adler LS, Milano NJ, Egan PA et al. 2019. Chemistry of floral rewards: intra‐ and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecol. Monogr. 89:e01335
    [Google Scholar]
  76. Parachnowitsch AL, Manson JS, Sletvold N 2018. Evolutionary ecology of nectar. Ann. Bot. 123:247–61
    [Google Scholar]
  77. Peay KG, Belisle M, Fukami T 2012. Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proc. R. Soc. B 279:749–58
    [Google Scholar]
  78. Peñuelas J, Farré-Armengol G, Llusia J, Gargallo-Garriga A, Rico L et al. 2014. Removal of floral microbiota reduces floral terpene emissions. Sci. Rep. 4:6727
    [Google Scholar]
  79. Pozo MI, de Vega C, Canto A, Herrera CM 2009. Presence of yeasts in floral nectar is consistent with the hypothesis of microbial-mediated signaling in plant-pollinator interactions. Plant Signal. Behav. 4:1102–4
    [Google Scholar]
  80. Pozo MI, Jacquemyn H. 2019. Addition of pollen increases growth of nectar-living yeasts. FEMS Microbiol. Lett. 366:fnz191
    [Google Scholar]
  81. Pozo MI, Lachance M-A, Herrera CM 2012. Nectar yeasts of two southern Spanish plants: the roles of immigration and physiological traits in community assembly. FEMS Microbiol. Ecol. 80:281–93
    [Google Scholar]
  82. Pozo MI, van Kemenade G, van Oystaeyen A, Aledón-Catalá T, Benavente A et al. 2020. The impact of yeast presence in nectar on bumble bee behavior and fitness. Ecol. Monogr. 90:e01393
    [Google Scholar]
  83. Primack RB. 1985. Longevity of individual flowers. Annu. Rev. Ecol. Syst. 16:15–37
    [Google Scholar]
  84. Pusey PL. 1999. Effect of nectar on microbial antagonists evaluated for use in control of fire blight of pome fruits. Phytopathology 89:39–46
    [Google Scholar]
  85. Pusey PL, Stockwell VO, Mazzola M 2009. Epiphytic bacteria and yeasts on apple blossoms and their potential as antagonists of Erwinia amylovora. . Phytopathology 99:571–81
    [Google Scholar]
  86. Pusey PL, Stockwell VO, Reardon CL, Smits TH, Duffy B 2011. Antibiosis activity of Pantoea agglomerans biocontrol strain E325 against Erwinia amylovora on apple flower stigmas. Phytopathology 101:1234–41
    [Google Scholar]
  87. Raguso RA. 2004. Why are some floral nectars scented. ? Ecology 85:1486–94
    [Google Scholar]
  88. Rebolleda Gómez M, Ashman T-L 2019. Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome. Mol. Ecol. 28:5155–71
    [Google Scholar]
  89. Rebolleda‐Gómez M, Forrester NJ, Russell AL, Wei N, Fetters AM et al. 2019. Gazing into the anthosphere: considering how microbes influence floral evolution. New Phytol 224:1012–20
    [Google Scholar]
  90. Rering CC, Beck JJ, Hall GW, McCartney MM, Vannette RL 2018. Nectar‐inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytol 220:750–59
    [Google Scholar]
  91. Rering CC, Vannette RL, Schaeffer RN, Beck JJ 2020. Microbial co-occurrence in floral nectar affects metabolites and attractiveness to a generalist pollinator. J. Chem. Ecol. 46:65967
    [Google Scholar]
  92. Rivest S, Forrest JRK. 2019. Defence compounds in pollen: Why do they occur and how do they affect the ecology and evolution of bees. ? New Phytol 225:1053–64
    [Google Scholar]
  93. Rosa CA, Lachance M-A, Silva JOC, Teixeira ACP, Marini MM et al. 2003. Yeast communities associated with stingless bees. FEMS Yeast Res 4:271–75
    [Google Scholar]
  94. Roulston TAH, Cane JH. 2000. Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222:187–209
    [Google Scholar]
  95. Rourke J, Wiens D. 1977. Convergent floral evolution in South African and Australian Proteaceae and its possible bearing on pollination by nonflying mammals. Ann. Mo. Bot. Gard. 64:1–17
    [Google Scholar]
  96. Roy BA. 1993. Floral mimicry by a plant pathogen. Nature 362:56–58
    [Google Scholar]
  97. Roy R, Schmitt AJ, Thomas JB, Carter CJ 2017. Nectar biology: from molecules to ecosystems. Plant Sci 262:148–64
    [Google Scholar]
