Detection of phytohormones in temperate forest fungi predicts consistent abscisic acid production and a common pathway for cytokinin biosynthesis

Mycologia

Volumn 107, Issue 2, 2015, Pages 245-257

  Morrison, Erin N ^a   Knowles, Sarah ^a   Hayward, Allison ^a   Greg Thorn, R ^b   Saville, Barry J ^a   Emery, R J N ^a  

^a TRENT UNIVERSITY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Abscisic acid; Cytokinins; Fungi; High performance liquid chromatography electrospray ionization tandem mass spectrometry; TRNA degradation pathway

Indexed keywords

ABSCISIC ACID; BIODEGRADATION; DETECTION METHOD; FUNGUS; HORMONE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; PHYTOCHEMISTRY; TEMPERATE FOREST;

FUNGI;

ABSCISIC ACID; CYTOKININ; PHYTOHORMONE;

BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; FOREST; FUNGUS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; TANDEM MASS SPECTROMETRY; TREE;

ABSCISIC ACID; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOKININS; FORESTS; FUNGI; PLANT GROWTH REGULATORS; TANDEM MASS SPECTROMETRY; TREES;

EID: 84938937506     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/14-157     Document Type: Article

References (67)

1. Ashby AM. 2000. Biotrophy and the cytokinin conundrum. Physiol Mol Plant Pathol 57:147-158, doi:10.1006/pmpp.2000.0294
2. Audenaert K, de Meyer GB, Hofte MM. 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128: 491-501, doi:10.1104/pp.010605
3. Barker SJ, Tagu D. 2000. The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144-154.
4. Behr M, Motyka V, Weihmann F, Malbeck J, Deising H, Wirsel S. 2012. Remodeling of cytokinin metabolism at infection sites of Colletotrichum graminicola on maize leaves. MPMI 25:1073-1082, doi:10.1094/MPMI-01-12-0012-R
5. Berger S, Sinha AK, Roitsch T. 2007. Plant physiology meets phytopathology: plant primary metabolism and plantpathogen interactions. J Exp Bot 58:4019-4026, doi:10.1093/jxb/erm298
6. Böker M, Basse CW, Schirawski J. 2008. Ustilago maydis secondary metabolism-from genomics to biochemistry. Fungal Genet Biol 45:S88-S93, doi:10.1016/j.fgb.2008.05.007
7. Braaksma A, Schaap DJ, Donkers JW, Schipper CMA. 2001. Effect of cytokinin on cap opening in Agaricus bisporus during storage. Postharvest Biol Technol 23:171-173, doi:10.1016/S0925-5214(01)00114-4
8. Bruce SA, Saville BJ, Emery RJN. 2011. Ustilago maydis produces cytokinins and abscisic acid for potential regulation of tumor formation in maize. J Plant Growth Regul 30:51-63, doi:10.1007/s00344-010-9166-8
9. Choi J, Choi D, Lee S, Ryu C-M, Hwang I. 2011. Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16:388-394, doi:10.1016/j.tplants.2011.03.003
10. Cooper SJ, Ashby AM. 1998. Comparison of cytokinin and cytokinin-O-glucoside cleaving β-glucosidase production in vitro by Venturia inaequalis and other phytopathogenic fungi with differing modes of nutrition in planta. Physiol Molecular Plant Pathol 53:61-72, doi:10.1006/pmpp.1998.0171
11. Costacurta A, Vanderleyden J. 1995. Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1-18, doi:10.3109/10408419509113531
12. Cowan AK, Cairns ALP, Bartels-Rahm B. 1999. Regulation of abscisic acid metabolism: toward a metabolic basis for abscisic acid-cytokinin antagonism. J Exp Bot 50:595-603, doi:10.1093/jxb/50.334.595
13. Crocoll C, Kettner J, Dörffling K. 1991. Abscisic acid in saprophytic and parasitic species of fungi. Phytochemistry 30:1059-1060, doi:10.1016/S0031-9422(00)95171-9
