The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Salvioli, Alessandra ^a   Zouari, Inès ^a   Chalot, Michel ^c   Bonfante, Paola ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b CNR   (Italy)

^c UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARBUSCULAR; FUNGI; GLOMUS; LYCOPERSICON ESCULENTUM;

ASPARAGINE; GLUTAMINE; NITROGEN; PLANT RNA; TRANSCRIPTOME;

ARTICLE; CARBOHYDRATE METABOLISM; CHEMISTRY; FLOWER; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; PLANT GENE; SIGNAL TRANSDUCTION; SYMBIOSIS; TIME; TOMATO;

ASPARAGINE; CARBOHYDRATE METABOLISM; FLOWERS; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUTAMINE; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE ANNOTATION; MYCORRHIZAE; NITROGEN; RNA, PLANT; SIGNAL TRANSDUCTION; SYMBIOSIS; TIME FACTORS; TRANSCRIPTOME;

EID: 84858842003     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-44     Document Type: Article

References (84)

1. Smith SE, Read DJ. Mycorrhizal symbiosis 2008, Cambridge, UK: Academic Press.
2. Bonfante P, Requena N. Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 2011, 14:1-7. 10.1016/j.pbi.2010.11.003, 21144795.
3. Javot H, Pumplin N, Harrison MJ. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 2007, 30:310-322. 10.1111/j.1365-3040.2006.01617.x, 17263776.
4. Bonfante P, Genre A. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 2010, 1:48.
5. Jakobsen I, Rosendahl L. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 1990, 115:77-83.
6. Pozo MJ, Azcón-Aguilar C. Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 2007, 10:393-398. 10.1016/j.pbi.2007.05.004, 17658291.
7. Wu QS, Xia RX. Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 2006, 163:417-425. 10.1016/j.jplph.2005.04.024, 16455355.
8. Medina A, Azcón R. Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. J Soil Sci Plant Nutr 2010, 10:354-372.
9. Leyval C, Joner EJ, del Val C, Haselwandter K. Potential of arbuscular mycorrhizal fungi for bioremediation. Mycorrhizal Technology in Agriculture 2002, 175-186. Switzerland: Birkhäuser Verlag, Gianinazzi S, Schuepp H, Barea JM, Haselwandter K.
10. Wang FY, Tong RJ, Shi ZY, Xu XF, He XH. Inoculations with arbuscular mycorrhizal fungi increase vegetable yields and decrease phoxim concentrations in carrot and green onion and their soils. PLoS One 2011, 6:e16949. 10.1371/journal.pone.0016949, 3036715, 21347374.
11. Tisdall JM, Oades JM. Stabilization of soil aggregates by the root systems of ryegrass. Aust J Soil Res 1979, 17:429-441.
12. Degens BP, Sparling GP, Abbott LK. Increasing the length of hyphae in a sandy soil increases the amount of water-stable aggregates. Appl Soil Ecol 1996, 3:149-159.
13. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010, 20:519-530. 10.1007/s00572-010-0333-3, 20697748.
14. Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ. Transcript profiling coupled with spatial expression analyses reveals genesinvolved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 2003, 15:2106-2123. 10.1105/tpc.014183, 181334, 12953114.
15. Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 2005, 137:1283-1301. 10.1104/pp.104.056572, 1088321, 15778460.
16. Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P. Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 2009, 182:200-212. 10.1111/j.1469-8137.2008.02725.x, 19192192.
17. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L. Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 2009, 184:975-987. 10.1111/j.1469-8137.2009.03031.x, 19765230.
18. Dermatsev V, Weingarten-Baror C, Resnick N, Gadkar V, Wininger S, Kolotilin I, Mayzlish-Gati E, Zilberstein A, Koltai H, Kapulnik Y. Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Mol Plant Path 2010, 11:121-135.
19. García Garrido JM, Morcillo RJL, Martín Rodríguez JA, Ocampo Bote JA. Variations in the mycorrhization characteristics in roots of wild-type and ABA-deficient tomato are accompanied by specific transcriptomic alterations. Mol Plant-Microbe In 2010, 23:651-664.
20. López-Ráez JA, Verhage A, Fernández I, Garciá JM, Azcón-Aguilar C, Flors V, Pozo MJ. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 2010, 61:2589-2601. 10.1093/jxb/erq089, 2882257, 20378666.
21. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo a massive and specific reprogramming during arbuscular mycorrhizal development. Plant J 2012, 69(3):510-528. doi: 10.1111/j.1365-313X.2011.04810.x, 10.1111/j.1365-313X.2011.04810.x, 21978245.
22. Ruzicka DR, Hausmann NT, Barrios-Masias FH, Jackson LE, Schachtman DP. Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil 2012, 350:145-162.
23. Taylor J, Harrier LA. Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae. Plant Mol Biol 2003, 51:619-629. 10.1023/A:1022341422133, 12650627.
24. García Rodríguez S, Pozo MJ, Azcon Aguilar C, Ferrol N. Expression of a tomato sugar transporter is increased in leaves of mycorrhizal or Phytophthora parasitica-infected plants. Mycorrhiza 2005, 15:489-496. 10.1007/s00572-005-0354-5, 15772814.
25. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 2007, 50:529-544. 10.1111/j.1365-313X.2007.03069.x, 17419842.
26. Subramanian KS, Santhanakrishnan P, Balasubramanian P. Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Hortic 2006, 107:245-253.
27. Dasgan HY, Kusvuran S, Ortas I. Responses of soilless grown tomato plants to arbuscular mycorrhizal fungal (Glomus fasciculatum) colonization in re-cycling and open systems. Afr J Biotechnol 2008, 7:3606-3613.
28. Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C, Scarpato R. Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Brit J Nutr 2012, 107:242-251. 10.1017/S000711451100290X, 21733294.
29. Schwarz D, Welter S, Greoge E, Franken P, Lehmann K, Weckwert W, Dölle S, Worm M. Impact of arbuscular mycorrhizal fungi on the allergenic potential of tomato. Mycorrhiza 2011, 21:341-349. 10.1007/s00572-010-0345-z, 21063890.
30. Martí E, Gisbert C, Bishop GJ, Dixon MS, Garcia-Martinez JL. Genetic and physiological characterization of tomato cv. Micro-Tom J Exp Bot 2006, 57:2037-2047.
31. Scott JW, Harbaugh BK. Micro-Tom. A miniature dwarf tomato. Florida Agr Expt Sta Cir 1989, 370:1-6.
32. Dan Y, Yan H, Munyikwa T, Dong J, Zhang Y, Armstrong CL. MicroTom-a high-throughput model transformation system for functional genomics. Plant Cell Rep 2006, 25:432-441. 10.1007/s00299-005-0084-3, 16341726.
33. Campos ML, Carvalho RF, Benedito VA, Peres LE. Small and remarkable: the Micro-Tom model system as a tool to discover novel hormonal functions and interactions. Plant Signal Behav 2010, 5:267-270. 10.4161/psb.5.3.10622, 2881274, 20037476.
34. Serrani J, Fos M, Atarés A, García-Martínez J. Effect of Gibberellin and Auxin on Parthenocarpic Fruit Growth Induction in the cv Micro-Tom of Tomato. J Plant Growth Regul 2007, 26:211-221.
35. Martinelli F, Uratsu SL, Reagan RL, Chen Y, Tricoli D, Fiehn O, Rocke DM, Gasser CS, Dandekar AM. Gene regulation in parthenocarpic tomato fruit. J Exp Bot 2009, 60:3873-3890. 10.1093/jxb/erp227, 2736898, 19700496.
36. Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latche A, Pech JC, Fernie AR, Bouzayen M. Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 2009, 21:1428-1452. 10.1105/tpc.108.060830, 2700536, 19435935.
37. Serrani JC, Carrera E, Ruiz-Rivero O, Gallego-Giraldo L, Peres LEP, Garcia-Martinez JL. Inhibition of auxin transport from the ovary or from the apical shoot induces parthenocarpic fruit-set in tomato mediated by gibberellins. Plant Physiol 2010, 153:851-862. 10.1104/pp.110.155424, 2879769, 20388661.
38. Waller JC, Akhtar TA, Lara- Núñez A, Gregory JF. McQuinn RP, Giovannoni JJ, Hanson AD: Developmental and Feedforward Control of the Expression of Folate Biosynthesis Genes in Tomato Fruit. Molecular Plant 2010, 3:66-77. 10.1093/mp/ssp057, 20085893.
39. Goff SA, Klee HJ. Plant volatile compounds: sensory cues for health and nutritional value?. Science 2006, 311:815-819. 10.1126/science.1112614, 16469919.
40. Sorrequieta A, Ferraro G, Boggio SB, Valle EM. Free amino acid production during tomato ripening: a focus on L-glutamate. Amino Acids 2010, 38:1523-1532. 10.1007/s00726-009-0373-1, 19876714.
41. Castellanos-Morales V, Villegas J, Wendelin S, Vierheilig H, Eder R, Cárdenas-Navarro R. Root colonisation by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruits (Fragaria × ananassaDuch.) at different nitrogen levels. J Sci Food Agric 2010, 90:1774-1782.
