Bacterial populations in juvenile maize rhizospheres originate from both seed and soil

Plant and Soil

Volumn 405, Issue 1-2, 2016, Pages 337-355

  Johnston Monje, David ^a,b   Lundberg, Derek S ^c   Lazarovits, George ^d   Reis, Veronica M ^e   Raizada, Manish N ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b Symbiota   (United States)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^d Agroecology Research Services Centre   (Canada)

^e EMBRAPA AGROBIOLOGIA   (Brazil)

Author keywords

16S; Bacteria; Colonization; Endophyte; Endosphere; Epiphyte; Inoculation; Maize; Microbial ecology; Microbiome; Miseq; Next generation sequencing; Phyllosphere; Rhizoplane; Rhizosphere; Root; Seed; Soil; Spermosphere; Terra preta; TRFLP; Vertical transmission; Zea mays

Indexed keywords

COLONIZATION; ENDOPHYTE; EPIPHYTE; GENOTYPE; INOCULATION; JUVENILE; MAIZE; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; PHYLLOSPHERE; POPULATION STRUCTURE; RHIZOBACTERIUM; RHIZOSPHERE; SEED; SOIL MICROORGANISM; VERTICAL TRANSMISSION;

AMAZONIA;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); BACTEROIDETES; FIRMICUTES; OTUS; PROTEOBACTERIA; ZEA MAYS;

EID: 84962235274     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-016-2826-0     Document Type: Article

References (72)