14. Dobrev PI, Kamínek M. 2002. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21-29, doi:10.1016/S0021-9673(02)00024-9
15. Dörffling K, Petersen W, Sprecher E, Urbasch I, Hanssen HP. 1984. Abscisic acid in phytopathogenic fungi of the genera Botrytis, Ceratocystis, Fusarium and Rhizoctonia. Z. Naturforsch 39:683-684.
16. Emery RJN, Leport L, Barton JE, Turner NC, Atkins CA. 1998. cis-isomers of cytokinins predominate in chickpea seeds throughout their development. Plant Physiol 117:1515-1523, doi:10.1104/pp.117.4.1515
17. Farrow SC, Emery RJN. 2012. Concurrent profiling of indole-3-acetic acid, abscisic acid, and cytokinins and structurally related purines by high-performance-liquid-chromatography tandem electrospray mass spectrometry. Plant Methods 8:42, doi:10.1186/1746-4811-8-42
18. Ferreira FJ, Kieber JJ. 2005. Cytokinin signaling. Curr Opin Plant Biol 8:518-525, doi:10.1016/j.pbi.2005.07.013
19. Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P. 2011. Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431-2452, doi:10.1093/jxb/err004
20. Gajdosova S, Spichal L, Kaminek M, Hoyerova K, Novak O, Dobrev P, Galuszka P, Klima P, Gaudinova A, Zizkova E, Hanus J, Dancak M, Travnicek B, Pesek B, Krupicka M, Vankova R, Strnad M, Motyka V. 2011. Distribution, biological activities, metabolism and the conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot 62:2827-2840, doi:10.1093/jxb/erq457
21. Golovko A, Hjälm G, Sitbon F, Nicander B. 2000. Cloning of a human tRNA isopentenyl transferase. Gene 258:85-93, doi:10.1016/S0378-1119(00)00421-2
22. Golovko A, Sitbon F, Tillberg E, Nicander B. 2002. Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana. Plant Mol Biol 49:161-169, doi:10.1023/A:1014958816241
23. Hartung W. 2010. The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37:806-812, doi:10.1071/FP10058
24. Hayward A, Coates KE, Galer AL, Hutchinson TC, Emery RJN. 2013. Chelator profiling in Deschampsia cespitosa (L.) Beauv. reveals a Ni reaction, which is distinct from the ABA and cytokinin-associated response to Cd. Plant Physiol Biochem 64:84-91, doi:10.1016/j.plaphy.2012.12.018
25. Hoyerová K, Gaudinová A, Malbeck J, Dobrev PI, Kocábek T, Solcova B, Trávnicková A, Kamínek M. 2006. Efficiency of different methods of extraction and purification of cytokinins. Phytochemistry 67:1151-1159, doi:10.1016/j.phytochem.2006.03.010
26. Hwang I, Sakakibara H. 2006. Cytokinin biosynthesis and perception. Physiol Plant 126:528-538, doi:10.1111/j.1399-3054.2006.00665.x
27. Jacobsen JV, Pearce DW, Poole AT, Pharis RP, Mander LN. 2002. Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant 115:428-441, doi:10.1034/j.1399-3054.2002.1150313.x
28. Jameson PA, Morris RO. 1989. Zeatin-like cytokinins in yeast: detection by immunological methods. J Plant Physiol 135:385-390, doi:10.1016/S0176-1617(89)80092-6
29. Johnston JC, Trione EJ. 1974. Cytokinin production by the fungi Taphrina cerasi and T. deformans. Can J Bot 52: 1583-1589, doi:10.1139/b74-207
30. Kakimoto T. 2003. Biosynthesis of cytokinins. J Plant Res 116:233-239, doi:10.1007/s10265-003-0095-5
31. Kaminek M. 1982. Mechanisms preventing the interference of tRNA cytokinins in hormonal regulation. In: Wareing, ed. Plant growth substances. New York: Academic Press. p 215-224.
32. Kettner J, Dörffling K. 1987. Abscisic acid metabolism in Ceratocystis coerulescens. Physiol Plant 69:278-282, doi:10.1111/j.1399-3054.1987.tb04287.x
