Biosynthetic pathway of indole-3-acetic acid in ectomycorrhizal fungi collected from northern Thailand
Autoři:
Jaturong Kumla aff001; Nakarin Suwannarach aff001; Kenji Matsui aff003; Saisamorn Lumyong aff001
Působiště autorů:
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand
aff001; Center of Excellence in Microbial Diversity and Sustainable Utilization, Chiang Mai University, Chiang Mai Thailand
aff002; Graduate School of Sciences and Technology for Innovation, Faculty of Agriculture, Yamaguchi University, Yamaguchi, 7 Japan
aff003; Academy of Science, The Royal Society of Thailand, Bangkok, Thailand
aff004
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0227478
Souhrn
Indole-3-acetic acid (IAA) is an imperative phytohormone for plant growth and development. Ectomycorrhizal fungi (ECM) are able to produce IAA. However, only a few studies on IAA biosynthesis pathways in ECM fungi have been reported. This study aimed to investigate the IAA biosynthesis pathway of six ECM cultures including Astraeus odoratus, Gyrodon suthepensis, Phlebopus portentosus, Pisolithus albus, Pisolithus orientalis and Scleroderma suthepense. The results showed that all ECM fungi produced IAA in liquid medium that had been supplemented with L-tryptophan. Notably, fungal IAA levels vary for different fungal species. The detection of indole-3-lactic acid and indole-3-ethanol in the crude culture extracts of all ECM fungi indicated an enzymatic reduction of indole-3-pyruvic acid and indole-3-acetaldehyde, respectively in the IAA biosynthesis via the indole-3-pyruvic acid pathway. Moreover, the tryptophan aminotransferase activity confirmed that all ECM fungi synthesize IAA through the indole-3-pyruvic acid pathway. Additionally, the elongation of rice and oat coleoptiles was stimulated by crude culture extract. This is the first report of the biosynthesis pathway of IAA in the tested ECM fungi.
Klíčová slova:
Fungi – Rice – Biosynthesis – High performance liquid chromatography – Tryptophan – Aminotransferases – Indoles – Scleroderma
Zdroje
1. Teale WD, Paponov IA, Palme K. Auxin in action: signalling, transport and the control of plant growth and development. Nat. Rev. Mol. Cell Biol. 2006; 7: 847–859. doi: 10.1038/nrm2020 16990790
2. Zhao Y. Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 2010; 61: 49–64. doi: 10.1146/annurev-arplant-042809-112308 20192736
3. Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 2007; 31: 425–448. doi: 10.1111/j.1574-6976.2007.00072.x 17509086
4. Apine OA, Jadhav JP. Optimization of medium for indole-3-acetic acid production using Pantoea agglomerans strain PVM. J. Appl. Microbiol. 2011; 110: 1235–1244. doi: 10.1111/j.1365-2672.2011.04976.x 21332896
5. Sun P, Fang W, Shin L, Wei J, Fu S, Chou J. Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant Drosera indica L. PLoS One 2014; 9: e114196. doi: 10.1371/journal.pone.0114196 25464336
6. Yan X, Wang Z, Mei Y, Wang L, Wang X, Xu Q, et al. Isolation, diversity, and growth-promoting activities of endophytic bacteria from tea cultivars of Zijuan and Yunkang-10. Front. Microbiol. 2018; 9: 1848. doi: 10.3389/fmicb.2018.01848 30186243
7. Chung KR, Shilts T, Ertürk Ü, Timmer LW, Ueng PP. Indole derivatives produced by the fungus Colletotrichum acutatum causing lime anthracnose and postbloom fruit drop of citus. FEMS Microbiol. Lett. 2003; 226: 23–30. doi: 10.1016/S0378-1097(03)00605-0 13129603
8. Duca D, Lorv J, Patten CL, Rose D, Glick BR. Indole-3-acetic acid in plant-microbe interactions. Antonie van Leeuwenhoek. 2014; 106: 85–125. doi: 10.1007/s10482-013-0095-y 24445491
9. Krause K, Henke C, Asiimwe T, Ulbricht A, Klemmer S, Schachtschabel D, et al. Biosynthesis and secretion of indole-3-acetic acid and its morphological effects on Tricholoma vaccinum-spruce ectomycorrhiza. Appl. Environ. Microbiol. 2015; 81: 7003–7011. doi: 10.1128/AEM.01991-15 26231639
10. Spaepen S, Vanderleyden J. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol. 2011; 3, a001438. doi: 10.1101/cshperspect.a001438 21084388
11. Oberhansli T, Defago G, Haas D. Indole-3-acetic-acid (IAA) synthesis in the biocontrol strain CHA0 of Pseudomonas fluorescens–role of tryptophan side-chain oxidase. J. Gen. Microbiol. 1991; 137: 2273–2279. doi: 10.1099/00221287-137-10-2273 1663150
12. Robinson M, Riov J, Sharon A Indole-3-acetic acid biosynthesis in Collectotrichum gloeosporioides f. sp. aeschynomene. Appl. Environ. Microbiol. 1998; 64, 5030–5032. 9835603
13. Chung KR, Tzeng DD. Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustilago esculenta. J. Biol. Sci. 2004; 4: 744–750. https://doi.org/0.3923/jbs.2004.744.750
14. Shilts T, Ertürk Ü, Patel NJ, Chung KR. Physiological regulation of biosynthesis of Indole-3 -acetic acid and other indole derivatives by the citrus fungal pathogen Collectotrichum acutatum. J. Biol. Sci. 2005; 5: 205–210.
