Fungal endophytes promote the accumulation of Amaryllidaceae alkaloids in Lycoris radiata.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
05
09
2019
accepted:
20
02
2020
pubmed:
25
2
2020
medline:
15
12
2020
entrez:
25
2
2020
Statut:
ppublish
Résumé
Lycoris radiata is a main source of Amaryllidaceae alkaloids; however, the low content of these alkaloids in planta remains a limit to their pharmaceutical development and utilization. The accumulation of secondary metabolites can be enhanced in plants inoculated with fungal endophytes. In this study, we analysed the diversity of culturable fungal endophytes in different organs of L. radiata. Then, by analysing the correlation between the detectable rate of each fungal species and the content of each tested alkaloid, we proposed several fungal candidates implicated in the increase of alkaloid accumulation. This was verified by inoculating these candidates to L. radiata plants. Based on the results of two independent experiments conducted in May 2018 and October 2019, the individual inoculation of nine fungal endophytes significantly increased the total content of the tested alkaloids in the entire L. radiata plants. This is the first study in L. radiata to show that fungal endophytes are able to improve the accumulation of various alkaloids. Therefore, our results provide insights into a better understanding of interactions between plants and fungal endophytes and suggest an effective strategy for enhancing the alkaloid content in the cultivation of L. radiata.
Identifiants
pubmed: 32090436
doi: 10.1111/1462-2920.14958
doi:
Substances chimiques
Amaryllidaceae Alkaloids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1421-1434Subventions
Organisme : National Natural Science Foundation of China
ID : 31572151
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31600074
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31800427
Pays : International
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20180318
Pays : International
Organisme : Open Fund of Jiangsu Key Laboratory for the Research and Utilization of Plant Resources
ID : JSPKLB201926
Pays : International
Informations de copyright
© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Aly, A.H., Debbab, A., and Proksch, P. (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90: 1829-1845.
Bednarek, P. (2012) Chemical warfare or modulators of defence responses-the function of secondary metabolites in plant immunity. Curr Opin Plant Biol 15: 407-414.
Berkov, S., Bastida, J., Viladomat, F., and Codina, C. (2011) Development and validation of a GC-MS method for rapid determination of galanthamine in Leucojum aestivum and Narcissus ssp: a metabolomic approach. Talanta 83: 1445-1465.
Biggs, A.R. (1995) Detection of latent infections in apple fruit with paraquat. Plant Dis 79: 1062-1067.
Camehl, I., Sherameti, I., Venus, Y., Bethke, G., Varma, A., Lee, J., and Oelmüller, R. (2010) Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 185: 1062-1073.
Chen, F., Ren, C.G., Zhou, T., Wei, Y.J., and Dai, C.C. (2016) A novel exopolysaccharide elicitor from endophytic fungus Gilmaniella sp. AL12 on volatile oils accumulation in Atractylodes lancea. Sci Rep-UK 6: 34735.
Clay, K., Shearin, Z.R.C., Bourke, K.A., Bickford, W.A., and Kowalshi, K.P. (2016) Diversity of fungal endophytes in non-native Phragmites australis in the Great Lakes. Biol Invasions 18: 2703-2716.
Cui, J.L., Guo, T.T., Ren, Z.X., Zhang, N.S., and Wang, M.L. (2015) Diversity and antioxidant activity of culturable endophytic fungi from Alpine plants of Rhodiola crenulata, R. angusta, and R. sachalinensis. PloS One 10: e0118204.
Demers, J.E., Gugino, B.K., and Jiménez-Gasco, M.M. (2015) Highly diverse endophytic and soil Fusarium oxysporum populations associated with field-grown tomato plants. Appl Environ Microbiol 81: 81-90.
Ding, Y., Qu, D., Zhang, K.M., Cang, X.X., Kou, Z.N., Xiao, W., and Zhu, J.B. (2017) Phytochemical and biological investigations of Amaryllidaceae alkaloids: a review. J Asian Nat Prod Res 19: 53-100.
Gleeson, D., McDermott, F., and Clipson, N. (2006) Structural diversity of bacterial communities in a heavy metal mineralized granite outcrop. Environ Microbiol 8: 383-393.
Griffin, E.A., and Carson, W.P. (2018) Tree endophytes: cryptic drivers of tropical forest diversity. In Endophytes of Forest Trees: Biology and Applications, 2nd ed, Pirttila, A.M., and Frank, A.C. (eds). Switzerland: Springer International Publishing AG, pp. 63-103.
Hammer, Ø., Harper, D.A.T., and Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 1-9.
Hao, G., Du, X., Zhao, F., and Ji, H. (2010) Fungal endophyte-induced abscisic acid is required for flavonoid accumulation in suspension cells of Ginkgo biloba. Biotechnol Lett 32: 305-314.
Hiruma, K., Gerlach, N., Sacristán, S., Nakano, R.T., Hacquard, S., Kracher, B., et al. (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165: 464-474.
Hsu, P.S. (1994) Synopsis of the genus Lycoris (Amaryllidaceae). SIDA 16: 301-331.
