Metabolomics suggests that soil inoculation with arbuscular mycorrhizal fungi decreased free amino acid content in roots of durum wheat grown under N-limited, P-rich field conditions

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Saia, Sergio ^a   Ruisi, Paolo ^a   Fileccia, Veronica ^a   Di Miceli, Giuseppe ^a   Amato, Gaetano ^a   Martinelli, Federico ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; NITROGEN; SATURATED FATTY ACID; PHOSPHORUS; SOIL;

AMINATION; ARBUSCULAR MYCORRHIZA; ARTICLE; BIOSYNTHESIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DERIVATIZATION; EXTRACTION; FUNGAL COLONIZATION; HYDROPHILIC INTERACTION CHROMATOGRAPHY; MASS FRAGMENTOGRAPHY; METABOLOME; METABOLOMICS; NONHUMAN; PLANT GROWTH; PLANT METABOLISM; PLANT ROOT; SOIL INOCULATION; TIME OF FLIGHT MASS SPECTROMETRY; TRITICUM DURUM; CHEMISTRY; GAS CHROMATOGRAPHY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PROCEDURES; SOIL; SOUTHERN EUROPE; WHEAT;

FUNGI; RHIZOBIALES; TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

AMINO ACIDS; CHROMATOGRAPHY, GAS; MEDITERRANEAN REGION; METABOLOMICS; MYCORRHIZAE; NITROGEN; PHOSPHORUS; PLANT ROOTS; SOIL; SOIL MICROBIOLOGY; TRITICUM;

EID: 84936128606     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129591     Document Type: Article

References (68)

1. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Smith SE, Read DJ, editors Academic Press. 787 p. doi: 10.1126/science.1208473
2. Saia S, Amato G, Frenda AS, Giambalvo D, Ruisi P (2014) Influence of arbuscular mycorrhizae on biomass production and nitrogen fixation of berseem clover plants subjected to water stress. PLoS One 9: e90738. doi: 10.1371/journal.pone.0090738 PMID: 24595111
3. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62: 227-250. doi: 10.1146/annurevarplant-042110-103846 PMID: 21391813
4. Hodge A, Storer K (2014) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil. doi: 10.1007/s11104-014-2162-1 PMID: 24744450
5. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, et al. (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109: 2666-2671. doi: 10.1073/pnas.1118650109 PMID: 22308426
6. Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2014) Mycorrhizal phenotypes and the Law of the Minimum. New Phytol. doi: 10.1111/nph.13172
7. Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant, Cell Environ 28: 1247-1254. doi: 10.1111/j.1365-3040.2005.01360.x
8. Saia S, Benítez E, García-Garrido JM, Settanni L, Amato G, Giambalvo D (2014) The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material. J Agric Sci 152: 370-378. doi: 10.1017/S002185961300004X
9. Leigh J, Fitter AH, Hodge A (2011) Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. Fems Micriobiology Ecol 76: 428-438. doi: 10.1111/j.1574-6941.2011.01066.x PMID: 21303398
10. Barea JM, Toro M, Orozco MO, Campos E, Azcón R (2002) The application of isotopic (32P and 15N) dilution techniques to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops. Nutr Cycl Agroecosystems 63: 35-42. doi: 10.1023/A:1020589732436
11. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, et al. (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819-823. doi: 10.1038/nature03610 PMID: 15944705
12. Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ, Shachar-Hill Y (2005) The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168: 687-696. doi: 10.1111/j.1469-8137.2005.01536.x PMID: 16313650
13. Guether M, Neuha¨user B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150: 73-83. doi: 10.1104/pp.109.136390 PMID: 19329566
14. Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182: 200-212. doi: 10.1111/j.1469-8137.2008.02725.x PMID: 19192192
15. Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, et al. (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136: 2483-2499. doi: 10.1104/pp.104.047019 PMID: 15375205
16. Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Bla¨sing O, et al. (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell Environ 30: 85-112. doi: 10.1111/j.1365-3040.2006.01608.x PMID: 17177879
17. Martinelli F, Remorini D, Saia S, Massai R, Tonutti P (2013) Metabolic profiling of ripe olive fruit in response to moderate water stress. Sci Hortic (Amsterdam) 159: 52-58. doi: 10.1016/j.scienta.2013.04.039
18. Martinelli F, Basile B, Morelli G, D'Andria R, Tonutti P (2012) Effects of irrigation on fruit ripening behavior and metabolic changes in olive. Sci Hortic (Amsterdam) 144: 201-207. doi: 10.1016/j.scienta.2012.07.012
19. Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69: 112-146. doi: 10.1016/j.phytochem.2007.06.032 PMID: 17706732
20. Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51: 139-148. doi: 10.1007/s13199-010-0083-1
21. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8: 1-10. doi: 10.1111/j.1462-2920.2005.00942.x PMID: 16343316
22. Draper J, Rasmussen S, Zubair H (2011) Metabolite Analysis and Metabolomics in the Study of Biotrophic Interactions between Plants and Microbes. In: Hall RD, editor. Annual Plant Reviews Volume 43: Biology of Plant Metabolomics. Oxford, UK: Wiley-Blackwell. doi: 10.1002/9781444339956.ch2
23. Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils. doi: 10.1007/s00374-015-0996-1
24. Glick BR (2012) Plant Growth-Promoting Bacteria: Mechanisms and Applications. Scientifica (Cairo) 2012: 1-15. doi: 10.6064/2012/963401
25. Lekberg Y, Koide RT (2014) Integrating physiological, community, and evolutionary perspectives on the arbuscular mycorrhizal symbiosis 1. Botany 92: 241-251. doi: 10.1139/cjb-2013-0182
26. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541-556. doi: 10.1146/annurev.micro.62.081307.162918 PMID: 19575558
27. Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 335: 311-323. doi: 10.1007/s11104-010-0417-z
28. Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer M, et al. (2011) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356: 151-163. doi: 10.1007/s11104-011-0960-2
29. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1: 387-396. doi: 10.1038/nprot.2006.59 PMID: 17406261
30. Kind T, Fiehn O (2006) Metabolomic database annotations via query of elemental compositions: mass accuracy is insufficient even at less than 1 ppm. BMC Bioinformatics 7: 234. doi: 10.1186/1471-2105-7-234 PMID: 16646969
31. Gika HG, Wilson ID, Theodoridis GA (2014) LC-MS-based holistic metabolic profiling. Problems, limitations, advantages, and future perspectives. J Chromatogr B Analyt Technol Biomed Life Sci 966: 1-6. doi: 10.1016/j.jchromb.2014.01.054 PMID: 24618029
32. Strehmel N, Kopka J, Scheel D, Böttcher C (2013) Annotating unknown components from GC/EI-MS-based metabolite profiling experiments using GC/APCI(+)-QTOFMS. Metabolomics 10: 324-336. doi: 10.1007/s11306-013-0569-y
33. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55: 158-IN18. doi: 10.1016/S0007-1536(70)80110-3
34. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84: 489-500. doi: 10.1111/j.1469-8137.1980.tb04556.x
35. Weckwerth W, Wenzel K, Fiehn O (2004) Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics 4: 78-83. doi: 10.1002/pmic.200200500 PMID: 14730673
