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Arbuscular mycorrhiza increase artemisinin accumulation in Artemisia annua by higher expression of key biosynthesis genes via enhanced jasmonic acid levels
Abstract
It is becoming increasingly evident that the formation of arbuscular mycorrhiza (AM) enhances secondary metabolite production in shoots. Despite mounting evidence, relatively little is known about the underlying mechanisms. This study suggests that increase in artemisinin concentration in Artemisia annua colonized by Rhizophagus intraradices is due to altered trichome density as well as transcriptional patterns that are mediated via enhanced jasmonic acid (JA) levels. Mycorrhizal (M) plants had higher JA levels in leaf tissue that may be due to induction of an allene oxidase synthase gene (AOS), encoding one of the key enzymes for JA production. Non-mycorrhizal (NM) plants were exogenously supplied with a range of methyl jasmonic acid concentrations. When leaves of NM and M plants with similar levels of endogenous JA were compared, these matched closely in terms of shoot trichome density, artemisinin concentration, and transcript profile of artemisinin biosynthesis genes. Mycorrhization increased artemisinin levels by increasing glandular trichome density and transcriptional activation of artemisinin biosynthesis genes. Transcriptional analysis of some rate-limiting enzymes of mevalonate and methyl erythritol phosphate (MEP) pathways revealed that AM increases isoprenoids by induction of the MEP pathway. A decline in artemisinin concentration in shoots of NM and M plants treated with ibuprofen (an inhibitor of JA biosynthesis) further confirmed the implication of JA in the mechanism of artemisinin production.
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“Mandal et al. (2015) showed that A. annua mutualism with AM fungus Rhizophagus intraradices results in increased artemisinin accumulation due to enhanced expression of certain artemisinin biosynthesis genes, namely ADS, CYP71AV1, ALDH1 and DBR2 mediated through enhanced JA levels, most probably due to stimulation of the allene oxide synthase gene.”
From Enhancing artemisinin content in and delivery from Artemisia annua: a review of alternative, classical, and transgenic approaches (2021) · cites this paper as Mandal et al. 2015
In the citing paper
“The mycorrhizal infection increased glandular trichome density and transcriptional activation of artemisinin biosynthesis genes.”
From Enhancing artemisinin content in and delivery from Artemisia annua: a review of alternative, classical, and transgenic approaches (2021) · cites this paper as Mandal et al. 2015
Citations
Cites
A formaldehyde - glutaraldehyde fixative of high osmolarity for use in electron microscopy
Karnovsky, M. J., & Karnovsky, M. J. (1965) · The Journal of Cell Biology · Cited by 9,412
Phillips, J. M., & Hayman, D. S. (1970) · Transactions of the British Mycological Society · doi:10.1016/s0007-1536(70)80110-3 · Cited by 8,587
AN EVALUATION OF TECHNIQUES FOR MEASURING VESICULAR ARBUSCULAR MYCORRHIZAL INFECTION IN ROOTS
Giovannetti, M., & Mosse, B. (1980) · New Phytologist · doi:10.1111/j.1469-8137.1980.tb04556.x · Cited by 5,925
A formaldehyde - glutaraldehyde fixative of high osmolarity for use in electron microscopy
Karnovsky, M. J. (1965) · The Journal of Cell Biology · Cited by 5,882
Chemical analysis of ecological materials.
