Bacterial seed endophytes: Genera, vertical transmission and interaction with plants

Environmental Microbiology Reports

Volumn 7, Issue 1, 2015, Pages 40-50

  Truyens, Sascha ^a   Weyens, Nele ^a   Cuypers, Ann ^a   Vangronsveld, Jaco ^a  

^a HASSELT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 84923359886     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12181     Document Type: Review

References (92)

1. Adams, P.D., and Kloepper, J.W. (2002) Effect of host genotype on indigenous bacterial endophytes of cotton (Gossypium hirsutum L). Plant Soil 240: 181-189.
2. Agarwal, V.K., and Sinclair, J.B. (1996) Principles of Seed Pathology. Boca Raton, FL, USA: Lewis Publication.
3. Ali, S., Duan, J., Charles, T.C., and Glick, B.R. (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343: 193-198.
4. Azevedo, J.L., and Araújo, W.L. (2007) Diversity and applications of endophytic fungi isolated from tropical plants. In Fungi: Multifaceted Microbes. Ganguli, B.N., and Deshmukh, S.K. (eds). Boca Raton, FL, USA: CRC Press, pp. 189-207.
5. Bacilio-Jiménez, M., Aguilar-Flores, S., del Valle, M.V., Pérez, A., Zepeda, A., and Zenteno, E. (2001) Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol Biochem 33: 167-172.
6. Bacilio-Jiménez, M., Aguilar-Flores, S., Ventura-Zapata, E., Pérez-Campos, E., Bouqelet, S., and Zenteno, E. (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249: 271-277.
7. Bacon, C.W., and Hinton, D.M. (1996) Isolation and culture of endophytic bacteria and fungi. In Manual of Environmental Microbiology. Hurst, C.J., Knudsen, G.R., McInerney, M.J., Stetzenbach, C., and Walter, M.V. (eds). Washington, DC, USA: ASM Press, pp. 413-421.
8. Baker, K.F., and Cook, R.J. (1974) Biological Control of Plant Pathogens. San Francisco, CA, USA: WH Freeman.
9. Berg, G., Krechel, A., Ditz, M., Sikora, R.A., Ulrich, A., and Hallmann, J. (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51: 215-229.
10. Camacho Carvajal, M.M. (2001) Molecular characterization of the roles of type 4 pili, NDH-I and PyrR in rhizosphere colonization of Pseudomonas fluorescens WCS365. PhD thesis, University Leiden, Leiden, The Netherlands.
11. Cankar, K., Kraigher, H., Ravnikar, M., and Rupnik, M. (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244: 341-345.
12. Cavalcante, J.J., Vargas, C., Noqueira, E.M., Vinagre, F., Schwarcz, K., Baldani, J.I., etal. (2007) Members of the ethylene signaling pathway are regulated in sugarcane during the association with nitrogen-fixing endophytic bacteria. J Exp Bot 58: 673-686.
13. Chee-Sanford, J.C., Williams, M.M., Davis, A.S., and Sims, G.K. (2006) Do microorganisms influence seed-bank dynamics? Weed Sci 54: 575-587.
14. Compant, S., Reiter, B., Sessitsch, A., Nowak, J., Clément, C., and Barka, E. (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71: 1685-1693.
15. Compant, S., Clément, C., and Sessitsch, A. (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42: 669-678.
16. Compant, S., Mitter, B., Coli-Mull, J.G., Gangl, H., and Sessitsch, A. (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microbial Ecol 62: 188-197.
17. Coombs, J.T., and Franco, C.M.M. (2003) Isolation and identification of Actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69: 5603-5608.
18. Cottyn, B., Regalado, E., Lanoot, B., De Cleene, M., Mew, T.W., and Swings, J. (2001) Bacterial populations associated with rice seed in the tropical environment. Phytopathol 91: 282-292.
19. Croes, S., Weyens, N., Janssen, J., Vercampt, H., Colpaert, J.V., Carleer, R., and Vangronsveld, J. (2013) Bacterial communities associated with Brassica napus L. grown on trace element-contaminated and non-contaminated fields: a genotypic and phenotypic comparison. Microb Biotechnol 6: 371-384.
20. Dent, K.C., Stephen, J.R., and Finch-Savage, W.E. (2004) Molecular profiling of microbial communities associated with seeds of Beta vulgaris subsp. Vulgaris (sugar beet). J Microbiol Methods 56: 17-26.