1. Adams PD, Kloepper JW (2002) Effect of host genotype on indigenous bacterial endophytes of cotton (Gossypium hirsutum L.). Plant and Soil 240:181–189
2. Ait Barka E, Gognies S, Nowak J, Audran JC, Belarbi A (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Control 24:135–142
3. Alves GC, Rodrigues dos Santos CL, Urquiaga S, Reis VM (2010) Milho inoculado com a estirpe BR 11417 em experimentos de campo nas safras e safrinhas de 3 anos consecutivos. In Agronomia/Ciência do Solo. UFRRJ, Seropedica
4. Bacilio-Jimenez M, Aguilar-Flores S, del Valle MV, Perez A, Zepeda A, Zenteno E (2001) Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol Biochem 33:167–172
5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
6. Bakker M, Chaparro J, Manter D, Vivanco J (2015) Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays. Plant Soil 1–12
7. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
8. Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, Knight R, Fierer N. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455
9. Block CC, Hill JH, McGee DC (1998) Seed transmission of Pantoea stewartii in field and sweet corn. Plant Dis 82:775–780
10. Bouffaud M-L, Kyselková M, Gouesnard B, Grundmann G, Muller D, Moënne-Loccoz Y (2012) Is diversification history of maize influencing selection of soil bacteria by roots? Mol Ecol 21:195–206
11. Bragina A, Cardinale M, Berg C, Berg G (2013) Vertical transmission explains the specific Burkholderia pattern in Sphagnum mosses at multi-geographic scale. Front Microbiol 4:394
12. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
13. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838
14. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
15. Castellanos T, Dohrmann AB, Imfeld G, Baumgarte S, Tebbe CC (2009) Search of environmental descriptors to explain the variability of the bacterial diversity from maize rhizospheres across a regional scale. Eur J Soil Biol 45:383–393
16. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 1;8(4):790–803
17. Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263
18. Cope-Selby NL (2013) Diversity and characterization of bacteral endophytes in the C4 energy crop Miscanthus (PhD thesis). Aberystwyth University, Aberystwyth
19. Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249
20. Culman SW, Gauch HG, Blackwood CB, Thies JE (2008) Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. J Microbiol Methods 75:55–63
21. Dalmastri C, Chiarini L, Cantale C, Bevivino A, Tabacchioni S (1999) Soil type and maize cultivar affect the genetic diversity of maize root–associated Burkholderia cepacia populations. Microb Ecol 38:273–284
22. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107:11971–11975
23. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920
24. Elliott GN, Chou J-H, Chen W-M, Bloemberg GV, Bontemps C, Martínez-Romero E, Velázquez E, Young JPW, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11:762–778
25. EMBRAPA (1997) Manual de métodos e análises de solo. Centro Nacional de Pesquisa de Solos, Rio de Janeiro
26. Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14
27. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364
28. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470
29. Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11:e1001631
30. Garbeva P, Van Elsas JD, Van Veen JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32
31. Germida J, Siciliano S (2001) Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fertil Soils 33:410–415
32. Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 19:1141–1152
33. Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438
34. Hawkes CV, DeAngelis KM, Firestone MK (2007) Root interactions with soil microbial communities and processes. In The rhizosphere: an ecological perspective. ZG Cardon, JL Whitbeck (eds.) pp 1–29. Elsevier Academic Press
35. Hong SH, Bunge J, Leslin C, Jeon S, Epstein S (2009) Polymerase chain reaction primers miss half of rRNA microbial diversity. ISME J 3:1365–1373
36. Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD, Subramanian S, Vetter MM, Vilhjálmsson BJ, Nordborg M, Gordon JI, Bergelson J (2014) Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat Commun 5
37. Inceoglu O, Salles JF, van Overbeek L, van Elsas JD (2010) Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl Environ Microbiol 76:3675–3684
38. Inceoglu O, Al-Soud WA, Salles JF, Semenov AV, van Elsas JD (2011) Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One 6:e23321
39. Johnston-Monje D, Raizada MN (2011a) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:20396–20396
40. Johnston-Monje D, Raizada MN (2011b) Plant and endophyte relationships: Nutrient management. In: Moo-Young M (ed) Comprehensive Biotechnology, 2nd edn. Elsevier, Oxford, pp 713–727
41. Johnston-Monje D, Mousa WK, Lazarovits G, Raizada MN (2014) Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol 14:233
42. Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24:154–162
43. Keister D, Cregan P, Lynch JM, Whipps JM (1991) Substrate flow in the rhizosphere. In The Rhizosphere and Plant Growth. Springer, Netherlands, pp 15–24
44. Liu Y, Zuo S, Xu L, Zou Y, Song W (2013a) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194:1001–1012
45. Liu Y, Zuo S, Zou Y, Wang J, Song W (2013b) 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
46. Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; Phytohormone manipulations do not result in common growth responses. PLoS One 3:e2702
47. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TGD, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
48. Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nat Meth 10:999–1002
49. Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, 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 21:86–100
50. Marris E (2006) Putting the carbon back: black is the new green. Nature 442:624–626
51. Micallef SA, Shiaris MP, Colón-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742
52. Mundt JO, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32:694–698
53. Normander B, Prosser JI (2000) Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl Environ Microbiol 66:4372–4377
54. Okon Y, Itzigsohn R (1995) The development of Azospirillum as a commercial inoculant for improving crop yields. Biotechnol Adv 13:415–424
55. Paterniani E, Goodman MM (1977) Races of maize in Brazil and adjacent areas. CIMMYT, Mexico City
56. Peiffer JA, Ley RE (2013) Exploring the maize rhizosphere microbiome in the field: A glimpse into a highly complex system. Commun Integr Biol 6:e25177
57. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci 110:6548–6553
58. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799
59. Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408
60. Raaijmakers JM, Weller DM (1998) Natural plant protection by 2,4-diacetylphloroglucinol-producing pseudomonas spp. in take-all decline soils. Mol Plant Microbe Interact 11:144–152
61. Raibaud P, Ducluzeau R, Dubos F, Hudault S, Bewa H, Muller MC (1980) Implantation of bacteria from the digestive tract of man and various animals into gnotobiotic mice. Am J Clin Nutr 33:2440–2447
62. Rijavec T, Lapanje A, Dermastia M, Rupnik M (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53:802–808
63. Romano-Keeler J, Weitkamp J-H (2014) Maternal influences on fetal microbial colonization and immune development. Pediatr Res 77:189–195
64. Singh BK, Munro S, Potts JM, Millard P (2007) Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Appl Soil Ecol 36:147–155
65. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol 15:971–981
66. van Overbeek L, van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296
67. Vandenkoornhuyse P, Mahé SP, Ineson P, Staddon P, Ostle N, Cliquet J-B, Francez A-J, Fitter AH, Young JPW (2007) Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci 104:16970–16975
68. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
69. Weinert N, Piceno Y, Ding G-C, Meincke R, Heuer H, Berg G, Schloter M, Andersen G, Smalla K (2011) PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa. pp. 497–506.
70. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755
71. White JF, Chen Q, Torres MS, Mattera R, Irizarry I, Tadych M, Bergen M (2015) Collaboration between grass seedlings and rhizobacteria to scavenge organic nitrogen in soils. AoB plants 7, plu093
72. Yourstone SM, Lundberg DS, Dangl JL, Jones CD (2014) MT-Toolbox: improved amplicon sequencing using molecule tags. BMC Bioinforma 15:284