Allen, S. E. (1974) · Blackwell Scientific Publications eBooks · Cited by 4,375
Production of the antimalarial drug precursor artemisinic acid in engineered yeast
Ro, D.-K., Paradise, E. M., Ouellet, M., Fisher, K. J., Newman, K. L., Ndungu, J. M., Ho, K. A., Eachus, R. A., Ham, T. S., Kirby, J., et al. (2006) · Nature · doi:10.1038/nature04640 · Cited by 2,805
Wasternack, C., & Hause, B. (2013) · Annals of Botany · doi:10.1093/aob/mct067 · Cited by 2,629
Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi
Akiyama, K., Matsuzaki, K.-I., & Hayashi, H. (2005) · Nature · doi:10.1038/nature03608 · Cited by 2,429
Elicitor signal transduction leading to production of plant secondary metabolites
Zhao, J. H., Davis, L. C., & Verpoorte, R. (2005) · Biotechnology Advances · doi:10.1016/j.biotechadv.2005.01.003 · Cited by 1,985
Natural products and plant disease resistance
Dixon, R. A. (2001) · Nature · doi:10.1038/35081178 · Cited by 1,796
Secondary metabolites in plant defence mechanisms
BENNETT, R. N., & WALLSGROVE, R. M. (1994) · New Phytologist · doi:10.1111/j.1469-8137.1994.tb02968.x · Cited by 1,654
Significance of flavonoids in plant resistance: a review
Treutter, D. (2006) · Environmental Chemistry Letters · doi:10.1007/s10311-006-0068-8 · Cited by 1,260
Gene silencing as an adaptive defence against viruses
Waterhouse, P. M., Wang, M., & Lough, T. J. (2001) · Nature · doi:10.1038/35081168 · Cited by 985
Walker, A. R., Davison, P. A., Bolognesi-Winfield, A. C., James, C. M., Srinivasan, N., Blundell, T. L., Esch, J. J., Marks, M. D., & Gray, J. C. (1999) · The Plant Cell · doi:10.1105/tpc.11.7.1337 · Cited by 984
Yu, Z.-X., Li, J., Yang, C., Hu, W., Wang, L.-J., & Chen, X. (2011) · Molecular Plant · doi:10.1093/mp/ssr087 · Cited by 474
QUANTIFYING VESICULAR‐ARBUSCULAR MYCORRHIZAE: A PROPOSED METHOD TOWARDS STANDARDIZATION *
Biermann, B. J., & Linderman, R. G. (1981) · New Phytologist · doi:10.1111/j.1469-8137.1981.tb01690.x · Cited by 436
Engineering secondary metabolite production in plants
Verpoorte, R., & Memelink, J. (2002) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(02)00308-7 · Cited by 377
Copetta, A., Lingua, G., & Berta, G. (2006) · Mycorrhiza · doi:10.1007/s00572-006-0065-6 · Cited by 355
Jasmonate-inducible gene: what does it mean?
Pauwels, L., Inzé, D., & Goossens, A. (2009) · Trends in Plant Science · doi:10.1016/j.tplants.2008.11.005 · Cited by 351
Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants
Cordoba, E., Salmi, M., & Leon, P. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp190 · Cited by 346
Chappell, J., Wolf, F., Proulx, J., Cuellar, R., & Saunders, C. (1995) · Plant Physiology · doi:10.1104/pp.109.4.1337 · Cited by 335
Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling
Laudert, D., & Weiler, E. W. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00245.x · Cited by 329
Zhang, Y., Teoh, K. H., Reed, D. W., Maes, L., Goossens, A., Olson, D. J. H., Ross, A. R. S., & Covello, P. S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803090200 · Cited by 312
Mercke, P., Bengtsson, M., Bouwmeester, H. J., Posthumus, M. A., & Brodelius, P. E. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2000.1962 · Cited by 283
Lopez-Raez, J. A., Verhage, A., Fernández, I., García, J. M., Azcón‐Aguilar, C., Flors, V., & Pozo, M. J. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq089 · Cited by 272
Kapoor, R., Giri, B., & Mukerji, K. G. (2004) · Bioresource Technology · doi:10.1016/j.biortech.2003.10.028 · Cited by 269
Self-citationTeoh, K. H., Polichuk, D. R., Reed, D. W., & Covello, P. S. (2009) · Botany · doi:10.1139/b09-032 · Cited by 251
Howe, G. A., Lee, G. I., Itoh, A., Li, L., & DeRocher, A. E. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.123.2.711 · Cited by 246
Wallaart, T. E., Bouwmeester, H. J., Hille, J., Poppinga, L., & Maijers, N. C. A. (2001) · Planta · doi:10.1007/s004250000428 · Cited by 242
Maes, L., Van Nieuwerburgh, F. C. W., Zhang, Y., Reed, D. W., Pollier, J., Vande Casteele, S. R. F., Inzé, D., Covello, P. S., Deforce, D. L. D., & Goossens, A. (2011) · New Phytologist · doi:10.1111/j.1469-8137.2010.03466.x · Cited by 240