21. Dong, Z.M., Canny, M.J., McCully, M.E., Roboredo, M.R., Cabadilla, C.F., Ortega, E., and Rodes, R. (1994) A nitrogen-fixing endophyte of sugarcane stems. A new role for the apoplast. Plant Physiol 105: 1139-1147.
22. Donnarumma, F., Capuana, M., Vettori, C., Petrini, G., Giannini, R., Indorato, C., and Mastromei, G. (2010) Isolation and characterisation of bacterial colonies from seeds and in vitro cultures of Fraxinus spp. from Italian sites. Plant Biol 13: 169-176.
23. Dunleavy, J.M. (1989) Curtobacterium plantarum sp. nov. is ubiquitous in plant leaves and is seed transmitted in soybean and corn. Int J Syst Bacteriol 39: 240-249.
24. Ebeltagy, A., Nishioka, K., Suzuki, H., Sato, T., Sato, Y., Morisaki, H., etal. (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46: 617-629.
25. Espinosa-Urgel, M., Salido, A., and Ramos, J. (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182: 2363-2369.
26. Ewald, P.W. (1989) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503: 295-306.
27. Ferreira, A., Quecine, M., Lacava, P., Oda, S., Azevedo, J., and Araújo, W. (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287: 8-14.
28. Fürnkranz, M., Lukesch, B., Müller, H., Huss, H., Grube, M., and Berg, G. (2012) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb Ecol 63: 418-428.
29. Gagne-Bourgue, F., Aliferis, K.A., Seguin, P., Rani, M., Samson, R., and Jabaji, S. (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol 114: 836-853.
30. Granér, G., Persson, P., Meijer, J., and Alström, S. (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224: 269-276.
31. Hallmann, J., Quadt-Hallmann, A., Mahaffee, W.F., and Kloepper, J.W. (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43: 895-914.
32. Hardoim, P.R., Hardoim, C.C.P., van Overbeek, L.S., and van Elsas, J.D. (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7: e30438.
33. Hill, N.S., and Roach, P.K. (2009) Endophyte survival during seed storage: endophyte-host interactions and heritability. Crop Sci 49: 1425-1430.
34. Hill, N.S., Bouton, J.H., Hiatt, E.E., and Kittle, B. (2005) Seed maturity, germination, and endophyte relationships in tall fescue. Crop Sci 45: 859-863.
35. Holland, M.A., and Polacco, J.C. (1994) PPFMs and other covert contaminants: is there more to plants physiology than just plants. Annu Rev Plant Physiol Plant Mol Biol 45: 197-209.
36. Hood, M.A., van Dijk, K.V., and Nelson, E.B. (1998) Factors affecting attachment of Enterobacter cloacae to germinating cotton seed. Microb Ecol 36: 101-110.
37. Hurek, T., Reinhold-Hurek, B., Van Montagu, M., and Kellenberger, E. (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J Bacteriol 176: 1913-1923.
38. Ikeda, S., Fuji, S., Sato, T., Ytow, N., Ezura, H., Minamisawa, K., and Fujimura, T. (2006) Community analysis of seed-associated microbes in forage crops using culture-independent methods. Microbes Environ 21: 112-121.
39. Ivanoff, S.S. (1933) Stewart's wilt disease of corn, with emphasis on the life history of Phytomonas stewartii in relation to pathogenesis. J Agr Res 47: 749-770.
40. James, E.K., Gyaneshwar, P., Manthan, N., Barraquio, W.L., Reddy, P.M., Ianetta, P.P.M., etal. (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 15: 894-906.
41. Johnston-Monje, D., and Raizada, M.N. (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6: e20396.
42. Kaga, H., Mano, H., Tanaka, F., Watanabe, A., Kaneko, S., and Morisaki, H. (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24: 154-162.
43. Klironomos, J.N. (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70.
44. Kremer, R.J. (1987) Identity and properties of bacteria inhabiting seeds of selected broadleaf weed species. Microbial Ecol 14: 29-37.
45. Kukkurainen, S., Leino, A., Vähämiko, S., Kärkkäinen, H.R., Ahanen, K., and Sorvari, S. (2005) Occurence and location of endophytic bacteria in garden and wild strawberry. Hortscience 40: 348-352.
46. Liu, Y., Zuo, S., Xu, L., Zou, Y., and Song, W. (2012) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194: 1001-1012.
47. Liu, Y., Zuo, S., Zou, Y., Wang, J., and Song, W. (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Ann Microbiol 63: 71-79.
