Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Johnston Monje, David ^a,b   Mousa, Walaa K ^a,c   Lazarovits, George ^b   Raizada, Manish N ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b Agroecology Research Services Centre   (Canada)

^c MANSOURA UNIVERSITY   (Egypt)

Author keywords

16S; Bacteria; Breeding; Corn hybrid; Domestication; Endophyte; Evolution; Landrace; Maize; Maize hybrid; Microbial ecology; Mixteco; Parviglumis; Root; Seed; Shoot; Soil; Teosinte; TRFLP; Vertical transmission; Yield stability; Zea

Indexed keywords

BACTERIA (MICROORGANISMS); ZEA; ZEA MAYS;

RNA 16S; SOIL;

CHEMISTRY; DNA FINGERPRINTING; ENDOPHYTE; GENETICS; GENOTYPE; MAIZE; MICROBIAL CONSORTIUM; MICROBIOLOGY; PLANT SEED; PRINCIPAL COMPONENT ANALYSIS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SOIL;

DNA FINGERPRINTING; ENDOPHYTES; GENOTYPE; MICROBIAL CONSORTIA; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PRINCIPAL COMPONENT ANALYSIS; RNA, RIBOSOMAL, 16S; SEEDS; SOIL; SOIL MICROBIOLOGY; ZEA MAYS;

EID: 84909638499     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0233-3     Document Type: Article

References (82)

