Role of root microbiota in plant productivity

Journal of Experimental Botany

Volumn 66, Issue 8, 2015, Pages 2167-2175

  Tkacz, Andrzej ^a   Poole, Philip ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Endophytes; metagenomics; microbiota; plant productivity; plantmicrobe interactions; rhizosphere

Indexed keywords

METAGENOMICS; MICROBIOLOGY; MICROFLORA; MYCORRHIZA; NODULATION; PHYSIOLOGY; PLANT DEVELOPMENT; PLANT ROOT;

METAGENOMICS; MICROBIOTA; MYCORRHIZAE; PLANT DEVELOPMENT; PLANT ROOT NODULATION; PLANT ROOTS;

EID: 84929657052     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv157     Document Type: Review

References (109)

1. Akiyama, K, Matsuzaki, K, Hayashi, H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827.
2. Alavi P, Starcher MR, Thallinger GG, Zachow C, Muller H, Berg G. 2014. Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria. BMC Genomics 15, 482.
3. Aslam Z, Yasir M, Yoon HS, Jeon CO, Chung YR. 2013. Diversity of the bacterial community in the rice rhizosphere managed under conventional and no-tillage practices. Journal of Microbiology 51, 747-756.
4. Augé RM. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3-42.
5. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM. 2013. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry 288, 4502-4512.
6. Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM. 2009. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiology 151, 2006-2017.
7. Bal HB, Das S, Dangar TK, Adhya TK. 2013. ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants. Journal of Basic Microbiology 53, 972-984.
8. Berbee ML, Taylor JW. 2007. Rhynie chert: a window into a lost world of complex plant-fungus interactions. New Phytologist 174, 475-479.
9. Berg G, Eberl L, Hartmann A. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environmental Microbiology 7, 1673-1685.
10. Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68, 1-13.
11. Bertalan M, Albano R, de Padua V, et al. 2009. Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics 10, 450.
12. Blanco Y, Blanch M, Pinon D, Legaz ME, Vicente C. 2005. Antagonism of Gluconacetobacter diazotrophicus (a sugarcane endosymbiont) against Xanthomonas albilineans (pathogen) studied in alginate-immobilized sugarcane stalk tissues. Journal of Bioscience and Bioengineering 99, 366-371.
13. Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G. 2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends in Plant Science 12, 224-230.
14. Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F. 2009. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytologist 184, 449-456.
15. Bulgarelli D, Rott M, Schlaeppi K, et al. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95.
16. Capoen W, Oldroyd G. 2008. How CYCLOPS keeps an eye on plant symbiosis. Proceedings of the National Academy of Sciences, USA 105, 20053-20054.
17. Caporaso JG, Lauber CL, Walters WA, et al. 2012. Ultra-highthroughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal 6, 1621-1624.
18. Cavalcante JJ, Vargas C, Nogueira EM, Vinagre F, Schwarcz K, Baldani JI, Ferreira PC, Hemerly AS. 2007. Members of the ethylene signalling pathway are regulated in sugarcane during the association with nitrogen-fixing endophytic bacteria. Journal of Experimental Botany 58, 673-686.
19. Chen C, Zhu H. 2013. Are common symbiosis genes required for endophytic rice-rhizobial interactions? Plant Signaling and Behavior 8, e25453.
20. Christiansen-Weniger C. 1996. Endophytic establishment of Azorhizobium caulinodans through auxin-induced root tumors of rice (Oryza sativa L.). Biology and Fertility of Soils 21, 293-302.
21. Conley DJ. 2012. Ecology: save the Baltic Sea. Nature 486, 463-464.
22. Crespo J, Boiardi J, Luna M. 2011. Mineral phosphate solubilization activity of Gluconacetobacter diazotrophicus under P-limitation and plant root environment. Agricultural Sciences 2, 16-22.
23. Crook MB, Mitra S, Ane JM, Sadowsky MJ, Gyaneshwar P. 2013. Complete genome sequence of the Sesbania symbiont and rice growth-promoting endophyte Rhizobium sp. strain IRBG74. Genome Announcements 1, e00934-13.
24. Cummings SP, Gyaneshwar P, Vinuesa P, et al. 2009. Nodulation of Sesbania species by Rhizobium (Agrobacterium) strain IRBG74 and other rhizobia. Environmental Microbiology 11, 2510-2525.
25. DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK. 2009. Selective progressive response of soil microbial community to wild oat roots. ISME Journal 3, 168-178.
26. Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt, M. 2014. Evolution of bacterial communities in the wheat crop rhizosphere. Environmental Microbiology (in press).
27. Doyle JJ. 2011. Phylogenetic perspectives on the origins of nodulation. Molecular Plant-Microbe Interactions 24, 1289-1295.
28. Ellis EC, Kaplan JO, Fuller DQ, Vavrus S, Klein Goldewijk K, Verburg PH. 2013. Used planet: a global history. Proceedings of the National Academy of Sciences, USA 110, 7978-7985.
29. Engelhard M, Hurek T, Reinhold-Hurek B. 2000. Preferential occurrence of diazotrophic endophytes, Azoarcus spp., in wild rice species and land races of Oryza sativa in comparison with modern races. Environmental Microbiology 2, 131-141.
30. Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J. 2014. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6.
31. Finlay RD. 2007. Modern soil microbiology . CRC Press, Taylor&Francis Group.
32. Fisher MM, Triplett EW. 1999. Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Applied Environmental Microbiology 65, 4630-4636.
33. Fouts DE, Tyler HL, DeBoy RT, et al. 2008. Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genetics 4, e1000141.
34. Fraser B. 2014. Deforestation: carving up the Amazon. Nature 509, 418-419.
35. Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE. 2013. Inside the root microbiome: bacterial root endophytes and plant growth promotion. American Journal of Botany 100, 1738-1750.
36. Galford GL, Soares-Filho B, Cerri CE. 2013. Prospects for landuse sustainability on the agricultural frontier of the Brazilian Amazon. Philosophical Transactions of the Royal Society B: Biological Sciences 368, 20120171.
37. Gao X, Lu X, Wu M, Zhang H, Pan R, Tian J, Li S, Liao H. 2012. Co-inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS One 7, e33977.
38. Gebhardt C, Turner GL, Gibson AH, Dreyfus BL, Bergersen FJ. 1984. Nitrogen-fixing growth in continuous culture of a strain of Rhizobium sp. isolated from stem nodules on Sesbania rostrata. Journal of General Microbiology 130, 843-848.
39. Glass ADM. 2003. Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Critical Reviews in Plant Sciences 22, 453-470.
40. Gobbato E, Marsh JF, Vernie T, et al. 2012. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Current Biology 22, 2236-2241.
41. Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C. 2010. Food security: the challenge of feeding 9 billion people. Science 327, 812-818.
42. Gutjahr C, Parniske M. 2013. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology 29, 593-617.
43. Gyaneshwar P, Hirsch AM, Moulin L, et al. 2011. Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Molecular Plant-Microbe Interactions 24, 1276-1288.
44. Hansen MC, Potapov PV, Moore R, et al. 2013. High-resolution global maps of 21st-century forest cover change. Science 342, 850-853.
45. Harrison MJ. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59, 19-42.
46. Harrison MJ, Dewbre GR, Liu J. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. The Plant Cell 14, 2413-2429.
47. Hartmann A, Fu H, Burris RH. 1986. Regulation of nitrogenase activity by ammonium chloride in Azospirillum spp. Journal of Bacteriology 165, 864-870.
48. Hartmann A, Rothballer M, Schmid M. 2008. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil 312, 7-14.
49. Hilton S, Bennett AJ, Keane G, Bending GD, Chandler D, Stobart R, Mills P. 2013. Impact of shortened crop rotation of oilseed rape on soil and rhizosphere microbial diversity in relation to yield decline. PLoS One 8, e59859.
50. Hurek T, Handley LL, Reinhold-Hurek B, Piche Y. 2002. Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Molecular Plant-Microbe Interactions 15, 233-242.
51. 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.
52. James TY, Kauff F, Schoch CL, et al. 2006. Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443, 818-822.
53. Jin CW, Ye YQ, Zheng SJ. 2014. An underground tale: contribution of microbial activity to plant iron acquisition via ecological processes. Annals of Botany 113, 7-18.
54. Jones CM, Thies JE. 2007. Soil microbial community analysis using twodimensional polyacrylamide gel electrophoresis of the bacterial ribosomal internal transcribed spacer regions. Journal of Microbiological Methods 69, 256-267.
55. Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova N, Lugtenberg B. 2006. Effects of the tomato pathogen Fusarium oxysporum f. sp. radicis-lycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Molecular Plant-Microbe Interactions 19, 1121-1126.
56. Krause A, Ramakumar A, Bartels D, et al. 2006. Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nature Biotechnology 24, 1385-1391.
57. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ. 2007. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist 174, 648-657.
58. Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencingbased assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied Environmental Microbiology 75, 5111-5120.
59. Lee KB, De Backer P, Aono T, et al. 2008. The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571. BMC Genomics 9, 271.
60. Lenton T. 2011. 2 degrees C or not 2 degrees C? That is the climate question. Nature 473, 7.
61. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63, 541-556.
62. Lundberg DS, Lebeis SL, Paredes SH, et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90.
63. Maillet F, Poinsot V, Andre O, et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-63.
64. Marie C, Broughton WJ, Deakin WJ. 2001. Rhizobium type III secretion systems: legume charmers or alarmers? Current Opinion in Plant Biology 4, 336-342.
65. Masalha J, Kosegarten H, Elmaci Ö, Mengel K. 2000. The central role of microbial activity for iron acquisition in maize and sunflower. Biology and Fertility of Soils 30, 433-439.
66. Masson-Boivin C, Giraud E, Perret X, Batut J. 2009. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends in Microbiology 17, 458-466.
67. Mehnaz S, Lazarovits G. 2006. Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microbial Ecology 51, 326-335.
68. Mendes R, Kruijt M, de Bruijn I, et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097-1100.
69. Micallef SA, Shiaris MP, Colon-Carmona A. 2009. Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. Journal of Experimental Botany 60, 1729-1742.
70. Mueller ND, Gerber JS, Johnston M, Ray DK, Ramankutty N, Foley JA. 2012. Closing yield gaps through nutrient and water management. Nature 490, 254-257.
71. Mutch LA, Young JP. 2004. Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Molecular Ecology 13, 2435-2444.
72. Okazaki S, Kaneko T, Sato S, Saeki K. 2013. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proceedings of the National Academy of Sciences, USA 110, 17131-17136.
73. Oldroyd GE. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology 11, 252-263.
74. Oldroyd GE, Harrison MJ, Udvardi M. 2005. Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiology 137, 1205-1210.
75. Oldroyd GE, Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Genetics 45, 119-144.
76. Osborne CA, Zwart AB, Broadhurst LM, Young AG, Richardson AE. 2011. The influence of sampling strategies and spatial variation on the detected soil bacterial communities under three different land-use types. FEMS Microbiology Ecology 78, 70-79.
77. Pedrosa FO, Monteiro RA, Wassem R, et al. 2011. Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genetics 7, e1002064.
78. 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. Proceedings of the National Academy of Sciences, USA 110, 6548-6553.
79. Pirozynski KA, Malloch DW. 1975. The origin of land plants: a matter of mycotrophism. Biosystems 6, 153-164.
80. Ray DK, Mueller ND, West PC, Foley JA. 2013. Yield trends are insufficient to double global crop production by 2050. PLoS One 8, e66428.
81. Rey T, Nars A, Bonhomme M, et al. 2013. NFP, a LysM protein controlling Nod factor perception, also intervenes in Medicago truncatula resistance to pathogens. New Phytologist 198, 875-886.
82. Robinson TP, Wint GR, Conchedda G, Van Boeckel TP, Ercoli V, Palamara E, Cinardi G, D'Aietti, L, Hay SI, Gilbert M. 2014. Mapping the global distribution of livestock. PLoS One 9, e96084.
83. Rockstrom J, Steffen W, Noone K, et al. 2009. A safe operating space for humanity. Nature 461, 472-475.
84. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones, A, Holton N, Malinovsky FG, Tor M, de Vries S, Zipfel C. 2011. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/ SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. The Plant Cell 23, 2440-2455.