42. Douds DD, Nagahashi G, Shenk JE, Demchak K. Inoculation of strawberries with AM fungi produced on-farm increased yield. Biol Agric Hortic 2008, 26:209-219.
43. Gillaspy G, Ben-David H, Gruissem W. Fruits: a developmental perspective. The Plant Cell 1993, 5:1439-1451. 160374, 12271039.
44. Defilippi BG, Kader AA, Dandekar AM. Apple aroma: alcohol acyltransferase, a rate limiting step for ester biosynthesis, is regulated by ethylene. Plant Science 2005, 168:1199-1210.
45. Yahyaoui FE, Wongs-Aree C, Latché A, Hackett R, Grierson D, Pech JC. Molecular and biochemical characteristics of a gene encoding an alcohol acyl-transferase involved in the generation of aroma volatile esters during melon ripening. Eur J Biochem 2002, 269:2359-2366. 10.1046/j.1432-1033.2002.02892.x, 11985619.
46. Schubert KR, Boland MJ. The ureides. The Biochemistry of Plants 1990, 197-282. New York: Academic New York, Miflin BJ, Lea PJ.
47. Ohta K, Kanahama K, Kanayama Y. Enhanced expression of a novel dioxygenase during the early developmental stage of tomato fruit. J Plant physiol 2005, 162:697-702. 10.1016/j.jplph.2004.10.007, 16008092.
48. Kotake T, Takata R, Verma R, Takaba M, Yamaguchi D, Orita T, Kaneko S, Matsuoka K, Koyama T, Reiter WD, Tsumuraya Y. Bifunctional cytosolic UDP-glucose 4-epimerases catalyse the interconversion between UDP-D-xylose and UDP-L-arabinose in plants. Biochem J 2009, 424:169-177. 10.1042/BJ20091025, 19754426.
49. Van der Rest B, Rolland N, Boisson AM, Ferro M, Bligny R, Douce R. Identification and characterization of plant glycerophosphodiester phosphodiesterase. Biochem J 2004, 379:601-607. 10.1042/BJ20031489, 1224124, 14750903.
50. Hayashi S, Ishii T, Matsunaga T, Tominaga R, Kuromori T, Wada T, Shinozaki K, Hirayama T. The Glycerophosphoryl Diester Phosphodiesterase-Like Proteins SHV3 and its homologs play important roles in cell wall organization. Plant Cell Physiol 2008, 49:1522-1535. 10.1093/pcp/pcn120, 18718934.
51. Duan CQ, Shen YY, Liang XE, Zhang DP. Membrane-associated protein kinase activities in developing apple fruit. Physiol Plant 2003, 118:105-113. 10.1034/j.1399-3054.2003.00103.x, 12702019.
52. Koyama T, Furutani M, Tasaka M, Masaru OT. TCP Transcription Factors Control the Morphology of Shoot Lateral Organs via Negative Regulation of the Expression of Boundary-Specific Genes in Arabidopsis. Plant Cell 2007, 19:473-484. 10.1105/tpc.106.044792, 1867346, 17307931.
53. Faivre-Rampant O, Bryan GJ, Roberts AG, Milbourne D, Viola R, Taylor MA. Regulated expression of a novel TCP domain transcription factor indicates an involvement in the control of meristem activation processes in Solanum tuberosum. J Exp Bot 2004, 55:951-953. 10.1093/jxb/erh082, 14990618.
54. Lanfranco L, Guether M, Bonfante P. Arbuscular mycorrhizas and N acquisition by plants. Ecological Aspects of Nitrogen Metabolism in Plants 2011, 52-68. Chichester: Wiley, Polacco JC, Todd CD.
55. Hildebrandt U, Schmelzer E, Bothe H. Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 2002, 115:125-136. 10.1034/j.1399-3054.2002.1150115.x, 12010476.
56. Liu Q, Feng Y, Zhu Z. Dicer-like (DCL) proteins in plants. Funct Integr Genom 2009, 9:277-286.
57. McKim S, Hay A. Patterning and evolution of floral structures - marking time. Curr Opin Genet Dev 2010, 20:448-453. 10.1016/j.gde.2010.04.007, 20452201.
58. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G. Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 2010, 138:226-237. 10.1111/j.1399-3054.2009.01320.x, 20015123.
59. Perez AG, Olias R, Luaces P, Sanz C. Biosynthesis of strawberry aroma compounds through amino acid metabolism. J Agric Food Chem 2002, 5:4037-4042.
60. Lucchetta L, Manríquez D, El-Sharkawy I, Flores FB, Latché A, Pech JC. The role of ethylene in the expression of genes involved in the biosynthesis of aroma volatiles in melon. Advances in Plant Ethylene Research. Proceedings of the 7th International Symposium on the Plant Hormone Ethylene 2007, 4:189-195.
61. Balbontín C, Gaete-Eastman C, Fuentes L, Figueroa CR, Herrera R, Manriquez D, Latché A, Pech JC, Moya-León MA. VpAAT1, a gene encoding an alcohol acyltransferase, is involved in ester biosynthesis during ripening of mountain papaya fruit. J Agric Food Chem 2010, 58:5114-5121. 10.1021/jf904296c, 20369803.