48. López-López, A., Rogel, M.A., Ormeño-Orillo, E., Martínez-Romero, J., and Martínez-Romero, E. (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33: 322-327.
49. Loper, J., and Henkels, M.D. (1999) Utilization of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere. Appl Environ Microbiol 65: 5357-5363.
50. Lopez-Velasco, G., Carder, P.A., Welbaum, G.E., and Ponder, M.A. (2013) Diversity of the spinach (Spinacia oleracea) spermosphere and phyllosphere bacterial communities. FEMS Microbiol Lett 346: 146-154.
51. Madmony, A., Chernin, L., Pleban, S., Peleg, E., and Riov, J. (2005) Enterobacter cloacae, an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbiol 50: 209-216.
52. Mahaffee, W.F., and Kloepper, J.W. (1997) Bacterial communities of the rhizosphere and endorhiza associated with field-grown cucumber plants inoculated with a plant growth-promoting rhizobacterium or its genetically modified derivative. Can J Microbiol 43: 344-353.
53. Malfanova, N., Lugtenberg, B.J.J., and Berg, G. (2013) Bacterial endophytes: who and where, and what are they doing there? In Molecular Microbial Ecology of the Rhizosphere. de Bruijn, F.J. (ed.). Hoboken, NJ, USA: Wiley-Blackwell, pp. 391-403.
54. Mano, H., Tanaka, F., Watanabe, A., Kaga, H., Okunishi, S., and Morisaki, H. (2006) Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 2: 86-100.
55. Mastretta, C. (2007) The potential role of plant-associated bacteria in metal uptake and metal translocation in Nicotiana tabacum. PhD Thesis, Hasselt University, Diepenbeek, Belgium.
56. Mastretta, C., Taghavi, S., van der Lelie, D., Mengoni, A., Galardi, F., Gonnelli, C., etal. (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11: 251-267.
57. Mathesius, U., Mulders, S., Goa, M., Teplitski, M., Caetano-Anollés, G., Rolfe, B.G., and Bauer, W.D. (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100: 1444-1449.
58. Molina, M.A., Godoy, P., Ramos-González, M.I., Muñoz, N., Ramos, J., and Espinosa-Urgel, M. (2005) Role of iron and the TonB system in colonization of corn seeds and roots by Pseudomonas putida KT2440. Environ Microbiol 7: 443-449.
59. Molina, M.A., Ramos, J., and Espinosa-Urgel, M. (2006) A two-partner secretion system is involved in seed and root colonization and iron uptake by Pseudomonas putida KT2440. Environ Microbiol 8: 639-647.
60. Mukhopadhyay, K., Garrison, N.K., Hinton, D.M., Bacon, C.W., Khush, G.S., Peck, H.D., and Data, N. (1996) Identification and characterization of bacterial endophytes of rice. Mycopathologia 134: 151-159.
61. Mundt, J.O., and Hinkle, N.F. (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32: 694-698.
62. Nelson, E.B. (2004) Microbial dynamics and interactions in the spermosphere. Ann Rev Phytopathol 42: 271-309.
63. Oehrle, N.W., Karr, D.B., Kremer, R.J., and Emerich, D.W. (2000) Enhanced attachment of Bradyrhizobium japonicum to soybean through reduced root colonization of internally seedborne microorganisms. Can J Microbiol 46: 600-606.
64. Okunishi, S., Sako, K., Mano, H., Imamura, A., and Morisaki, H. (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environ 20: 168-177.
65. Perez-Ramirez, N.O., Rogel, M.A., Wang, E., Castellanos, J.Z., and Martínez-Romero, E. (1998) Seeds of Phaseolus vulgarisbean carry Rhizobium etli. FEMS Microbiol Ecol 26: 289-296.
66. Perry, D.A. (1978) Report of the vigour test committee 1974-1977. Seed Sci Technol 6: 159-181.
67. Pirttilä, A.M., Laukkanen, H., Pospiech, H., Myllyla, R., and Hohtola, A. (2000) Detection of intracellular bacteria in the buds of Scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66: 3073-3077.
68. Pleban, S., Ingel, F., and Chet, I. (1995) Control of Rhizoctonia solani and Sclerotium rolfsii in the green house using endophytic Bacillus sp. Eur J Plant Pathol 101: 665-672.