33. Kraigher H, Grayling A, Wang TL, Hanke DE. 1991. Cytokinin production by two ectomycorrhizal fungi in liquid culture. Phytochemistry 30:2249-2254, doi:10.1016/0031-9422(91)83623-S
34. Laten HM, Zahareas-Doktor S. 1985. Presence and source of free isopentenyladenosine in yeasts. Proc Natl Acad Sci USA 82:1113-1115, doi:10.1073/pnas.82.4.1113
35. Mauch-Mani B, Mauch F. 2005. The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8: 409-414, doi:10.1016/j.pbi.2005.05.015
36. Mok DWS, Mok MC. 2001. Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89-118, doi:10.1146/annurev.arplant.52.1.89
37. Mok MC, Mok DWS, Armstrong DJ. 1978. Differential cytokinin structure-activity relationships in Phaseolus. Plant Physiol 61:72-75, doi:10.1104/pp.61.1.72
38. Murphy AM, Pryce-Jones E, Johnstone K, Ashby AM. 1997. Comparison of cytokinin production in vitro by Pyrenopeziza brassicae with other plant pathogens. Physiol Mol Plant Pathol 50:53-65, doi:10.1006/pmpp.1996.0070
39. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165-185, doi:10.1146/annurev.arplant.56.032604.144046
40. Nasim G, Rahman M. 2009. Cytokinin priming as a tool to induct in vitro growth and biomass production of some soil fungi. Pak J Bot 41:1445-1452.
41. Ng PP, Cole ALJ, Jameson PE, Mcwha JA. 1982. Cytokinin production by ectomycorrhizal fungi. New Phytol 91: 57-62, doi:10.1111/j.1469-8137.1982.tb03292.x
42. Nishiyama R, Wattanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Phan Tran LS. 2011. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169-2183, doi:10.1105/tpc.111.087395
43. Novák O, Tarkowski P, Tarkowská D, Dolezal K, Lenobel R, Strnad M. 2003. Quantitative analysis of cytokinins in plants by liquid chromatography-single-quadrupole mass spectrometry. Anal Chim Acta 480:207-218, doi:10.1016/S0003-2670(03)00025-4
44. Oritani T, Kiyota H. 2003. Biosynthesis and metabolism of abscisic acid and related compounds. Nat Prod Rep 20: 414-425, doi:10.1039/b109859b
45. Persson BC, Bjork GR. 1993. Isolation of the gene (miaE) encoding the hydroxylase involved in the synthesis of 2-methylthio-cis-ribozeatin in tRNA of Salmonella typhimurium and characterization of mutants. J Bacteriol 175:7776-7785.
46. Persson BC, Esberg B, Olafsen O, Bjork GR. 1994. Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie 76:1152-1160, doi:10.1016/0300-9084(94)90044-2
47. Pertry I, Václaviková K, Gemrotová M, Spichal L, Galuszka P, Depuydt S, Temmerman W, Stes E, de Keyser A, Fiefler M, Biondi S, Novak O, Schmülling T, Strnad M, Tarkowski P, Holsters M, Vereecke D. 2010. Rhodococcus fascians impacts plant development through the dynamic fas-mediated production of a cytokinin mix. MPMI 23:1164-1174, doi:10.1094/MPMI-23-9-1164
48. Prinsen E, Kaminek M, van Onckelen HA. 1997. Cytokinin biosynthesis: a black box? Plant Growth Regul 23:3-15, doi:10.1023/A:1005990123270
49. Quesnelle PE, Emery RJN. 2007. cis-cytokinins that predominate in Pisum sativum during early embryogenesis will accelerate embryo growth in vitro. Can J Bot 85:91-103, doi:10.1139/b06-149
50. Roitsch T, Ehneß R. 2000. Regulation of source/sink relations by cytokinins. Plant Growth Regul 32:359-367, doi:10.1023/A:1010781500705
51. Ross ARS, Ambrose SJ, Cutler AJ, Feurtado JA, Kermode AR, Nelson K, Zhou R, Abrams SR. 2004. Determination of endogenous and supplied deuterated abscisic acid in plant tissues by high-performance liquid chromatography-electrospray ionization tandem mass spectrometry with multiple reaction monitoring. Anal Biochem 329: 324-333, doi:10.1016/j.ab.2004.02.026