Huang, W.Y., Cai, Y.Z., Hyde, K.D., Corke, H., and Sun, M. (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33: 61-75.
Iqbal, Z., Nasir, H., Hiradate, S., and Fujii, Y. (2006) Plant growth inhibitory activity of Lycoris radiata herb. And the possible involvement of lycorine as an allelochemical. Weed Biol Manage 6: 221-227.
Joosten, L., and van Veen, J.A. (2011) Defensive properties of pyrrolizidine alkaloids against microorganisms. Phytochem Rev 10: 127-136.
Karasov, T.L., Chae, E., Herman, J.J., and Bergelson, J. (2017) Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29: 666-680.
Kilgore, W.B., and Kutchan, T.M. (2016) The Amaryllidaceae alkaloids: biosynthesis and methods for enzyme discovery. Phytochem Rev 15: 317-337.
Kumar, D.S.S., and Hyde, K.D. (2004) Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Divers 17: 69-90.
Liu, K., Tang, C.F., Zhou, S.B., Wang, Y.P., Zhang, D., Wu, G.W., and Chang, L.L. (2012) Comparison of the photosynthetic characteristics of four Lycoris species with leaf appearing in autumn under field conditions. Photosynthetica 50: 570-576.
Liu, W., and Reinscheid, U.M. (2004) Camptothecin-resistant fungal endophytes of Camptotheca acuminata. Mycol Prog 3: 189-192.
Lubbe, A., Gude, H., Verpoorte, R., and Choi, Y.H. (2013) Seasonal accumulation of major alkaloids in organs of pharmaceutical crop Narcissus Carlton. Phytochemistry 88: 43-53.
Luo, Y.L., Yang, S., Zhao, Z.M., Peng, F., and Li, Y.Y. (2011) Isolation and identification of a galanthamine-producing endophytic fungus from Lycoris aurea bulbs. Northwest Pharm J 26: 241-243.
Matsuura, H.N., and Fett-Neto, A.G. (2017) Plant alkaloids: main features, toxicity, and mechanisms of action. In Plant Toxins, Gopalakrishnakone, P., Carlini, C., and Ligabue-Braun, R. (eds). Dordrecht, Netherlands: Springer, pp. 243-261.
Mishra, A., Gond, S.K., Kumar, A., Sharma, V.K., Verma, S.K., Kharwar, R.N., and Sieber, T.N. (2012) Season and tissue type affect fungal endophyte communities of the India medicinal plant Tinospora cordifolia more strongly than geographic location. Microb Ecol 64: 388-398.
Mu, H.M., Wang, R., Li, X.D., Jiang, Y.M., Peng, F., and Xia, B. (2010) Alkaloid accumulation in different parts and ages of Lycoris chinensis. Z Naturforsch C 65: 458-462.
Oliveros, J.C. (2007-2015) Venny. An interactive tool for comparing lists with Venn's diagrams. URL http://bioinfogp.cnb.csic.es/tools/venny/index.html.
Pandey, S.S., Singh, S., Babu, C.S.V., Shanker, K., Srivastava, N.K., Shukla, A.K., and Kalra, A. (2016) Fungal endophytes of Catharanthus roseus enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis. Sci Rep-UK 6: 26583.
Potshangbam, M., Devi, S.I., Sahoo, D., and Strobel, G.A. (2017) Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Front Microbiol 8: 325.
Pusztahelyi, T., Holb, I.J., and Pócsi, I. (2015) Secondary metabolites in fungus-plant interactions. Front Plant Sci 6: 573.
Rai, M., and Agarkar, G. (2014) Plant-fungal interactions: what triggers the fungi to switch among lifestyles? Crit Rev Microbiol 42: 428-438.
Reis, A., Magne, K., Massot, S., Tallini, L.R., Scopel, M., Bastida, J., et al. (2019) Amaryllidaceae alkaloids: identification and partial characterization of montanine production in Rhodophiala bifida plant. Sci Rep-UK 9: 8471.
Rodriguez, R., and Redman, R. (2008) More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59: 1109-1114.
Saunders, M., and Kohn, L.M. (2009) Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytol 182: 229-238.
Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., et al. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109: 6241-6246.
Schulz, B., and Boyle, C. (2005) The endophytic continuum. Mycol Res 109: 661-686.
Sessa, L., Abreo, E., and Lupo, S. (2018) Diversity of fungal latent pathogens and true endophytes associated with fruit trees in Uruguay. J Phytopathol 166: 633-647.
Shi, Y.J., Wang, J., Jin, X., Wang, Z.L., Pan, D.D., Zhuang, Y., et al. (2019) Effects of intercropping of wheat on composition of cucumber seedling rhizosphere fungal community. Allelopathy J 46: 241-249.
Shitan, N., Bazin, I., Dan, K., Obata, K., Kigawa, K., Ueda, K., et al. (2003) Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc Natl Acad Sci U S A 100: 751-756.
Singh, A., and Desgagné-Penix, I. (2014) Biosynthesis of the Amaryllidaceae alkaloids. Plant Sci Today 1: 114-120.