Induction of Jasmonate Biosynthesis in Arbuscular Mycorrhizal Barley Roots,
Hause, B., Maier, W., Miersch, O., Kramell, R., & Strack, D. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.006007 · Cited by 239
Meixner, C., Ludwig‐Müller, J., Miersch, O., Gresshoff, P. M., Staehelin, C., & Horst Vierheilig, C. (2005) · Planta · doi:10.1007/s00425-005-0003-4 · Cited by 220
Shan, C., & Liang, Z. (2009) · Plant Science · doi:10.1016/j.plantsci.2009.11.002 · Cited by 218
Toussaint, J.-P., Smith, F. A., & Smith, S. E. (2007) · Mycorrhiza · doi:10.1007/s00572-006-0104-3 · Cited by 215
Chemical Analysis of Ecological Materials
Lotse, E. G. (1976) · Soil Science · doi:10.1097/00010694-197606000-00008 · Cited by 212
Kapoor, R., Chaudhary, V., & Bhatnagar, A. K. (2007) · Mycorrhiza · doi:10.1007/s00572-007-0135-4 · Cited by 211
Self-citationWalter, M. H., Fester, T., & Strack, D. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00708.x · Cited by 209
Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae)
Khaosaad, T., Horst Vierheilig, C., Nell, M., Zitterl‐Eglseer, K., & Novak, J. (2006) · Mycorrhiza · doi:10.1007/s00572-006-0062-9 · Cited by 209
Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis
Yoshida, Y., Sano, R., Wada, T., Takabayashi, J., & Okada, K. (2009) · Development · doi:10.1242/dev.030585 · Cited by 208
Morandi, D. (1996) · Plant and Soil · doi:10.1007/bf02257529 · Cited by 206
Bruinsma, M., Posthumus, M. A., Mumm, R., Mueller, M. J., van Loon, J. J. A., & Dicke, M. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp101 · Cited by 194
In vivo transformations of dihydroartemisinic acid in Artemisia annua plants
Brown, G. D., & Sy, L.-K. (2004) · Tetrahedron · doi:10.1016/j.tet.2003.11.070 · Cited by 183
Gupta, M. L., Prasad, A., Ram, M., & Kumar, S. (2002) · Bioresource Technology · doi:10.1016/s0960-8524(01)00109-2 · Cited by 170
Self-citationTowler, M. J., & Weathers, P. J. (2007) · Plant Cell Reports · doi:10.1007/s00299-007-0420-x · Cited by 170
Maucher, H. P., Hause, B., Feußner, I., Ziegler, J., & Wasternack, C. H. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00669.x · Cited by 169
The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms
Hause, B., & Schaarschmidt, S. (2009) · Phytochemistry · doi:10.1016/j.phytochem.2009.07.003 · Cited by 166
Kapoor, R., Giri, B., & Mukerji, K. G. (2002) · World Journal of Microbiology and Biotechnology · doi:10.1023/a:1015522100497 · Cited by 158
Self-citationIsoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots
Strack, D., & Fester, T. (2006) · New Phytologist · doi:10.1111/j.1469-8137.2006.01837.x · Cited by 156
Artemisinin biosynthesis in growing plants of Artemisia annua. A 13CO2 study
Schramek, N., Wang, H., Römisch-Margl, W., Keil, B., Radykewicz, T., Winzenhörlein, B., Beerhues, L., Bacher, A., Rohdich, F., Gershenzon, J., et al. (2010) · Phytochemistry · doi:10.1016/j.phytochem.2009.10.015 · Cited by 150
Kapoor, R., Giri, B., & Mukerji, K. G. (2002) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.1039 · Cited by 146
Self-citationFloß, D. S., Hause, B., Lange, P. R., Küster, H., Strack, D., & Walter, M. H. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03575.x · Cited by 129
Lipid metabolism in arbuscular mycorrhizal roots of Medicago truncatula
Stumpe, M., Carsjens, J.-G., Stenzel, I., Göbel, C., Lang, I., Pawlowski, K., Hause, B., & Feußner, I. (2005) · Phytochemistry · doi:10.1016/j.phytochem.2005.01.020 · Cited by 129
Signalling in Arbuscular Mycorrhiza: Facts and Hypotheses
Vierheilig, H., & Piché, Y. (2002) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-5235-9_3 · Cited by 118
Torelli, A., Trotta, A., Acerbi, L., Arcidiacono, G., Berta, G., & Branca, C. (2000) · Plant and Soil · doi:10.1023/a:1026430019738 · Cited by 113
Hans, J., Hause, B., Strack, D., & Walter, M. H. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.032342 · Cited by 113
Rapparini, F., Llusià, J., & Peñuelas, J. (2008) · Plant Biology · doi:10.1055/s-2007-964963 · Cited by 112
Biochemistry and Physiology of Lower Terpenoids
Loomis, W. D., & Croteau, R. (1973) · Recent advances in phytochemistry · doi:10.1016/b978-0-12-612406-4.50012-7 · Cited by 106