69. Puente, M.E., Li, C.Y., and Bashan, Y. (2009a) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66: 402-408.
70. Puente, M.E., Li, C.Y., and Bashan, Y. (2009b) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66: 389-401.
71. Rand, F.V., and Cash, L.C. (1933) Bacterial wilt of corn. USDA Technical Bulletins 362: 1-22.
72. Rijavec, T., Lapanje, A., Dermastia, M., and Rupnik, M. (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 3: 802-808.
73. Ringelberg, D., Foley, K., and Reynolds, C.M. (2012) Bacterial endophyte communities of two wheatgrass varieties following propagation in different growing media. Can J Microbiol 58: 67-80.
74. Roberts, D.P., Dery, D.P., Yucel, I., Buyer, J., Holtman, M.A., and Kobayashi, D.Y. (1999) Role of pfkA and general carbohydrate catabolism in seed colonization by Enterobacter cloacae. Appl Environ Microbiol 65: 2513-2519.
75. Roberts, D.P., Baker, C.J., McKenna, L., Liu, S., Buyer, J.S., and Kobayashi, D.Y. (2009) Influence of host seed on metabolic activity of Enterobacter cloacae in the spermosphere. Soil Biol Biochem 41: 754-761.
76. Rosenblueth, M., and Martínez-Romero, E. (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19: 827-837.
77. Rosenblueth, M., López-López, A., Martínez, J., Rogel, M.A., Toledo, I., and Martínez-Romero, I. (2010) Seed bacterial endophytes: common genera, seed-to-seed variability and their possible role in plants. Acta Hort 938: 39-48.
78. Rudgers, J.A., Afkhami, M.E., Rúa, M.A., Davitt, A.J., Hammer, S., and Huguet, V.M. (2009) A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology 90: 1531-1539.
79. Ruiz, D., Agaras, B., Werra, P., Wall, L.G., and Valverde, C. (2011) Characterization and screening of plant probiotic traits of bacteria isolated from rice seeds cultivated in Argentina. J Microbiol 49: 902-912.
80. Samish, Z., and Etinger-Tulczynska, R. (1963) Distribution of bacteria within the tissue of healthy tomatoes. Appl Microbiol 11: 7-10.
81. Schenck, S., and Stotzky, G. (1975) Effect on microorganisms of volatile compounds released from germinating seeds. Can J Microbiol 21: 1622-1634.
82. Sessitsch, A., Hardoim, P., Döring, J., Weilharter, A., Krause, A., Woyke, T., etal. (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25: 28-36.
83. Smerda, J.S., Sedláček, I., Páčová, Z., Durnová, E., Smišková, A., and Havel, L. (2005) Paenibacillus mendelii sp. nov., from surface-sterilized seeds of Pisum sativum L. Int J Syst Evol Microbiol 55: 2351-2354.
84. Sobolev, C.S., Orner, V.A., and Arias, R.S. (2013) Distribution of bacterial endophytes in peanut seeds obtained from axenic and control plant material under field conditions. Plant Soil 371: 367-376.
85. Tripathi, A., Verma, S., Chowdhury, S., Lebuhn, M., Gattinger, A., and Schloter, M. (2006) Ochrobactrum oryzae sp. nov., an endophytic bacterial species isolated from deep-water rice in India. Int J Syst Evol Microbiol 56: 1677-1680.
86. Truyens, S., Weyens, N., Cuypers, A., and Vangronsveld, J. (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol 15: 971-981.
87. Truyens, S., Jambon, I., Croes, S., Janssen, J., Weyens, N., Mench, M., etal. (2014) The effect of long-term Cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int J Phytoremediation 16: 643-659.
88. Vega, F., Pava-Ripoll, M., Posada, F., and Buyer, J. (2005) Endophytic bacteria in Coffea arabica L. J Basic Microbiol 45: 371-380.
89. 2-fixing endophytic bacteria association. J Exp Bot 57: 559-569.
90. de Weert, S., Vermeiren, H., Mulders, I.H.M., Kuiper, I., Hendrickx, N., Bloemberg, G.V., etal. (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15: 1173-1180.
91. Weyens, N., van der Lelie, D., Taghavi, S., and Vangronsveld, J. (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20: 248-254.
92. Xu, M., Sheng, J., Chen, L., Men, Y., Gan, L., Guo, S., and Shen, L. (2014) Bacterial community compositions of tomato (Lycopersicum esculentum Mill.) seeds and plant growth promoting activity of ACC deaminase producing Bacillus subtilis (HYT-12-1) on tomato seedlings. World J Microbiol Biotechnol 30: 835-845.