Anthosphere Microbiome and Their Associated Interactions at the Aromatic Interface

  • Nagarathinam Arunkumar
  • Suchitra Rakesh
  • Kaushik Rajaram
  • Narayanasamy Ravi Kumar
  • Siva Sundara Kumar DurairajanEmail author


The American quote “snug as a bug in a rug” (which means very comfortable and everyone has their own tastes) fits perfectly for the relation between plant and microbes with their associated interactions. Microbes interact at anthosphere, caulosphere, carposphere, phyllophane, rhizosphere, and spermosphere regions of the plants, and the plant-microbe interface acts as a medium of communication between these two diversified living systems. The interface is influenced by an extensive variety of biotic and abiotic determinants responsible for shaping plant-associated habitats, considerably modifying the active composition of the microbial communities, which alter themselves according to the environment for beneficial interactions. The microbiome of root and leaf interactions is most studied as evident from the availability of humongous literature; however, even a small microhabitat such as the anthosphere has its own group of associated microbes obtained from autochthonous or allochthonous. In addition, these microhabitats are contiguous with mutualistic pollinators, florivores, and nectar robbers, which alter the dynamic microbial inhabitants of these aromatic interfaces. To attain sustainability in plant conservation, food, and agriculture, an in-depth understanding of the entire plant-microbe environment is crucial. This chapter was written to provide an overview of the different interfaces, in particular, the anthosphere region of the phyllosphere.


Phyllosphere Spermosphere Anthosphere Caulosphere Carposphere Phyllophane Rhizosphere 


  1. Adam ZR, Fahrenbach AC, Kacar B, Aono M (2018) Prebiotic geochemical automata at the intersection of radiolytic chemistry, physical complexity, and systems biology. Complexity 2018:1. CrossRefGoogle Scholar
  2. Aizenberg-Gershtein Y, Izhaki I, Halpern M (2013) Do honeybees shape the bacterial community composition in floral nectar? PLoS One 8(7):e67556PubMedPubMedCentralCrossRefGoogle Scholar
  3. Aleklett K, Hart M, Shade A (2014) The microbial ecology of flowers: an emerging frontier in phyllosphere research. Botany 92(4):253–266CrossRefGoogle Scholar
  4. Álvarez-Pérez S, Herrera CM (2013) Composition, richness and nonrandom assembly of culturable bacterial–microfungal communities in floral nectar of Mediterranean plants. FEMS Microbiol Ecol 83(3):685–699PubMedCrossRefGoogle Scholar
  5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681PubMedCrossRefGoogle Scholar
  6. Barret M, Briand M, Bonneau S, Préveaux A, Valière S, Bouchez O, Jacques MA (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81(4):1257–1266PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bartlewicz J, Lievens B, Honnay O, Jacquemyn H (2016) Microbial diversity in the floral nectar of Linaria vulgaris along an urbanization gradient. BMC Ecol 16(1):18PubMedPubMedCentralCrossRefGoogle Scholar
  8. Basim E, Basim H, Özcan M (2006) Antibacterial activities of Turkish pollen and propolis extracts against plant bacterial pathogens. J Food Eng 77(4):992–996CrossRefGoogle Scholar
  9. 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(4):711–718PubMedCrossRefGoogle Scholar
  10. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486PubMedCrossRefGoogle Scholar
  11. Bringel F, Couée I (2015) Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front Microbiol 6:486PubMedPubMedCentralCrossRefGoogle Scholar
  12. Brysch-Herzberg M (2004) Ecology of yeasts in plant–bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 50(2):87–100PubMedCrossRefGoogle Scholar
  13. Bumroongsook S (2018) Abiotic and biotic factors affecting the occurrence of thrips on lotus flowers. Appl Ecol Environ Res 16(3):2827–2836CrossRefGoogle Scholar
  14. Chohan S, Perveen R, Abid M, Naqvi AH, Naz S (2017) Management of seed borne fungal diseases of tomato: a review. Pak J Phytopathol 29(1):193–200CrossRefGoogle Scholar