15. Tsavkelova E, Oeser B, Oren-young L, Israeli M, Sasson Y, Tudzynski B, et al. Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fungal Genet. Biol. 2012; 49: 48–57. doi: 10.1016/j.fgb.2011.10.005 22079545
16. Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S. Indole-3-acetic acid biosynthetic pathways in the basidiomycetous yeast Rhodosporidium paludigenum. Arch. Microbiol. 2016; 198: 429–437. doi: 10.1007/s00203-016-1202-z 26899734
17. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N. Working with mycorrhizas in forestry and agriculture. ACIAR Monograph. Camberra, 1996.
18. Ramachela K, Theron JM. Effect of ectomycorrhizal fungi in the protection of Uapaca kirkiana seedlings against root pathogens in Zimbabwe. Southern For. 2010; 72: 37–45. https://doi.org/10.2989/20702620.2010.482343
19. Makita N, Hirano Y, Yamanaka T, Yoshimura K, Kosugi Y. Ectomycorrhizal-fungal colonization induces physio-morphological change in Quercus serrata leaves and roots. J. Plant Nutr. Soil Sci. 2012; 175: 900–906. https://doi.org/10.1002/jpln.201100417
20. Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, et al. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 2009; 154: 1991–2005. doi: 10.1104/pp.109.147231 19854859
21. Luo ZB, Janz D, Jiang X, Gobel C, Wildhagen H, Tan Y, et al. Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol. 2009; 151: 1902–1917. doi: 10.1104/pp.109.143735 19812185
22. Gay G, Debaud C. Genetic study on indole-3-acetic acid production by ectomycorrhizal Hebeloma species: inter- and intraspecific variability in homo- and dikaryotic mycelia. Appl. Microbiol. Biotechnol. 1987; 26: 141–146.
23. Barker SJ, Tagu D. The roles of auxins and cytokinins in mycorrhizal symbioses. J. Plant. Growth Regul. 2000; 19: 144–154. doi: 10.1007/s003440000021 11038224
24. Niemi K, Vuorinen T, Ernstsen A, Häggman H. Ectomycorrhizal fungi and exogenous auxins influence root and mycorrhiza formation of Scots pine hypocotyl cuttings in vitro. Tree Physiol. 2002; 22: 1231–1239. doi: 10.1093/treephys/22.17.1231 12464576
25. Gay G, Rouillon R, Bernillon J, Favre-Bonvin J. IAA biosynthesis by the ectomycorrhizal fungus Hebeloma hiemale as affected by different precursors. Can. J. Bot. 1989; 67: 2235–2239.
26. Bartel B. Auxin biosynthesis. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 1997; 48: 51–66. doi: 10.1146/annurev.arplant.48.1.51 15012256
27. Frankenberger WTJ, Poth M. Biosynthesis of indole-3-acetic acid by the pine ectomycorrhizal fungus Pisolithus tinctorius. Appl. Environ. Microbiol. 1987; 53: 2908–2913. 16347506
28. Splivallo R, Fischer U, Göbel C, Feussner I, Karlovsky P. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol. 2009; 150: 2018–2029. doi: 10.1104/pp.109.141325 19535471
29. Kumla J, Suwannarach N, Bussaban B, Matsui K, Lumyong S. Indole-3-acetic acid production, solubilization of insoluble metal minerals and metal tolerance of some sclerodermatiod fungi collected from northern Thailand. Ann. Microbiol. 2014; 64: 707–720. https://doi.org/10.1007/s13213-013-0706-x
30. Tsavkelova EA, Cherdyntseva TA, Botina SG, Netrusov AI. Bacteria associated with orchid roots and microbial production of auxin. Microbiol Res. 2007; 162: 69–76. doi: 10.1016/j.micres.2006.07.014 17140781
31. Libbert E, Risch H. Interactions between plants and epiphytic bacteria regarding their auxin metabolism. V. Isolation and identification of the IAA-producing and destroying bacteria from pea plants. Physiol. Plantar. 1969; 22: 51–58.
32. Numponsak T, Kumla J, Suwannarach N, Matsui K, Lumyong S. Biosynthetic pathway and optimal conditions for the production of indole-3-acetic acid by an endophytic fungus, Colletotrichum fructicola CMU-A109. PLoS One. 2018; 13: e0205070. doi: 10.1371/journal.pone.0205070 30335811
33. Ehmann A. The van Urk-Salkowski reagent-a sensitive and specific chromogenic reagent for silica gel thin-layer chromatographic detection and identification of indole derivatives. J. Chromatogr.1997; 132: 267–276.