  98. Russell AL, Ashman T-L. 2019. Associative learning of flowers by generalist bumble bees can be mediated by microbes on the petals. Behav. Ecol. 30:746–55
    [Google Scholar]
  99. Russell AL, Rebolleda-Gómez M, Shaible TM, Ashman T-L 2019. Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers. Ecosphere 10:e02714
    [Google Scholar]
  100. Samuni-Blank M, Izhaki I, Laviad S, Bar-Massada A, Gerchman Y, Halpern M 2014. The role of abiotic environmental conditions and herbivory in shaping bacterial community composition in floral nectar. PLOS ONE 9:e99107
    [Google Scholar]
  101. Schaeffer RN, Irwin RE. 2014. Yeasts in nectar enhance male fitness in a montane perennial herb. Ecology 95:1792–98
    [Google Scholar]
  102. Schaeffer RN, Mei YZ, Andicoechea J, Manson JS, Irwin RE 2017. Consequences of a nectar yeast for pollinator preference and performance. Funct. Ecol. 31:613–21
    [Google Scholar]
  103. Schaeffer RN, Rering CC, Maalouf I, Beck JJ, Vannette RL 2019. Microbial metabolites elicit distinct olfactory and gustatory preferences in bumblebees. Biol. Lett. 15:20190132
    [Google Scholar]
  104. Schaeffer RN, Vannette RL, Brittain C, Williams NM, Fukami T 2017. Non‐target effects of fungicides on nectar‐inhabiting fungi of almond flowers. Environ. Microbiol. Rep. 9:79–84
    [Google Scholar]
  105. Schaeffer RN, Vannette RL, Irwin RE 2015. Nectar yeasts in Delphinium nuttallianum (Ranunculaceae) and their effects on nectar quality. Fungal Ecol 18:100–6
    [Google Scholar]
  106. Schmitt AJ, Sathoff AE, Holl C, Bauer B, Samac DA, Carter CJ 2018. The major nectar protein of Brassica rapa is a non-specific lipid transfer protein, BrLTP2.1, with strong antifungal activity. J. Exp. Bot. 69:5587–97
    [Google Scholar]
  107. Schroth MN, Thomson SV, Hildebrand DC, Moller WJ 1974. Epidemiology and control of fire blight. Annu. Rev. Phytopathol. 12:389–412
    [Google Scholar]
  108. Shade A, McManus PS, Handelsman J 2013. Unexpected diversity during community succession in the apple flower microbiome. mBio 4:e00602–12
    [Google Scholar]
  109. Shykoff JA, Bucheli E, Kaltz O 2017. Anther smut disease in Dianthus silvester (Caryophyllaceae): natural selection on floral traits. Evolution 51:383–92
    [Google Scholar]
  110. Smessaert J, Van Geel M, Verreth C, Crauwels S, Honnay O et al. 2019. Temporal and spatial variation in bacterial communities of “Jonagold” apple (Malus x domestica Borkh.) and “Conference” pear (Pyrus communis L.) floral nectar. MicrobiologyOpen 8:12e918
    [Google Scholar]
  111. Sobhy IS, Baets D, Goelen T, Herrera-Malaver B, Bosmans L et al. 2018. Sweet scents: Nectar specialist yeasts enhance nectar attraction of a generalist aphid parasitoid without affecting survival. Front. Plant Sci. 9:1009
    [Google Scholar]
  112. Steffan SA, Dharampal PS, Danforth BN, Gaines-Day HR, Takizawa Y, Chikaraishi Y 2019. Omnivory in bees: elevated trophic positions among all major bee families. Am. Nat. 194:414–21
    [Google Scholar]
  113. Strauss SY, Whittall JB. 2006. Non-pollinator agents of selection on floral traits. Ecology and Evolution of Flowers LD Harder, SCH Barrett 120–38 New York: Oxford Univ. Press
    [Google Scholar]
  114. Talbert TJ. 1925. Fire blight of apples and pears Circ. 137, Univ. Mo. Coll. Agric., Agric. Exp. Stn Columbia, MO:
    [Google Scholar]
  115. Thornburg RW, Carter C, Powell A, Mittler R, Rizhsky L, Horner HT 2003. A major function of the tobacco floral nectary is defense against microbial attack. Plant Syst. Evol. 238:211–18
    [Google Scholar]
  116. Tucker CM, Fukami T. 2014. Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes. Proc. R. Soc. B 281:177820132637
    [Google Scholar]
  117. Urru I, Stensmyr MC, Hansson BS 2011. Pollination by brood-site deception. Phytochemistry 72:1655–66
    [Google Scholar]
  118. Ushio M, Yamasaki E, Takasu H, Nagano AJ, Fujinaga S et al. 2015. Microbial communities on flower surfaces act as signatures of pollinator visitation. Sci. Rep. 5:8695
    [Google Scholar]