  15. 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(4):792–800PubMedCrossRefGoogle Scholar
  16. El-Gawad HA, Ibrahim MFM, El-Hafez AA, El-Yazied AA (2015) Contribution of pink pigmented facultative methylotrophic bacteria in promoting antioxidant enzymes, growth and yield of snap bean. Synthesis 2:4Google Scholar
  17. Felestrino ÉB, Santiago IF, Freitas LDS, Rosa LH, Ribeiro SP, Moreira LM (2017) Plant growth promoting bacteria associated with Langsdorffia hypogaea-rhizosphere-host biological interface: a neglected model of bacterial prospection. Front Microbiol 8:172PubMedPubMedCentralCrossRefGoogle Scholar
  18. Field B, Jordán F, Osbourn A (2006) First encounters–deployment of defence-related natural products by plants. New Phytol 172(2):193–207PubMedCrossRefGoogle Scholar
  19. Frank AC, Saldierna Guzmán JP, Shay JE (2017) Transmission of bacterial endophytes. Microorganisms 5(4):70PubMedCentralCrossRefGoogle Scholar
  20. Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environ Microbiol Rep 4(1):97–104PubMedCrossRefGoogle Scholar
  21. Fürnkranz M, Lukesch B, Müller H, Huss H, Grube M, Berg G (2012) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb Ecol 63(2):418–428PubMedCrossRefGoogle Scholar
  22. Gao Y, Jin YJ, Li HD, Chen HJ (2005) Volatile organic compounds and their roles in bacteriostasis in five conifer species. J Integr Plant Biol 47(4):499–507CrossRefGoogle Scholar
  23. Garcia J, Kao-Kniffin J (2018) Microbial group dynamics in plant rhizospheres and their implications on nutrient cycling. Front Microbiol 9.
  24. Gianfreda L (2015) Enzymes of importance to rhizosphere processes. J Soil Sci Plant Nutr 15(2):283–306Google Scholar
  25. Golonka AM, Vilgalys R (2013) Nectar inhabiting yeasts in Virginian populations of Silene latifolia (Caryophyllaceae) and coflowering species. Am Midl Nat 169:235–258CrossRefGoogle Scholar
  26. Hacquard S, Spaepen S, Garrido-Oter R, Schulze-Lefert P (2017) Interplay between innate immunity and the plant microbiota. Annu Rev Phytopathol 55:565–589PubMedCrossRefGoogle Scholar
  27. Herrera CM, de Vega C, Canto A, Pozo MI (2009) Yeasts in floral nectar: a quantitative survey. Ann Bot 103(9):1415–1423PubMedPubMedCentralCrossRefGoogle Scholar
  28. Heuer H, Smalla K (2012) Plasmids foster diversification and adaptation of bacterial populations in soil. FEMS Microbiol Rev 36(6):1083–1104PubMedCrossRefGoogle Scholar
  29. Heydenreich B, Bellinghausen I, König B, Becker WM, Grabbe S, Petersen A, Saloga J (2012) Gram-positive bacteria on grass pollen exhibit adjuvant activity inducing inflammatory T cell responses. Clin Exp Allergy 42(1):76–84PubMedCrossRefGoogle Scholar
  30. Huisman R, Bouwmeester K, Brattinga M, Govers F, Bisseling T, Limpens E (2015) Haustorium formation in Medicago truncatula roots infected by Phytophthora palmivora does not involve the common endosymbiotic program shared by arbuscular mycorrhizal fungi and rhizobia. Mol Plant-Microbe Interact 28(12):1271–1280PubMedCrossRefGoogle Scholar
  31. Jacquemyn H, Lenaerts M, Brys R, Willems K, Honnay O, Lievens B (2013) Among-population variation in microbial community structure in the floral nectar of the bee-pollinated forest herb Pulmonaria officinalis L. PLoS One 8(3):e56917PubMedPubMedCentralCrossRefGoogle Scholar
  32. Junker RR, Tholl D (2013) Volatile organic compound mediated interactions at the plant-microbe interface. J Chem Ecol 39(7):810–825PubMedCrossRefGoogle Scholar
  33. 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(6):918–924PubMedCrossRefGoogle Scholar
  34. Kaneko T, Minamisawa K, Isawa T, Nakatsukasa HIROKI, Mitsui H, Kawaharada YASU, Shimizu Y (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17(1):37–50PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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. Proc Natl Acad Sci U S A 111(38):13715–13720PubMedPubMedCentralCrossRefGoogle Scholar