Mandal, S., Evelin, H., Giri, B., Singh, V. P., & Kapoor, R. (2013) · Applied Soil Ecology · doi:10.1016/j.apsoil.2013.07.003 · Cited by 102
Self-citationIn vivo transformations of artemisinic acid in Artemisia annua plants
Brown, G. D., & Sy, L.-K. (2007) · Tetrahedron · doi:10.1016/j.tet.2007.06.062 · Cited by 100
Wang, H., Ma, C., Li, Z., Ma, L., Wang, H., Ye, H., Xu, G., & Liu, B. (2009) · Industrial Crops and Products · doi:10.1016/j.indcrop.2009.10.008 · Cited by 98
Weathers, P. J., Elkholy, S., & Wobbe, K. K. (2006) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1079/ivp2006782 · Cited by 97
Ferreira, J. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf063017v · Cited by 83
Landgraf, R., Schaarschmidt, S., & Hause, B. (2012) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2012.02495.x · Cited by 81
Caretto, S., Quarta, A., Durante, M., Nisi, R., Paolis, A. D., Blando, F., & Mita, G. (2010) · Plant Biology · doi:10.1111/j.1438-8677.2009.00306.x · Cited by 79
Morone-Fortunato, I., & Avato, P. (2008) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-008-9353-5 · Cited by 78
Manthey, J. A., Buslig, B. S., & Baker, M. E. (2002) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-5235-9_1 · Cited by 74
Henkes, G. J., Thorpe, M. R., Minchin, P. E. H., Schurr, U., & Röse, U. S. R. (2008) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2008.01828.x · Cited by 67
Morcillo, R. J. L., Angel, J., Martin-Rodriguez, Horst Vierheilig, C., Ocampo, J. A., & García‐Garrido, J. M. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers010 · Cited by 65
HMG-CoA reductase limits artemisinin biosynthesis and accumulation in Artemisia annua L. plants
Ram, M., Khan, M. A., Jha, P., Khan, S., Kiran, U., Ahmad, M. M., Javed, S., & Abdin, M. Z. (2010) · Acta Physiologiae Plantarum · doi:10.1007/s11738-010-0470-5 · Cited by 59
Self-citationMatsuura, H., Aoi, A., Satou, C., Nakaya, M., Masuta, C., & Nabeta, K. (2008) · Plant Growth Regulation · doi:10.1007/s10725-008-9347-7 · Cited by 43
Liu, S., Tian, N., Li, J., Huang, J., & Liu, Z. (2009) · Planta Medica · doi:10.1055/s-0029-1185809 · Cited by 37
Lu, X., Zhang, F., Shen, Q., Jiang, W., Pan, Q., Lv, Z., Yan, T., Fu, X., Wang, Y., Qian, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091741 · Cited by 35
Qu, H., Christensen, K. B., Fretté, X. C., Tian, F., Rantanen, J., & Christensen, L. P. (2010) · Organic Process Research & Development · doi:10.1021/op1000176 · Cited by 12
Lu, X., Zhang, F., Jiang, W., Lin, X., Chen, Y., Shen, Q., Wang, T., Wu, S., Sun, X., & Tang, K. (2011) · Molecular Biology Reports · doi:10.1007/s11033-011-0976-y · Cited by 9
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Metadata
- Authors
- Mandal, S., Upadhyay, S., Wajid, S., Ram, M., Jain, D. C., Singh, V. P., Abdin, M. Z., & Kapoor, R.
- Affiliations
- University of Delhi (IN)
- Jamia Hamdard (IN)
- Ipca Laboratories (India) (IN)
- Corresponding author
- Kapoor, Rupam
- Venue
- Mycorrhiza
- Published
- 2014-11-05
- Volume
- 25
- Issue
- 5
- Pages
- 345-357
- ISSN
- 0940-6360 (ISSN-L)
- 1432-1890
- OpenAlex
- W2009545804
- Cited by
- 111
- References
- 74
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 8 · 2023: 13 · 2022: 26 · 2021: 11 · 2020: 8 · 2019: 4 · 2018: 12 · 2017: 8 · 2016: 5 · 2015: 6
- FWCI
- 2.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Mycorrhiza (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycorrhizal Fungi and Plant Interactions
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Keywords
- arbuscular mycorrhizal symbiosis, artemisinin biosynthesis, Artemisia annua, Glomus intraradices, jasmonic acid, glandular trichomes, trichome density, allene oxide synthase, methyl jasmonic acid, mevalonate pathway, methylerythritol phosphate pathway, terpenoids, secondary metabolite production, gene expression, ibuprofen
- MeSH terms
- Cyclopentanes, Plant Proteins, Gene Expression Regulation, Plant, Plant Leaves, Plant Roots, Intramolecular Oxidoreductases, Artemisia annua, Artemisinins, Mycorrhizae, Biosynthetic Pathways, Oxylipins
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