Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Yang, Bo ^a,b   Wang, Xiao Mi ^a,b   Ma, Hai Yan ^a   Yang, Teng ^b   Jia, Yong ^a,b   Zhou, Jun ^a   Dai, Chuan Chao ^a,b  

^a NANJING NORMAL UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Ammonia oxidizing archaea (AOA); Ammonia oxidizing bacteria (AOB); Diazotroph; Fungal endophyte; Rhizosphere; Root exudate

Indexed keywords

AMINO ACID; AMMONIA; CARBOHYDRATE; CARBOXYLIC ACID; NITRATE;

ARTICLE; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA EXTRACTION; ECOSYSTEM; ENDOPHYTIC FUNGUS; FEEDBACK SYSTEM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MICROBIAL COMMUNITY; NITRIFICATION; NITROGEN FIXATION; NITROGEN TRANSFORMATION; NONHUMAN; PHOMOPSIS; PHOMOPSIS LIQUIDAMBARI; PLANT GROWTH; REAL TIME POLYMERASE CHAIN REACTION; RHIZOSPHERE; RICE; SEEDLING; SOIL ANALYSIS;

EID: 84946748262     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00982     Document Type: Article

References (86)

1. Alam, M. S., Ren, G. D., Lu, L., Zheng, Y., Peng, X. H., and Jia, Z. J. (2013). Conversion of upland to paddy field specifically alters the community structure of archaeal ammonia oxidizers in an acid soil. Biogeosciences 10, 5739-5753. doi: 10.5194/bg-10-5739-2013
2. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., and Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233-266. doi: 10.1146/annurev.arplant.57.032905.105159
3. Bardgett, R. D., Bowman, W. D., Kaufmann, R., and Schmidt, S. K. (2005). A temporal approach to linking aboveground and belowground ecology. Trends Ecol. Evol. 20, 634-641. doi: 10.1016/j.tree.2005.08.005
4. Bei, Q. C., Liu, G., Tang, H. Y., Cadisch, G., Rasche, F., and Xie, Z. B. (2013). Heterotrophic and phototrophic 15N2 fixation and distribution of fixed 15N in a flooded rice-soil system. Soil Biol. Biochem. 59, 25-31. doi: 10.1016/j.soilbio.2013.01.008
5. Boddey, R. M., and Dobereiner, J. (1995). Nitrogen fixation associated with grasses and cereals: recent progress and perspectives for the future. Nutr. Cycl. Agroecosyst. 42, 241-250.
6. Briones, A. M., Okabe, S., Umemiya, Y., Ramsing, N., Reichardt, W., and Okuyama, H. (2003). Ammonia-oxidizing bacteria on root biofilms and their possible contribution to N use efficiency of different rice cultivars. Plant Soil 250, 335-348. doi: 10.1023/A:1022897621223
7. Britto, D. T., and Kronzucker, H. J. (2004). Bioengineering nitrogen acquisition in rice: can novel initiatives in rice genomics and physiology contribute to global food security? Bioessays 26, 683-692. doi: 10.1002/bies.20040
8. Bürgmann, H., Meier, S., Bunge, M. W., Widmer, F., and Zeyer, J. (2005). Effects of model root exudates on structure and activity of a soil diazotroph community. Environ. Microbiol. 7, 1711-1724. doi: 10.1111/j.1462-2920.2005.00818.x
9. Cardoso, I. M., and Kuyper, T. W. (2006). Mycorrhizas and tropical soil fertility. Agric. Ecosyst. Environ. 116, 72-84. doi: 10.1016/j.agee.2006.03.011
10. Casas, C., Omacini, M., Montecchia, M. S., and Correa, O. S. (2011). Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340, 347-355. doi: 10.1007/s11104-010-0607-8
11. Cavagnaro, T. R., Jackson, L. E., Scow, K. M., and Hristova, K. R. (2007). Effects of arbuscular mycorrhizas on ammonia oxidizing bacteria in an organic farm soil. Microb. Ecol. 54, 618-626. doi: 10.1007/s00248-007-9212-7
12. Cawthray, G. R. (2003). An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J. Chromatogr. A 1011, 233-240. doi: 10.1016/S0021-9673(03)01129-4