85. Santi C, Bogusz D, Franche C. 2013. Biological nitrogen fixation in nonlegume plants. Annals of Botany 111, 743-767.
86. Sarkar A, Reinhold-Hurek B. 2014. Transcriptional profiling of nitrogen fixation and the role of NifA in the diazotrophic endophyte Azoarcus sp. strain BH72. PLoS One 9, e86527.
87. Schachtman DP, Reid RJ, Ayling SM. 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447-453.
88. Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze-Lefert P. 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proceedings of the National Academy of Sciences, USA 111, 585-592.
89. Schmer MR, Vogel KP, Varvel GE, Follett RF, Mitchell RB, Jin VL. 2014. Energy potential and greenhouse gas emissions from bioenergy cropping systems on marginally productive cropland. PLoS One 9, e89501.
90. Schmidt MA, Balsanelli E, Faoro H, et al. 2012. The type III secretion system is necessary for the development of a pathogenic and endophytic interaction between Herbaspirillum rubrisubalbicans and Poaceae. BMC Microbiology 12, 98.
91. Schreiter S, Ding GC, Heuer H, Neumann G, Sandmann M, Grosch R, Kropf S, Smalla K. 2014. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Frontiers in Microbiology 5, 144.
92. Sevilla M, Burris RH, Gunapala N, Kennedy C. 2001. Comparison of benefit to sugarcane plant growth and 15N2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and Nif-mutants strains. Molecular Plant-Microbe Interactions 14, 358-366.
93. Shi S, Richardson AE, O'Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK, Condron LM. 2011. Effects of selected root exudate components on soil bacterial communities. FEMS Microbiology Ecology 77, 600-610.
94. Shippers B, Bakker A, Baker P. 1987. Interactions of deletorious and beneficial microorganisms and the effect on cropicing practices. Annual Review of Phytopathology 25, 339-358.
95. Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133, 16-20.
96. Speidel JJ, Weiss DC, Ethelston SA, Gilbert SM. 2009. Population policies, programmes and the environment. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 3049-3065.
97. Suzuki S, Aono T, Lee KB, Suzuki T, Liu CT, Miwa H, Wakao S, Iki T, Oyaizu H. 2007. Rhizobial factors required for stem nodule maturation and maintenance in Sesbania rostrata-Azorhizobium caulinodans ORS571 symbiosis. Applied Environmental Microbiology 73, 6650-6659.
98. Swenson W, Wilson DS, Elias R. 2000. Artificial ecosystem selection. Proceedings of the National Academy of Sciences, USA 97, 9110-9114.
99. Tan Z, Hurek T, Vinuesa P, Muller P, Ladha JK, Reinhold-Hurek B. 2001. Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer-targeted PCR. Applied Environmental Microbiology 67, 3655-3664.
100. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. 2012. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Molecular Microbiology 86, 628-644.
101. Turner TR, James EK, Poole PS. 2013a. The plant microbiome. Genome Biology 14, 209.
102. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A, Grant A, Poole PS. 2013b. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME Journal 7, 2248-2258.
103. Udvardi M, Poole PS. 2013. Transport and metabolism in legume-rhizobia symbioses. Annual Review of Plant Biology 64, 781-805.
104. Vassilev N, Vassileva M, Nikolaeva I. 2006. Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Applied Microbiology and Biotechnology 71, 137-144.
105. Venkateshwaran M, Volkening JD, Sussman MR, Ané J-M. 2013. Symbiosis and the social network of higher plants. Current Opinion in Plant Biology 16, 118-127.
106. Vermeiren H, Willems A, Schoofs G, de Mot R, Keijers V, Hai W, Vanderleyden J. 1999. The rice inoculant strain Alcaligenes faecalis A15 is a nitrogen-fixing Pseudomonas stutzeri. Systematic and Applied Microbiology 22, 215-224.
107. Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GE. 2012. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology 22, 2242-2246.
108. Yan Y, Ping S, Peng J, et al. 2010. Global transcriptional analysis of nitrogen fixation and ammonium repression in root-associated Pseudomonas stutzeri A1501. BMC Genomics 11, 11.
109. Yan Y, Yang J, Dou Y, et al. 2008. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proceedings of the National Academy of Sciences, USA 105, 7564-7569.