34. Ahmad F, Ahmad I, Khan MS. Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk. J. Biol. 2005; 29: 29–34.
35. Carreño-Lopez R, Campos-Reales N, Elmerich C, Baca BE. Physiological evidence for differently regulated tryptophan dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilense. Mol. Gen. Genet. 2000; 264: 521–530. doi: 10.1007/s004380000340 11129057
36. Rudawska M, Kieliszewska-Rokicka B. Mycorrhizal formation by Paxillus involutus in relation to their IAA-synthesizing activity. New Phytol. 1997; 137: 509–517.
37. Karabaghli C, Frey-Klett P, Sotta B, Bonnet M, Tacon FL. In vitro effects of Laccaria bicolor S238N and Pseudomonas fluorescens strain BBc6 on rooting of de-rooted shoot hypocotyls of Norway spruce. Tree Physiol. 1998; 18: 103–111. doi: 10.1093/treephys/18.2.103 12651394
38. Gay G, Normand L, Marmeisse R, Sotta B, Debaud JC. Auxin overproducer mutants of Hebeloma cylindrosporum Romagnesi have increased mycorrhizal activity. New Phytol. 1994; 128: 645–657.
39. Strelczyck E, Pokojska-Burdziej A (1984) Production of auxins and gibberellin-like substances by mycorrhizal fungi, bacteria and actinomycetes isolated from soil and the mycorrhizosphere of pine (Pinus sylvestris L.). Plant and Soil. 1984; 81:185–194.
40. Sarjala T, Niemi K, Häggman H. Mycorrhiza formation is not needed for early growth induction and growth-related changes in polyamines in Scots pine seedlings in vitro. Plant Physiol. Biochem. 2010; 48: 596–601. doi: 10.1016/j.plaphy.2010.01.022 20188581
41. Ditengou FA, Béguiristain T, Lapeyrie F. Root hair elongation is inhibited by hypaphorine, the indole alkaloid from the ectomycorhizal fungus Pisolithus tinctorius, and restored by indole-3-acetic acid. Planta. 2000; 211: 722–728. doi: 10.1007/s004250000342 11089686
42. Sardar P, Kempken F. Characterization of indole-3-pyruvic acid pathway-mediated biosynsthesis od auxin in Neurospora crassa. PLoS One 2018; 13: e0192293. doi: 10.1371/journal.pone.0192293 29420579.
43. Costacurta A, Keijers V, Vanderleyden J. Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3-pyruvate decarboxylase gene. Mol. Gen. Genet. 1994; 243: 463–472. doi: 10.1007/bf00280477 8202090
44. Minamisawa K, Ogawa K, Fukuhara H, Koga J. Indolepyruvate pathway for indole-3-acetic acid biosynthesis in Bradyrhizobium elkanii. Plant Cell Physiol. 1996; 37: 449–453. https://doi.org/10.1093/oxfordjournals.pcp.a028966
45. Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW. Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol. Plant Pathol. 2008; 9: 339–355. doi: 10.1111/j.1364-3703.2008.00470.x 18705875
46. Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A. Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol. 2012; 196: 520–534. doi: 10.1111/j.1469-8137.2012.04275.x 22924530
47. Szkop M, Bielawski W. A simple method for simultaneous RP-HPLC determination of indolic compounds related to bacterial biosynthesis of indole-3-acetic acid. Antonie van Leeuwenhoek. 2013; 103: 683–691. doi: 10.1007/s10482-012-9838-4 23111785
48. Rodrigues EP, Soares CP, Galvão PG, Imada EL, Simões-Araújo JL, Rouws LF, et al. Identification of genes involved in indole-3-acetic acid biosynthesis by Gluconacetobacter diazotrophicus PAL5 strain using transposon mutagenesis. Front. Microbiol. 2016; 7: 1527. doi: 10.3389/fmicb.2016.01527 27774087
49. Imada EL, dos Santos AAPR, de Oliveira ALM, Hungria M, Rodrigues EP. Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Res. Microbiol. 2016; 168: 283–292. doi: 10.1016/j.resmic.2016.10.010 27845247
50. Tomaszewski M, Wojciechowska B. The role of growth regulators released by fungi in pine mycorrhizae. Hirokawa Publishing. Tokyo, 1975.
51. Chutima R, Lumyong S. (2012). Production of indole-3-acetic acid by Thai native orchid-associated fungi. Symbiosis. 2012; 56: 35–44. https://doi.org/10.1007/s13199-012-0158-2
52. Suwannarach N., Kumla J., Matsui K. and Lumyong S. (2015). Characterization and efficacy of Muscodor cinnamomi in promoting plant growth and controlling Rhizoctonia root rot in tomatoes. Biol. Control. 90, 25–33. https://doi.org/10.1016/j.biocontrol.2015.05.008
53. Bose A, Shah D, Keharia H. Production of indole-3-acetic-acid (IAA) by white rot fungus Pleurotus ostreatus under submerged condition of Jatropha seedcake. Mycology. 2014; 4: 103–111. https://doi.org/10.1080/21501203.2013.823891
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