52. Rypacek V, Sladky Z. 1972. The character of endogenous growth regulators in the course of development in the fungus Lentinus tigrinus. Mycopathol Mycol Appl 46: 65-72, doi:10.1007/BF02051897
53. Rypacek V, Sladky Z. 1973. Relation between the level of endogenous growth regulators and the differentiation of the fungus Lentinus tigrinus studied in a synthetic medium. Biol Plant 15:20-26, doi:10.1007/BF02922509
54. Sakakibara H. 2006. Cytokinins: activity biosynthesis and translocation. Annu Rev Plant Biol 57:431-449, doi:10.1146/annurev.arplant.57.032905.105231
55. Schmelz EA, Engelberth J, Alborn HT, O'Donnell P, Sammons M, Toshima H, Tumlinson III JH. 2003. Simultaneous analysis of phytohormones, phytotoxins and volatile organic compounds in plants. PNAS 100: 10552-10557, doi:10.1073/pnas.1633615100
56. Schmidt K, Pflugmacher M, Klages S, Maser A, Mock A, Stahl DJ. 2008. Accumulation of the hormone abscisic acid (ABA) at the infection site of the fungus Cercospora beticola supports the role of ABA as a repressor of plant defense in sugar beet. Mol Plant Pathol 9:661-673, doi:10.1111/j.1364-3703.2008.00491.x
57. Schmitz RY, Skoog F, Playtis AJ, Leonard NJ. 1972. Cytokinins: synthesis and biological activity of geometric and position isomers of zeatin. Plant Physiol 50:702-705, doi:10.1104/pp.50.6.702
58. Seitzman BH, Ouimette A, Mixon RL, Hobbie EA, Hibbett DS. 2011. Conservation of biotrophy in Hygrophor-aceae inferred from combined stable isotope and phylogenetic analyses. Mycologia 103:280-290, doi:10.3852/10-195
59. Sood M. 2011. Cultural Physiology: effect of plant growth hormones on the growth and sporulation of Aspergillus umbrosus. J Phytol 3:27-29.
60. Spichal L. 2012. Cytokinins-recent news and views of evolutionally old molecules. Funct Plant Biol 39:267-284, doi:10.1071/FP11276
61. Stirk WA, van Staden J. 2010. Flow of cytokinins through the environment. Plant Growth Regul 62:101-116, doi:10.1007/s10725-010-9481-x
62. Tsai I, Tanaka E, Masuya H, Tanaka R, Hirooka Y, Endoh R, Sahashi N, Kikuchi T. 2014. Comparative genomics of Taphrina fungi causing varying degrees of tumorous deformity in plants. Genome Biol Evol 6:861-872, doi:10.1093/gbe/evu067
63. Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI. 2006. Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:133-143.
64. Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novak O, Strnad M, Ludwig-Muller J, Oelmuller R. 2008. The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. MPMI 21:1371-1383, doi:10.1094/MPMI-21-10-1371
65. van Rhijn JA, Heskamp HH, Davelaar E, Jordi W, Leloux MS, Brinkman UATh. 2001. Quantitative determination of glycosylated and aglycon isoprenoid cytokinins at sub-picomolar levels by microcolumn liquid chromatography combined with electrospray tandem mass spectrometry. J Chromatogr A 929:31-42, doi:10.1016/S0021-9673(01)01134-7
66. Walters DR, McRoberts N, Fitt BDL. 2008. Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biol Rev 83:79-102, doi:10.1111/j.1469-185X.2007.00033.x
67. Yarian C, Townsend H, Czestkowski W, Sochacka E, Malkiewicz AJ, Guenther R, Miskiewicz A, Agris PF. 2002. Accurate translation of the genetic code depends on tRNA modified nucleosides. J Biol Chem 277: 16391-16395, doi:10.1074/jbc.M200253200