  36. Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49(5):840–854PubMedCrossRefGoogle Scholar
  37. Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6(7):1378PubMedCrossRefGoogle Scholar
  38. Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72(1):1CrossRefGoogle Scholar
  39. Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Divers 17:69–90Google Scholar
  40. Lemanceau P, Barret M, Mazurier S, Mondy S, Pivato B, Fort T, Vacher C (2017) Plant communication with associated microbiota in the spermosphere, rhizosphere and phyllosphere. In: Advances in botanical research, vol 82. Academic, Cambridge, MA, pp 101–133Google Scholar
  41. Lenaerts M, Álvarez-Pérez S, De Vega C, Van Assche A, Johnson SD, Willems KA, Lievens B (2014) Rosenbergiella australoborealis sp. nov., Rosenbergiella collisarenosi sp. nov. and Rosenbergiella epipactidis sp. nov., three novel bacterial species isolated from floral nectar. Syst Appl Microbiol 37(6):402–411PubMedCrossRefGoogle Scholar
  42. Maignien L, DeForce EA, Chafee ME, Eren AM, Simmons SL (2014) Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. MBio 5(1):e00682–e00613PubMedPubMedCentralCrossRefGoogle Scholar
  43. Maruthachalam K, Klosterman SJ, Anchieta A, Mou B, Subbarao KV (2013) Colonization of spinach by Verticillium dahliae and effects of pathogen localization on the efficacy of seed treatments. Phytopathology 103(3):268–280PubMedCrossRefGoogle Scholar
  44. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9(3):274–280PubMedCrossRefGoogle Scholar
  45. Menzler-Hokkanen I, Hokkanen HM (2017) Entomovectoring: an agroecological practice of using bees for biocontrol. Agroecol Pract Sustain Agric Princ Appl Mak Transit. CrossRefGoogle Scholar
  46. Mittelbach M, Yurkov AM, Nocentini D, Nepi M, Weigend M, Begerow D (2015) Nectar sugars and bird visitation define a floral niche for basidiomycetous yeast on the Canary Islands. BMC Ecol 15(1):2PubMedPubMedCentralCrossRefGoogle Scholar
  47. Mommer L, Hinsinger P, Prigent-Combaret C, Visser EJ (2016) Advances in the rhizosphere: stretching the interface of life. Plant Soil 407(1–2):1–8. CrossRefGoogle Scholar
  48. Mwajita MR, Murage H, Tani A, Kahangi EM (2013) Evaluation of rhizosphere, rhizoplane and phyllosphere bacteria and fungi isolated from rice in Kenya for plant growth promoters. SpringerPlus 2(1):606PubMedPubMedCentralCrossRefGoogle Scholar
  49. Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309PubMedCrossRefGoogle Scholar
  50. Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139PubMedPubMedCentralCrossRefGoogle Scholar
  51. Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C (2015) Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small-secreted proteins. Front Microbiol 6:1278PubMedPubMedCentralCrossRefGoogle Scholar
  52. Pozo MI, Lachance MA, Herrera CM (2012) Nectar yeasts of two southern Spanish plants: the roles of immigration and physiological traits in community assembly. FEMS Microbiol Ecol 80(2):281–293PubMedCrossRefGoogle Scholar
  53. Pozo MI, Herrera CM, Alonso C (2014) Spatial and temporal distribution patterns of nectar-inhabiting yeasts: how different floral microenvironments arise in winter-blooming Helleborus foetidus. Fungal Ecol 11:173–180CrossRefGoogle Scholar
  54. Prasad R, Kumar M, Varma A (2015) Role of PGPR in soil fertility and plant health. In: Egamberdieva D, Shrivastava S, Varma A (eds) Plant growth-promoting rhizobacteria (PGPR) and medicinal plants. Springer International Publishing, Switzerland, pp 247–260CrossRefGoogle Scholar
  55. Reisberg EE, Hildebrandt U, Riederer M, Hentschel U (2012) Phyllosphere bacterial communities of trichome-bearing and trichomeless Arabidopsis thaliana leaves. Antonie Van Leeuwenhoek 101(3):551–560PubMedCrossRefGoogle Scholar
  56. Remus-Emsermann MN, Schlechter RO (2018) Phyllosphere microbiology: at the interface between microbial individuals and the plant host. New Phytologist 218(4):1327–1333PubMedCrossRefGoogle Scholar
  57. Rering CC, Beck JJ, Hall GW, McCartney MM, Vannette RL (2017) Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytol 220(3):750–759PubMedCrossRefGoogle Scholar