13. Chaintreuil, C., Giraud, E., Prin, Y., Lorquin, J., Bâ, A., Gillis, M., et al. (2000). Photosynthetic Bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66, 5437-5447. doi: 10.1128/AEM.66.12.5437-5447.2000
14. Chen, X. P., Zhu, Y. G., Xia, Y., Shen, J. P., and He, J. Z. (2008). Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ. Microbiol. 10, 1978-1987. doi: 10.1111/j.1462-2920.2008.01613.x
15. Chen, Y., Peng, Y., Dai, C. C., and Ju, Q. (2011). Biodegradation of 4-hydroxybenzoic acid by Phomopsis liquidambari. Appl. Soil Ecol. 51, 102-110. doi: 10.1007/s10529-013-1347-7
16. Chen, Y., Ren, C. G., Yang, B., Peng, Y., and Dai, C. C. (2013a). Priming effects of the endophytic fungus Phomopsis liquidambari on soil mineral N transformation. Microb. Ecol. 65, 161-170. doi: 10.1007/s00248-012-0093-z
17. Chen, Y., Wang, H. W., Li, L., and Dai, C. C. (2013b). The potential application of the endophyte Phomopsis liquidambari to the ecological remediation of long-term cropping soil. Appl. Soil Ecol. 67, 20-26. doi: 10.1016/j.apsoil.2013.02.004
18. Chen, Y., Xie, X. G., Ren, C. G., and Dai, C. C. (2013c). Degradation of N-heterocyclic indole by a novel endophytic fungus Phomopsis liquidambari. Bioresour. Technol. 129, 568-574. doi: 10.1016/j.biortech.2012.11.100
19. Chen, Y. L., Chen, B. D., Hu, Y. J., Li, T., Zhang, X., Hao, Z. P., et al. (2013d). Direct and indirect influence of arbuscular mycorrhizal fungi on abundance and community structure of ammonia oxidizing bacteria and archaea in soil microcosms. Pedobiologia 56, 205-212. doi: 10.1016/j.pedobi.2013.07.003
20. Chen, Y. L., Xu, Z. W., Hu, H. W., Hu, Y. J., Hao, Z. P., Jiang, Y., et al. (2013e). Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl. Soil Ecol. 68, 36-45. doi: 10.1016/j.apsoil.2013.03.006
21. Cocking, E. C. (2003). Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252, 169-175. doi: 10.1023/A:1024106605806
22. Cohen, S. A., Meys, M., and Tarvin, T. L. (1989). The Pico-Tag Method-A Manual of Advanced Techniques for Amino Acids Analysis. Bedford: Waters, Division of Milipore.
23. Di, H. J., Cameron, K. C., Shen, J. P., Winefield, C. S., O'Callaghan, M., Bowatte, S., et al. (2009). Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2, 621-624. doi: 10.1038/ngeo613
24. Escobar, M. A., Geisler, D. A., and Rasmusson, A. G. (2006). Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J. 45, 775-788. doi: 10.1111/j.1365-313X.2005.02640.x
25. Falkowski, P. G., Fenchel, T., and Delong, E. F. (2008). The microbial engines that drive Earth's biogeochemical cycles. Science 320, 1034-1039. doi: 10.1126/science.1153213
26. Feng, Y., Shen, D., and Song, W. (2006). Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J. Appl. Microbiol. 100, 938-945. doi: 10.1111/j.1365-2672.2006.02843.x
27. Fontaine, S., and Barot, S. (2005). Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol. Lett. 8, 1075-1087. doi: 10.1111/j.1461-0248.2005.00813.x
28. Francis, C. A., Roberts, K. J., Beman, J. M., Alyson, E. S., and Oakley, B. B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. U.S.A. 102, 14683-14688. doi: 10.1073/pnas.0506625102
29. Grayston, S. J., Wang, S. Q., Campbell, C. D., and Edwards, A. C. (1998). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol. Biochem. 30, 369-378. doi: 10.1016/S0038-0717(97)00124-7
30. Gruber, N., and Galloway, J. N. (2008). An Earth-system perspective of the global nitrogen cycle. Nature 451, 293-296. doi: 10.1038/nature06592
31. Gubry-Rangin, C., Nicol, G. W., and Prosser, J. I. (2010). Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol. Ecol. 74, 566-574. doi: 10.1111/j.1574-6941.2010.00971.x