36. Gullberg J, Jonsson P, Nordström A, Sjöström M, Moritz T (2004) Design of experiments: An efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal Biochem 331: 283-295. doi: 10.1016/j.ab.2004.04.037 PMID: 15265734
37. Lee DY, Fiehn O (2008) High quality metabolomic data for Chlamydomonas reinhardtii. Plant Methods 4: 7. doi: 10.1186/1746-4811-4-7 PMID: 18442406
38. SAS (2008) SAS/STAT 9.2. User's Guide. SAS Inst Inc.
39. Chagoyen M, Pazos F (2011) MBRole: enrichment analysis of metabolomic data. Bioinformatics 27: 730-731. doi: 10.1093/bioinformatics/btr001 PMID: 21208985
40. Leader DP, Burgess K, Creek D, Barrett MP (2011) Pathos: a web facility that uses metabolic maps to display experimental changes in metabolites identified by mass spectrometry. Rapid Commun Mass Spectrom 25: 3422-3426. doi: 10.1002/rcm.5245 PMID: 22002696
41. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B 57: 289-300. doi: 10.2307/2346101
42. Justes E, Mary B, Meynard J (1997) Evaluation of a nitrate test indicator to improve the nitrogen fertilisation of winter wheat crops. Diagnostic Proced Crop N Manag a Work Poitiers, Fr 22-23 November, 1995.
43. Longnecker N, Kirby EJM, Robson A (1993) Leaf Emergence, Tiller Growth, and Apical Development of Nitrogen-Dificient Spring Wheat. Crop Sci 33: 154. doi: 10.2135/cropsci1993.0011183X003300010028x
44. Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14: 263-269. doi: 10.1007/s00572-003-0265-2 PMID: 12942358
45. Gao X, Akhter F, Tenuta M, Flaten DN, Gawalko EJ, Grant CA (2010) Mycorrhizal colonization and grain Cd concentration of field-grown durum wheat in response to tillage, preceding crop and phosphorus fertilization. J Sci Food Agric 90: 750-758. doi: 10.1002/jsfa.3878 PMID: 20355108
46. Germida JJ, Walley FL (1996) Plant growth-promoting rhizobacteria alter rooting patterns and arbuscular mycorrhizal fungi colonization of field-grown spring wheat. Biol Fertil Soils 23: 113-120. doi: 10.1007/BF00336050
47. Teng W, Deng Y, Chen X-P, Xu X-F, Chen R-Y, Lv Y, et al. (2013) Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. J Exp Bot 64: 1403-1411. doi: 10.1093/jxb/ert023 PMID: 23382547
48. Mohammad A, Mitra B, Khan AG (2004) Effects of sheared-root inoculum of Glomus intraradices on wheat grown at different phosphorus levels in the field. Agric Ecosyst Environ 103: 245-249. doi: 10.1016/j.agee.2003.09.017
49. Fester T, Fetzer I, Buchert S, Lucas R, Rillig MC, Ha¨rtig C (2011) Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction. Oecologia 167: 913-924. doi: 10.1007/s00442-011-2037-6 PMID: 21643790
50. Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiol 146: 1440-1453. doi: 10.1104/pp.107.111898 PMID: 18218971
51. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci U S A 107: 13754-13759. doi: 10.1073/pnas.1005874107 PMID: 20631302
52. Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9: 110-115. doi: 10.1016/j.tplants.2004.01.006 PMID: 15003233
53. Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M-R, Borriss R, von Wirén N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174: 3-11. doi: 10.1002/jpln.201000085
54. Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30: 205-240. doi: 10.1080/10408410490468786 PMID: 15646398
55. Ramos-Gonzalez MI, Campos MJ, Ramos JL (2005) Analysis of Pseudomonas putida KT2440 Gene Expression in the Maize Rhizosphere: In Vivo Expression Technology Capture and Identification of Root-Activated Promoters. J Bacteriol 187: 5504-5504. doi: 10.1128/JB.187.15.5504.2005
56. Carvalhais LC, Dennis PG, Fan B, Fedoseyenko D, Kierul K, Becker A, et al. (2013) Linking plant nutritional status to plant-microbe interactions. PLoS One 8: e68555. doi: 10.1371/journal.pone.0068555 PMID: 23874669
57. Návarová H, Bernsdorff F, Döring A-C, Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24: 5123-5141. doi: 10.1105/tpc.112.103564 PMID: 23221596
58. Vogel-Adghough D, Stahl E, Návarová H, Zeier J (2013) Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco. Plant Signal Behav 8: e26366. doi: 10.4161/psb.26366 PMID: 24025239
59. Vranova V, Rejsek K, Skene KR, Formanek P (2011) Non-protein amino acids: Plant, soil and ecosystem interactions. Plant Soil 342: 31-48. doi: 10.1007/s11104-010-0673-y
60. Pálfi G, Dézsi L (1968) Pipecolic acid as an indicator of abnormal protein metabolism in diseased plants. Plant Soil 29: 285-291. doi: 10.1007/BF01348946
61. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, et al. (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100: 4927-4932. doi: 10.1073/pnas.0730845100 PMID: 12684534
62. Pfeffer P, Douds DD Jr, Becard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120: 587-598. PMID: 10364411
63. Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, et al. (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131: 1496-1507. doi: 10.1104/pp.102.007765 PMID: 12644699
64. Moche M, Stremlau S, Hecht L, Göbel C, Feussner I, Stöhr C (2010) Effect of nitrate supply and mycorrhizal inoculation on characteristics of tobacco root plasma membrane vesicles. Planta 231: 425-436. doi: 10.1007/s00425-009-1057-5 PMID: 19937342
65. Kobae Y, Gutjahr C, Paszkowski U, Kojima T, Fujiwara T, Hata S (2014) Lipid droplets of arbuscular mycorrhizal fungi emerge in concert with arbuscule collapse. Plant Cell Physiol. doi: 10.1093/pcp/pcu123
66. Laparre J, Malbreil M, Letisse F, Portais JC, Roux C, Bécard G, et al. (2014) Combining metabolomics and gene expression analysis reveals that propionyl- and butyryl-carnitines are involved in late stages of arbuscular mycorrhizal symbiosis. Mol Plant 7: 554-566. doi: 10.1093/mp/sst136 PMID: 24121293
67. Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, et al. (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128: 108-124. doi: 10.1104/pp.010466 PMID: 11788757
68. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23: 3812-3823. doi: 10.1105/tpc.111.089813 PMID: 21972259