1. Johnston-Monje D, Raizada MN. Plant and Endophyte Relationships: Nutrient Management. Comprehensive Biotechnology 2011, 713-727. Elsevier, Oxford, Moo-Young M, 2, 10.1016/B978-0-08-088504-9.00264-6.
2. Rosenblueth M, Martinez-Romero E. Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 2006, 19(8):827-837. 10.1094/MPMI-19-0827.
3. McCully ME. Niches for bacterial endophytes in crop plants: a plant biologist's view. Australian J Plant Phys 2001, 28(9):983-990.
4. Hallmann J, Quadt A, Mahaffee WF, Kloepper JW. Bacterial endophytes in agricultural crops. Can J Microbiol 1997, 43(10):895-914. 10.1139/m97-131.
5. Van Overbeek L, Van Elsas JD. Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 2008, 64(2):283-296. 10.1111/j.1574-6941.2008.00469.x.
6. Rasche F, Velvis H, Zachow C, Berg G, Van Elsas JD, Sessitsch A. Impact of transgenic potatoes expressing anti-bacterial agents on bacterial endophytes is comparable with the effects of plant genotype, soil type and pathogen infection. J Appl Ecol 2006, 43(3):555-566. 10.1111/j.1365-2664.2006.01169.x.
7. Mahaffee WF, Kloepper JW. Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.). Microb Ecol 1997, 34(3):210-223. 10.1007/s002489900050.
8. Long HH, Sonntag DG, Schmidt DD, Baldwin IT. The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. New Phytol 2010, 185(2):554-567. 10.1111/j.1469-8137.2009.03079.x.
9. Lundberg D, Lebeis S, Paredes S, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio T, Edgar R, Eickhorst T, Ley R, Hugenholtz P, Tringe S, Dangl J. Defining the core Arabidopsis thaliana root microbiome. Nature 2012, 488(7409):86-90. 10.1038/nature11237.
10. Hallmann J, Berg G. Spectrum and Population Dynamics of Bacterial Root Endophytes. Microbial Root Endophytes 2006, 15-31. Springer, Heidelberg, Schulz BJE, Boyle CJC, Sieber TN, vol. 9, 10.1007/3-540-33526-9_2.
11. Brundrett MC. Coevolution of roots and mycorrhizas of land plants. New Phytol 2002, 154(2):275-304. 10.1046/j.1469-8137.2002.00397.x.
12. Slattery JF, Coventry DR, Slattery WJ. Rhizobial ecology as affected by the soil environment. Aust J Exp Agric 2001, 41(3):289-298. 10.1071/EA99159.
13. Dowling DN, Broughton WJ. Competition for nodulation of legumes. Annu Rev Microbiol 1986, 40(1):131-157. 10.1146/annurev.mi.40.100186.001023.
14. Ruiz Sainz J, Zhou J, Rodriguez-Navarro DN, Vinardell J, Thomas-Oates J. Soybean Cultivation and BNF in China. Nitrogen Fixation in Agriculture, Forestry, Ecology, and the Environment 2005, 67-87. Springer, Dordrecht, Warner D, Newton WE, 10.1007/1-4020-3544-6_5.
15. Pueppke SG. Nitrogen Fixation by Soybean in North America. Nitrogen Fixation in Agriculture, Forestry, Ecology, and the Environment 2005, 15-23. Springer, Dordrecht, Warner D, Newton WE, 10.1007/1-4020-3544-6_2.
16. Hartmann A, Rothballer M, Schmid M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil 2008, 312(1):7-14. 10.1007/s11104-007-9514-z.
17. Catroux G, Amarger N. Rhizobia as Soil Inoculants in Agriculture. Release of Genetically Engineered and Other Micro-Organisms 1992, 1-9. University of Cambridge, Cambridge, Fry JC, Day MJ, vol. 2.
18. Alves BJR, Boddey RM, Urquiaga S. The success of BNF in soybean in Brazil. Plant and Soil 2003, 252(1):1-9. 10.1023/A:1024191913296.
19. Adams PD, Kloepper JW. Effect of host genotype on indigenous bacterial endophytes of cotton (Gossypium hirsutum L.). Plant Soil 2002, 240(1):181. 10.1023/A:1015840224564.
20. Christensen MJ, Voisey CR. The Biology of The Endophyte/Grass Partnership. 6th International Symposium on Fungal Endophytes of Grasses 2007, 123-133. New Zealand Grassland Association, Christchurch, New Zealand, Papay AJ, Thorn ER, vol. 13, 6 edn.
21. Schardl CL, Leuchtmann A, Spiering MJ. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 2004, 55:315-340. 10.1146/annurev.arplant.55.031903.141735.
22. Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL. Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans . FEMS Microbiol Lett 2008, 287(1):8-14. 10.1111/j.1574-6968.2008.01258.x.
23. Puente ME, Li CY, Bashan Y. Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 2009, 66(3):402-408. 10.1016/j.envexpbot.2009.04.007.
24. Mundt JO, Hinkle NF. Bacteria within ovules and seeds. Appl Environ Microbiol 1976, 32(5):694-698.
25. Okunishi S, Sako K, Mano H, Imamura A, Morisaki H. Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microb Environ 2005, 20(3):168-177. 10.1264/jsme2.20.168.
26. Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, Morisaki H. Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microb Environ 2006, 21(2):86-100. 10.1264/jsme2.21.86.
27. Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H. Rice seeds as sources of endophytic bacteria. Microb Environ 2009, 24(2):154-162. 10.1264/jsme2.ME09113.