32. He, J. Z., Shen, J. P., Zhang, L. M., Zhu, Y. G., Zheng, Y. M., Xu, M. G., et al. (2007). Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364-2374. doi: 10.1111/j.1462-2920.2007.01358.x
33. Jia, Z., and Conrad, R. (2009). Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11, 1658-1671. doi: 10.1111/j.1462-2920.2009.01891.x
34. Ke, X., Angel, R., Lu, Y., and Conrad, R. (2013). Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ. Microbiol. 15, 2275-2292. doi: 10.1111/1462-2920.12098
35. Knauth, S., Hurek, T., Brar, D., and Reinhold-Hurek, B. (2005). Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ. Microbiol. 7, 1725-1733. doi: 10.1111/j.1462-2920.2005.00841.x
36. Kronzucker, H. J., Glass, A. D. M., Siddiqi, M. Y., and Kirk, G. J. D. (2000). Comparative kinetic analysis of ammonium and nitrate acquisition by tropical lowland rice: implications for rice cultivation and yield potential. New Phytol. 145, 471-476. doi: 10.1046/j.1469-8137.2000.00606.x
37. Kronzucker, H. J., Siddiqi, M. Y., Glass, A. D. M., and Kirk, G. J. D. (1999). Nitrate-ammonium synergism in rice: a subcellular flux analysis. Plant Physiol. 119, 1041-1046. doi: 10.1104/pp.119.3.1041
38. Kurola, J., Salkinoja-Salonen, M., Aarnio, T., Hultman, J., and Romantschuk, M. (2005). Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil. FEMS Microbiol. Lett. 250, 33-38. doi: 10.1016/j.femsle.2005.06.057
39. Kuzyakov, Y. (2002). Review: factors affecting rhizosphere priming effects. J. Plant Nutr. Soil Sci. 165, 382-396. doi: 10.1002/1522-2624(200208)165:4<382::AID-JPLN382>3.0.CO;2-#
40. Ladha, J., and Reddy, P. (2003). Nitrogen fixation in rice systems: state of knowledge and future prospects. Plant Soil 252, 151-167. doi: 10.1023/A:1024175307238
41. Lakshmanan, V., Selvaraj, G., and Bais, H. P. (2014). Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol. 166, 689-700. doi: 10.1104/pp.114.245811
42. Lemons, A., Clay, K., and Rudgers, J. A. (2005). Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia 145, 595-604. doi: 10.1007/s00442-005-0163-8
43. Li, X., Wang, C., Ren, C. G., and Dai, C. C. (2009). Effect of endophytic fungus B3 and different amounts of nitrogen applied on growth and yield in rice (Oriza sativa L.). Jiangsu J. Agric. Sci. 25, 1207-1212.
44. Lu, Y., Rosencrantz, D., Liesack, W., and Conrad, R. (2006). Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ. Microbiol. 8, 1351-1360. doi: 10.1111/j.1462-2920.2006.01028.x
45. Lyons, P. C., Evans, J. J., and Bacon, C. W. (1990). Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiol. 92, 726-732. doi: 10.1104/pp.92.3.726
46. Ma, B. L., Dwyer, L. M., and Gregorich, E. G. (1999). Soil nitrogen amendment effects on seasonal nitrogen mineralization and nitrogen cycling in maize production. Agron. J. 91, 1003-1009. doi: 10.2134/agronj1999.914650x
47. Marschner, P., Yang, C. H., Lieberei, R., and Crowley, D. E. (2001). Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol. Biochem. 33, 1437-1445. doi: 10.1016/S0038-0717(01)00052-9
48. Nobili, M. D., Contin, M., Mondini, C., and Brookes, P. C. (2001). Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol. Biochem. 33, 1163-1170. doi: 10.1016/S0038-0717(01)00020-7
49. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Michin, P. R., O'Hara, R. B., et al. (2012). Vegan: Community Ecology Package. Available at: http://CRAN.R-project.org/package=vegan
50. Omacini, M., Chaneton, E. J., Ghersa, C. M., and Otero, P. (2004). Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos 104, 581-590.