Sun, B., Wang, P., Wang, R., Li, Y., and Xu, S. (2018) Molecular cloning and characterization of a meta/para-O-methyltransferase from Lycoris aurea. Int J Mol Sci 19: 1911.
Takos, A.M., and Rook, F. (2013) Towards a molecular understanding of the biosynthesis of Amaryllidaceae alkaloids in support of their expanding medical use. Int J Mol Sci 14: 11713-11741.
Tian, Y.Q., Zhang, C.Y., and Guo, M.Q. (2015) Comparative analysis of Amaryllidaceae alkaloids from three Lycoris species. Molecules 20: 21854-21869.
Valles-Colomer, M., Falony, G., Darzi, Y., Tigchelaar, E.F., Wang, J., Tito, R.Y., et al. (2019) The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol 4: 623-632.
Wang, H.M., Chen, P., and Tang, M. (2014) Progress in asymmetric synthesis of galanthamine-type alkaloids. Chin J Org Chem 34: 852-864.
Wang, L., Yin, Z.Q., Cai, Y., Zhang, X.Q., Yao, X.S., and Ye, W.C. (2010) Amaryllidaceae alkaloids from the bulbs of Lycoris radiata. Biochem Syst Ecol 38: 444-446.
Wang, X.H., Zhang, C.H., Yang, L.L., and Gomes-Laranjo, J. (2011) Production of dragon's blood in Dracaena cochinchinensis plants by inoculation of Fusarium proliferatum. Plant Sci 180: 292-299.
Wearn, J.A., Sutton, B.C., Morley, N.J., and Gange, A.C. (2012) Species and organ specificity of fungal endophytes in herbaceous grassland plants. J Ecol 100: 1085-1092.
Wikee, S., Lombard, L., Crous, P.W., Nakashima, C., Motohashi, K., Chukeatirote, E., et al. (2013) Phyllosticta capitalensis, a widespread endophyte of plants. Fungal Divers 60: 91-105.
Yang, S., Nan, X.H., Lu, Y.B., and Peng, F. (2010) Study on isolation and anti-microbial activity of endophyte in Lycoris aurea herb. J TCM Univ Hunan 30: 78-80.
Yang, T., Weisenhorn, P., Gilbert, J.A., Ni, Y., Sun, R., Shi, Y., and Chu, H. (2016) Carbon constrains fungal endophyte assemblages along the timberline. Environ Microbiol 18: 2455-2469.
Yuan, J., Sun, K., Deng-Wang, M.Y., and Dai, C.C. (2016b) The mechanism of ethylene signaling induced by endophytic fungus Gilmaniella sp. AL12 mediating sesquiterpenoids biosynthesis in Atractylodes lancea. Front Plant Sci 7: 361.
Yuan, J., Zhang, W., Sun, K., Tang, M.J., Chen, P.X., Li, X., and Dai, C.C. (2019) Comparative transcriptomics and proteomics of Atractylodes lancea in response to endophytic fungus Gilmaniella sp. AL12 reveals regulation in plant metabolism. Front Microbiol 10: 1208.
Yuan, J., Zhou, J.Y., Li, X., and Dai, C.C. (2016a) The primary mechanism of endophytic fungus Gilmaniella sp. AL12 promotion of plant growth and sesquiterpenoid accumulation in Atractylodes lancea. Plant Cell Tissue Organ Cult 125: 571-584.
Zhai, X., Jia, M., Chen, L., Zheng, C.J., Rahman, K., Han, T., and Qin, L.P. (2017) The regulatory mechanism of fungal elicitor-induced secondary metabolite biosynthesis in medical plants. Crit Rev Microbiol 43: 238-261.
Zhang, J., Liu, Y.X., Zhang, N., Hu, B., Jin, T., Xu, H., et al. (2019) NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol 37: 676-684.
Zheng, Y.K., Qiao, X.G., Miao, C.P., Liu, K., Chen, Y.W., Xu, L.H., and Zhao, L.X. (2016) Diversity, distribution and biotechnological potential of endophytic fungi. Ann Microbiol 66: 529-542.
Zhou, J.Y., Sun, K., Chen, F., Yuan, J., Li, X., and Dai, C.C. (2018) Endophytic Pseudomonas induces metabolic flux changes that enhance medicinal sesquiterpenoid accumulation in Atractylodes lancea. Plant Physiol Biochem 130: 473-481.
Zhou, J.Y., Yuan, J., Li, X., Ning, Y.F., and Dai, C.C. (2016) Endophytic bacterium-triggered reactive oxygen species directly increase oxygenous sesquiterpenoid content and diversity in Atractylodes lancea. Appl Environ Microbiol 82: 1577-1585.
Zhou, P., Wu, Z.D., Tan, D.D., Yang, J., Zhou, Q., Zeng, F.R., et al. (2017) Atrichodermones A-C, three new secondary metabolites from the solid culture of an endophytic fungal strain, Trichoderma atroviride. Fitoterapia 123: 18-22.