62. Picton S, Gray JE, Payton S, Barton SL, Lowe A, Grierson D. A histidine decarboxylase-like mRNA is involved in tomato fruit ripening. Plant Mol Biol 1993, 23:627-631. 10.1007/BF00019310, 8219096.
63. Carbone F, Pizzichini D, Giuliano G, Rosati C, Perrotta G. Comparative profiling of tomato fruits and leaves evidences a complex modulation of global transcript profiles. Plant Science 2005, 169:165-175.
64. Lackey GD, Gross KC, Wallner SJ. Loss of tomato cell wall Galactan may involve reduced rate of synthesis. Plant Physiol 1980, 66:532-533. 10.1104/pp.66.3.532, 440668, 16661470.
65. Ge W, Song Y, Zhang C, Zhang Y, Burlingame AL, Guo Y. Proteomic analyses of apoplastic proteins from germinating Arabidopsis thaliana pollen. Biochim Biophys Acta 2011, 1814(12):1964-1973. 10.1016/j.bbapap.2011.07.013, 21798377.
66. Smith SE, Jakobsen I, Grønlund M, Smith FA. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 2011, 156:1050-1057. 10.1104/pp.111.174581, 21467213.
67. Cheng L, Bucciarelli B, Liu J, Zinn K, Miller S, Patton-Vogt J, Allan D, Shen J, Vance CP. White Lupin Cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiol 2011, 156:1131-1148. 10.1104/pp.111.173724, 3135957, 21464471.
68. Hause B, Mrosk C, Isayenkov S, Strack D. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 2007, 68:101-110. 10.1016/j.phytochem.2006.09.025, 17097695.
69. Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM. Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 2007, 175:554-564. 10.1111/j.1469-8137.2007.02107.x, 17635230.
70. Riedel T, Groten K, Baldwin IT. Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant Cell Environ 2008, 31:1203-1213. 10.1111/j.1365-3040.2008.01827.x, 18507809.
71. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435:819-823. 10.1038/nature03610, 15944705.
72. Desimone M, Catoni E, Ludewig U, Hilpert M, Schneider A, Kunze R, Tegeder M, Frommer WB, Schumacher K. A novel superfamily of transporters for allantoin and other oxo derivatives of nitrogen heterocyclic compounds in Arabidopsis. Plant Cell 2002, 14:847-856. 10.1105/tpc.010458, 150686, 11971139.
73. Yang J, Han KH. Functional characterization of allantoinase genes from arabidopsis and a nonureide-type legume black locust. Plant Physiol 2004, 134:1039-104972. 10.1104/pp.103.034637, 389928, 14976234.
74. Lam HM, Peng SSY, Coruzzi GM. Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol 1994, 106:1347-1357. 10.1104/pp.106.4.1347, 159672, 7846154.
75. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 2009, 9:10. 10.1186/1471-2229-9-10, 2649119, 19161626.
76. Schliemann W, Ammer C, Strack D. Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 2008, 69:112-146. 10.1016/j.phytochem.2007.06.032, 17706732.
77. Giovannoni JJ. Genetic regulation of fruit development and ripening. Plant Cell 2004, 16:170-180.
78. Kausch KD, Sobolev AP, Goyal RK, Fatima T, Laila-Beevi R, Sfatner RA, Handa AK, Matoo AK. Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicum L.) fruit. Amino Acids 2012, 42(2-3):843-856. 10.1007/s00726-011-1000-5, 21814797.
79. Hewitt EJ. Sand and water culture methods used in the study of plant nutrition. Tech Comm 22 1966, Crops, East Melling, Maidstone, Kent, England, 2, Commonw. Bur. Hortic. Plant.
80. Trouvelot A, Kough JL, Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de methods d'estimation ayant une signification fonctionnelle. Physiological and Genetical Aspects of Mycorrhizae 1986, 217-221. Paris: INRA, Gianinazzi-Pearson V, Gianinazzi S.
81. Smyth GK. Limma: linear models for microarray data. Bioinformatics and computational biology solutions using R and Bioconductor 2005, 397-420. New York, USA: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
82. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics Appl Note 2005, 21:3674-3676.
83. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
84. Javelle A, Morel M, Rodríguez-Pastrana BR, Botton B, André B, Marini AM, Brun A, Chalot M. Molecular characterization, function and regulation of ammonium transporters (Amt) and ammonium metabolizing enzymes (GS, NADP-GDH) in the ectomycorrhizal fungus Hebeloma cylindrosporum. Mol Microbiol 2003, 47:411-430. 10.1046/j.1365-2958.2003.03303.x, 12519192.