51. Prosser, J. I., and Nicol, G. W. (2008). Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931-2941. doi: 10.1111/j.1462-2920.2008.01775.x
52. R Development Core Team. (2010). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
53. Raman, D. R., Spanswick, R. M., and Walker, L. P. (1995). The kinetics of nitrate uptake from flowing nutrient solutions by rice: influence of pretreatment and light. Bioresour. Technol. 53, 125-132. doi: 10.1016/0960-8524(95)98138-E
54. Rasmussen, S., Parsons, A. J., Bassett, S., Christensen, M. J., Hume, D. E., Johnson, L. J., et al. (2007). High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol. 173, 787-797. doi: 10.1111/j.1469-8137.2006.01960.x
55. Ravel, C., Courty, C., Coudret, A., and Charmet, G. (1997). Beneficial effects of Neotyphodium lolii on the growth and the water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie 17, 173-181. doi: 10.1051/agro:19970304
56. Raymond, J., Siefert, J. L., Staples, C. R., and Blankenship, R. E. (2004). The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541-554. doi: 10.1093/molbev/msh047
57. Redman, R. S., Sheehan, K. B., Stout, R. G., Rodriguez, R. J., and Henson, J. M. (2002). Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298, 1581. doi: 10.1126/science.1072191
58. Rengel, Z. (2002). Genetic control of root exudation. Plant Soil 245, 59-70. doi: 10.1023/A:1020692715291
59. Revsbech, N. P., Pedersen, O., Reichardt, W., and Briones, A. (1999). Microsensor analysis of oxygen and pH in the rice rhizosphere under field and laboratory conditions. Biol. Fertil. Soils 29, 379-385. doi: 10.1007/s003740050568
60. Rodriguez, R. J., Henson, J., Van Volkenburgh, E., Hoy, M., Wright, L., Beckwith, F., et al. (2008). Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2, 404-416. doi: 10.1038/ismej.2007.106
61. Roger, P. A., and Ladha, J. (1992). Biological N2 fixation in wetland rice fields: estimation and contribution to nitrogen balance. Plant Soil 141, 41-55. doi: 10.1007/BF00011309
62. Rotthauwe, J. H., Witzel, K. P., and Liesack, W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular finescale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704-4712.
63. Rovira, A. (1969). Plant root exudates. Bot. Rev. 35, 35-57. doi: 10.1007/BF02859887
64. Saari, S., and Faeth, S. H. (2012). Hybridization of Neotyphodium endophytes enhances competitive ability of the host grass. New Phytol. 195, 231-236. doi: 10.1111/j.1469-8137.2012.04140.x
65. Schardl, C. L., Leuchtmann, A., and Spiering, M. J. (2004). Symbioses of grasses with seedborne fungal endophytes. Annu. Rev. Plant Biol. 55, 315-334. doi: 10.1146/annurev.arplant.55.031903.141735
66. Shi, Y., Dai, C. C., Wu, Y. C., and Yuan, Z. L. (2004). Study on the degradation of wheat straw by endophytic fungi. Acta Sci. Circum. 24, 144-149. doi: 10.1016/j.biortech.2011.02.064
67. Tian, L. S., Dai, C. C., Zhao, Y. T., Zhao, M., Yong, Y. H., and Wang, X. X. (2007). The degradation of phenanthrene by endophytic fungi Phomopsis sp. single and co-cultured with rice. China Environ. Sci. 27, 757-762.