  119. Vanneste JL. 2000. Fire Blight: The Disease and Its Causative Agent, Erwinia amylovora New York: CABI Publ.
    [Google Scholar]
  120. Vannette RL, Fukami T. 2014. Historical contingency in species interactions: towards niche-based predictions. Ecol. Lett. 17:115–24
    [Google Scholar]
  121. Vannette RL, Fukami T. 2016. Nectar microbes can reduce secondary metabolites in nectar and alter effects on nectar consumption by pollinators. Ecology 97:1410–19
    [Google Scholar]
  122. Vannette RL, Fukami T. 2017. Dispersal enhances beta diversity in nectar microbes. Ecol. Lett. 20:901–10
    [Google Scholar]
  123. Vannette RL, Fukami T. 2018. Contrasting effects of yeasts and bacteria on floral nectar traits. Ann. Bot. 121:1343–49
    [Google Scholar]
  124. Vannette RL, Gauthier M-PL, Fukami T 2013. Nectar bacteria, but not yeast, weaken a plant-pollinator mutualism. Proc. R. Soc. B 280:20122601
    [Google Scholar]
  125. von Arx M, Moore A, Davidowitz G, Arnold AE 2019. Diversity and distribution of microbial communities in floral nectar of two night-blooming plants of the Sonoran Desert. PLOS ONE 14:e0225309
    [Google Scholar]
  126. Voulgari-Kokota A, Grimmer G, Steffan-Dewenter I, Keller A 2018. Bacterial community structure and succession in nests of two megachilid bee genera. FEMS Microbiol. Ecol. 95:fiy218
    [Google Scholar]
  127. Voulgari-Kokota A, Steffan-Dewenter I, Keller A 2020. Susceptibility of red mason bee larvae to bacterial threats due to microbiome exchange with imported pollen provisions. Insects 11:6373
    [Google Scholar]
  128. Vuong HQ, McFrederick QS. 2019. Comparative genomics of wild bee and flower isolated Lactobacillus reveals potential adaptation to the bee host. Genome Biol. Evol. 11:2151–61
    [Google Scholar]
  129. Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS 2012. The overlooked biodiversity of flower-visiting invertebrates. PLOS ONE 7:e45796
    [Google Scholar]
  130. Wei N, Ashman T-L. 2018. The effects of host species and sexual dimorphism differ among root, leaf and flower microbiomes of wild strawberries in situ. Sci. Rep. 8:5195
    [Google Scholar]
  131. Wiens F, Zitzmann A, Lachance M-A, Yegles M, Pragst F, Wurst FM 2008. Chronic intake of fermented floral nectar by wild treeshrews. PNAS 105:10426–31
    [Google Scholar]
  132. Wilson M, Lindow SE. 1994. Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl. Environ. Microbiol. 60:4468–77
    [Google Scholar]
  133. Yang M, Deng G-C, Gong Y-B, Huang S-Q 2019. Nectar yeasts enhance the interaction between Clematis akebioides and its bumblebee pollinator. Plant Biol 21:732–37
    [Google Scholar]
  134. Zemenick AT, Vannette RL, Rosenheim JA 2019. Linked networks reveal dual roles of insect dispersal and species sorting for bacterial communities in flowers. bioRxiv 847376. https://doi.org/10.1101/847376
    [Crossref]
/content/journals/10.1146/annurev-ecolsys-011720-013401
Loading
/content/journals/10.1146/annurev-ecolsys-011720-013401
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