28. Cankar K, Kraigher H, Ravnikar M, Rupnik M. Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 2005, 244(2):341-345. 10.1016/j.femsle.2005.02.008.
29. Rijavec T, Lapanje A, Dermastia M, Rupnik M. Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 2007, 53(6):802-808. 10.1139/W07-048.
30. Daniel R. The metagenomics of soil. Nat Rev Microbiol 2005, 3(6):470-478. 10.1038/nrmicro1160.
31. Fulthorpe RR, Roesch LFW, Riva A, Triplett EW. Distantly sampled soils carry few species in common. Int Soc Microb Ecol J 2008, 2(9):901-910.
32. Warburton ML, Frisch JC, Bohn M, Bedoya M, Xia C, Crossa XC, Franco J, Hoisington J, Pixley D, Taba K. Genetic diversity in CIMMYT nontemperate maize germplasm: landraces, open pollinated varieties, and inbred lines. Crop Sci 2008, 48(2):617. 10.2135/cropsci2007.02.0103.
33. Wilkes G. Corn, strange and marvelous: but is a definitive origin known?. Corn: Origin, History, Technology, and Production 2004, John Wiley & Sons, New Jersey, Smith CW, Betran J, Runge ECA.
34. Wilkes G. Urgent notice to all maize researchers: disappearance and extinction of the last wild teosinte population is more than half completed. A modest proposal for teosinte evolution and conservation in situ: the Balsas, Guerrero, Mexico. Maydica 2007, 52(1):49.
35. Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J. A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci U S A 2002, 99(9):6080-6084. 10.1073/pnas.052125199.
36. Troyer AF. Persistent and popular germplasm in seventy centuries of corn evolution. Corn: Origin, History, Technology, and Production 2004, 133-231. John Wiley & Sons, Hoboken, Smith CW, Betran J, Runge ECA.
37. Tollenaar M, Lee EA. Yield potential, yield stability and stress tolerance in maize. Field Crop Res 2002, 75(2-3):161-169. 10.1016/S0378-4290(02)00024-2.
38. Frey KJ. National Plant Breeding Study-I 1996, Iowa State University, Ames.
39. Chelius MK, Triplett EW. The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 2001, 41(3):252-263.
40. Estrada P, Mavingui P, Cournoyer B, Fontaine F, Balandreau J, Caballero-Mellado J. A N2-fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico. Can J Microbiol 2002, 48(4):285-294. 10.1139/w02-023.
41. Johnston-Monje D, Raizada MN. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 2011, 6(6):20396. 10.1371/journal.pone.0020396.
42. Lambers H, Mougel C, Jaillard B, Hinsinger P. Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant and Soil 2009, 321(1):83-115. 10.1007/s11104-009-0042-x.
43. Nassar AH, El-Tarabily KA, Sivasithamparam K. Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fertil Soils 2005, 42(2):97-108. 10.1007/s00374-005-0008-y.
44. Glick BR. Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 2005, 251(1):1-7. 10.1016/j.femsle.2005.07.030.
45. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Pare PW, Kloepper JW. Bacterial volatiles promote growth in Arabidopsis . Proc Natl Acad Sci U S A 2003, 100(8):4927-4932. 10.1073/pnas.0730845100.
46. Ping L, Boland W. Signals from the underground: bacterial volatiles promote growth in Arabidopsis . Trends Plant Sci 2004, 9(6):263-266. 10.1016/j.tplants.2004.04.008.
47. Conn KL, Lazarovits G, Nowak J. A gnotobiotic bioassay for studying interactions between potatoes and plant growth-promoting rhizobacteria. Can J Microbiol 1997, 43(9):801-808. 10.1139/m97-117.
48. Berg G, Smalla K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 2009, 68(1):1-13. 10.1111/j.1574-6941.2009.00654.x.
49. Singh BK, Munro S, Potts JM, Millard P. Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Appl Soil Ecol 2007, 36(2-3):147-155. 10.1016/j.apsoil.2007.01.004.
50. Normander B, Prosser JI. Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl Environ Microbiol 2000, 66(10):4372-4377. 10.1128/AEM.66.10.4372-4377.2000.
51. Rosenblueth M, Martínez-Romero E. Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 2004, 181(5):337-344. 10.1007/s00203-004-0661-9.
52. Roesch LFW, Passaglia LMP, Bento FM, Triplett EW, Camargo FAO. Diversity of diazotrophic endophytic bacteria associated with maize plants. Rev Bras Ciência Solo 2007, 31:1367-1380. 10.1590/S0100-06832007000600015.
53. Cocking EC. Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant and Soil 2001, 252:169-175. 10.1023/A:1024106605806.
54. James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivares FL, Ladha JK. Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 2002, 15(9):894-906. 10.1094/MPMI.2002.15.9.894.
55. Dong Y, Iniguez AL, Triplett EW. Quantitative assessments of the host range and strain specificity of endophytic colonization by Klebsiella pneumoniae 342. Plant Soil 2003, 257(1):49-59. 10.1023/A:1026242814060.
56. Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C. Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 2008, 63(1):84-93. 10.1111/j.1574-6941.2007.00410.x.
57. Van Peer R, Punte HLM, De Weger LA, Schippers B. Characterization of root surface and endorhizosphere pseudomonads in relation to their colonization of roots. Appl Environ Microbiol 1990, 56(8):2462.
58. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 2001, 67(10):4742-4751. 10.1128/AEM.67.10.4742-4751.2001.
59. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 2010, 4(10):1340-1351. 10.1038/ismej.2010.58.
60. Mastretta C, Taghavi S, Van Der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J. Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 2009, 11(3):251-267. 10.1080/15226510802432678.
61. Ait Barka E, Gognies S, Nowak J, Audran JC, Belarbi A. Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Contr 2002, 24:135-142. 10.1016/S1049-9644(02)00034-8.
62. Raibaud P, Ducluzeau R, Dubos F, Hudault S, Bewa H, Muller MC. Implantation of bacteria from the digestive tract of man and various animals into gnotobiotic mice. Am J Clin Nutr 1980, 33(11):2440-2447.
63. Bacilio-Jimenez M, Aguilar-Flores S, del Valle MV, Perez A, Zepeda A, Zenteno E. Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense . Soil Biol Biochem 2001, 33:167-172. 10.1016/S0038-0717(00)00126-7.
64. Germida J, Siciliano S. Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fertil Soils 2001, 33(5):410-415. 10.1007/s003740100343.
65. Osborn AM, Moore ERB, Timmis KN. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2000, 2(1):39-50. 10.1046/j.1462-2920.2000.00081.x.
66. Lukow T, Dunfield PF, Liesack W. Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiol Ecol 2000, 32(3):241-247. 10.1111/j.1574-6941.2000.tb00717.x.
67. Schütte U, Abdo Z, Bent S, Shyu C, Williams C, Pierson J, Forney L. Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl Microbiol Biotechnol 2008, 80(3):365-380. 10.1007/s00253-008-1565-4.
68. Wang M, Ahrne S, Antonsson M, Molin G. T-RFLP combined with principal component analysis and 16S rRNA gene sequencing: an effective strategy for comparison of fecal microbiota in infants of different ages. J Microbiol Methods 2004, 59(1):53-69. 10.1016/j.mimet.2004.06.002.
69. Dickie IA, Xu B, Koide RT. Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 2002, 156(3):527-535. 10.1046/j.1469-8137.2002.00535.x.
70. Scala DJ, Kerkhof LJ. Horizontal heterogeneity of denitrifying bacterial communities in marine sediments by terminal restriction fragment length polymorphism analysis. Appl Environ Microbiol 2000, 66(5):1980-1986. 10.1128/AEM.66.5.1980-1986.2000.
71. Hong S, Bunge J, Leslin C, Jeon S, Epstein SS. Polymerase chain reaction primers miss half of rRNA microbial diversity. Int Soc Microb Ecol J 2009, 3(12):1365-1373.
72. Smalla K. Culture-Independent Microbiolgy. Microbial Biodiversity and Bioprospecting 2004, 88-99. ASM Press, Washington D.C, Bull A, 10.1128/9781555817770.ch9.
73. Culman SW, Gauch HG, Blackwood CB, Thies JE. Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. J Microbiol Methods 2008, 75(1):55-63. 10.1016/j.mimet.2008.04.011.
74. Kemp BM, Smith DG. Use of bleach to eliminate contaminating DNA from the surface of bones and teeth. Forensic Sci Int 2005, 154(1):53-61. 10.1016/j.forsciint.2004.11.017.
75. Bonne N, Clark P, Shearer P, Raidal S. Elimination of false-positive polymerase chain reaction results resulting from hole punch carryover contamination. J Vet Diagn Invest 2008, 20(1):60-63. 10.1177/104063870802000111.
76. Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, MacNeil IA, Minor C, Tiong CL, Gilman M, Osburne MS, Clardy J, Handelsman J, Goodman RM. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 2000, 66(6):2541-2547. 10.1128/AEM.66.6.2541-2547.2000.
77. Meyer-Aurich A, Janovicek K, Deen W, Weersink A. Impact of tillage and rotation on yield and economic performance in corn-based cropping systems. Agron J 2006, 98(5):1204-1212. 10.2134/agronj2005.0262.
78. Serratos JA, Willcox MC, Castillo F. Gene flow among maize landraces, impoved maize varieties, and teosinte: implications for transgenic maize. CIMMYT 1997, 1997:1997.
79. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 2008, 74(8):2461-2470. 10.1128/AEM.02272-07.
80. Junier P, Junier T, Witzel K-P. TRiFLe: a program for in silico T-RFLP analysis with user-defined sequences sets. Appl Environ Microbiol 2008, 74(20):6452-6456. 10.1128/AEM.01394-08.
81. Shyu C, Soule T, Bent SJ, Foster JA, Forney LJ. MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA genes. Microb Ecol 2007, 53(4):562-570. 10.1007/s00248-006-9106-0.
82. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410. 10.1016/S0022-2836(05)80360-2.