68. Treonis, A. M., Grayston, S. J., Murray, P. H., and Dawson, L. A. (2005). Effects of root feeding, cranefly larvae on soil microorganisms and the composition of rhizosphere solutions collected from grassland plants. Appl. Soil Ecol. 28, 203-215. doi: 10.1016/j.apsoil.2004.08.004
69. Upson, K. K., Read, D. J., and Newsham, K. K. (2009). Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20, 1-11. doi: 10.1007/s00572-009-0260-3
70. Van Hecke, M., Treonis, A., and Kaufman, J. (2005). How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275, 101-109. doi: 10.1007/s11104-005-0380-2
71. Veresoglou, S. D., Sen, R., Mamolos, A. P., and Veresoglou, D. S. (2011). Plant species identity and arbuscular mycorrhizal status modulate potential nitrification rates in nitrogen-limited grassland soils. J. Ecol. 99, 1339-1349. doi: 10.1111/j.1365-2745.2011.01863.x
72. Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setala, H., van der Putten, W. H., and Wall, D. H. (2004). Ecological linkages between aboveground and belowground biota. Science 304, 1629-1633. doi: 10.1126/science.1094875
73. Wartiainen, I., Eriksson, T., Zheng, W. W., and Rasmussen, U. (2008). Variation in the active diazotrophic community in rice paddy-nifH PCR-DGGE analysis of rhizosphere and bulk soil. Appl. Soil. Ecol. 39, 65-75. doi: 10.1016/j.apsoil.2007.11.008
74. Whipps, J. M. (2001). Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487-511. doi: 10.1093/jexbot/52.suppl_1.487
75. Yang, B., Wang, X. M., Ma, H. Y., Jia, Y., Li, X., and Dai, C. C. (2014a). Effects of the fungal endophyte Phomopsis liquidambari on nitrogen uptake and metabolism in rice. Plant Growth Regul. 73, 165-179. doi: 10.1016/j.plaphy.2014.06.002
76. Yang, B., Ma, H. Y., Wang, X. M., Jia, Y., Hu, J., Li, X., et al. (2014b). Improvement of nitrogen accumulation and metabolism in rice (Oryza sativa L.) by the endophyte Phomopsis liquidambari. Plant Physiol. Biochem. 82, 172-182. doi: 10.1016/j.plaphy.2014.06.002
77. Yang, T., Du, W., Zhou, J., Wang, X. X., and Dai, C. C. (2013). Effects of the symbiosis between fungal endophytes and Atractylodes lancea on rhizosphere and phyllosphere microbial communities. Symbiosis 61, 23-36. doi: 10.1007/s13199-013-0254-y
78. Yemm, E. W., and Willis, A. J. (1954). The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57, 508-514. doi: 10.1042/bj0570508
79. Yoshida, S., Forno, D. A., Cock, J. H., and Gomez, K. A. (1976). Laboratory Manual for Physiological Studies of Rice. Los Banos: International Rice Research Institute.
80. Youngdahl, L., Pacheco, R., Street, J., and Vlex, P. L. G. (1982). The kinetics of ammonium and nitrate uptake by young rice plants. Plant Soil 69, 225-232. doi: 10.1007/BF02374517
81. Yuan, Z. L., Dai, C. C., Li, X., Tian, L. S., and Wang, X. X. (2007). Extensive host range of an endophytic fungus affects the growth and physiological functions in rice (Oryza sativa L.). Symbiosis 43, 21-28.
82. Yuan, Z. L., Dai, C. C., Shi, Y., Zhang, D. Z., and Wang, A. Q. (2004). Study of the mechanism of a strain of endophytic fungi's stimulation the growth of rice. Jiangsu J. Agric. Sci. 2, 10-13.
83. Zehr, J. P., Jenkins, B. D., Short, S. M., and Steward, G. F. (2003). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5, 539-554. doi: 10.1046/j.1462-2920.2003.00451.x
84. Zhang, L. M., Hu, H. W., Shen, J. P., and He, J. Z. (2012). Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J. 6, 1032-1045. doi: 10.1038/ismej.2011.168
85. Zhang, L. M., Offre, P. R., He, J. Z., Verhamme, D. T., Nicol, G. W., and Prosser, J. I. (2010). Autotrophic ammonia oxidation by soil thaumarchaea. Proc. Natl. Acad. Sci. U.S.A. 107, 17240-17245. doi: 10.1073/pnas.1004947107
86. Zhu, Z. (1989). "Progress in irrigated rice research," in Dynamics of Soil Nitrogen and Its Management, (Manila: International Rice Research Institute), 151-164.