  58. Rodríguez MA, Venedikian N, Godeas A (2001) Fungal populations on sunflower (Helianthus annuus) anthosphere and their relation to susceptibility or tolerance to Sclerotinia sclerotiorum attack. Mycopathologia 150(3):143PubMedCrossRefGoogle Scholar
  59. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340PubMedCrossRefGoogle Scholar
  60. Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Int J Life Sci Med Res 21(1):30Google Scholar
  61. 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(6):e99107PubMedPubMedCentralCrossRefGoogle Scholar
  62. Santoyo G, Pacheco CH, Salmerón JH, León RH (2017) The role of abiotic factors modulating the plant-microbe-soil interactions: toward sustainable agriculture. A review. Span J Agric Res 15(1):13CrossRefGoogle Scholar
  63. Schaeffer RN, Irwin RE (2014) Yeasts in nectar enhance male fitness in a montane perennial herb. Ecology 95(7):1792–1798PubMedCrossRefGoogle Scholar
  64. Schiltz S, Gaillard I, Pawlicki-Jullian N, Thiombiano B, Mesnard F, Gontier E (2015) A review: what is the spermosphere and how can it be studied? J Appl Microbiol 119(6):1467–1481PubMedCrossRefGoogle Scholar
  65. Shade A, McManus PS, Handelsman J (2013) Unexpected diversity during community succession in the apple flower microbiome. MBio 4(2):e00602–e00612PubMedPubMedCentralCrossRefGoogle Scholar
  66. Shrivastava S, Prasad R, Varma A (2014) Anatomy of root from eyes of a microbiologist. In: Morte A, Varma A (eds) Root engineering, vol 40. Springer, Berlin, pp 3–22CrossRefGoogle Scholar
  67. Simon HM, Smith KP, Dodsworth JA, Guenthner B, Handelsman J, Goodman RM (2001) Influence of tomato genotype on growth of inoculated and indigenous bacteria in the spermosphere. Appl Environ Microbiol 67(2):514–520PubMedPubMedCentralCrossRefGoogle Scholar
  68. Singh D, Mathur SB (2004) Location of fungal hyphae in seeds. In: Histopathology of seed-borne infections. CRC Press, Boca Raton, FL, pp 101–168CrossRefGoogle Scholar
  69. Tian Y, Zhao Y, Wu X, Liu F, Hu B, Walcott RR (2015) The type VI protein secretion system contributes to biofilm formation and seed-to-seedling transmission of Acidovorax citrulli on melon. Mol Plant Pathol 16(1):38–47PubMedCrossRefGoogle Scholar
  70. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7(1):40–50CrossRefGoogle Scholar
  71. Ushio M, Yamasaki E, Takasu H, Nagano AJ, Fujinaga S, Honjo MN, Kudoh H (2015) Microbial communities on flower surfaces act as signatures of pollinator visitation. Sci Rep 5:8695PubMedPubMedCentralCrossRefGoogle Scholar
  72. Vannette RL, Gauthier MPL, Fukami T (2013) Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism. Proc R Soc Lond B Biol Sci 280(1752):20122601CrossRefGoogle Scholar
  73. Vega Y, Marques I (2015) Both biotic and abiotic factors influence floral longevity in three species of Epidendrum (Orchidaceae). Plant Species Biol 30(3):184–192CrossRefGoogle Scholar
  74. Violante A, Caporale AG (2015) Biogeochemical processes at soil-root interface. J Soil Sci Plant Nutr 15(2):422–448Google Scholar
  75. Whipps J, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105(6):1744–1755PubMedCrossRefGoogle Scholar
  76. Wiens F, Zitzmann A, Lachance MA, Yegles M, Pragst F, Wurst FM, Spanagel R (2008) Chronic intake of fermented floral nectar by wild treeshrews. Proc Natl Acad Sci U S A 105(30):10426–10431PubMedPubMedCentralCrossRefGoogle Scholar
  77. Williams TR, Marco ML (2014) Phyllosphere microbiota composition and microbial community transplantation on lettuce plants grown indoors. MBio 5(4):e01564–e01514PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Nagarathinam Arunkumar
    • 1
  • Suchitra Rakesh
    • 1
  • Kaushik Rajaram
    • 1
  • Narayanasamy Ravi Kumar
    • 1
  • Siva Sundara Kumar Durairajan
    • 1
    Email author
  1. 1.Department of Microbiology, School of Basic and Applied SciencesCentral University of Tamil NaduThiruvarurIndia

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