The Endophytic Fungus Cyanodermella asteris Influences Growth of the Nonnatural Host Plant Arabidopsis thaliana.

Arabidopsis thaliana; Cyanodermella asteris; astins; endophyte; fungus–plant interactions; plant–microbe-interaction; secondary metabolism; volatiles; Plant Growth Regulators; Endophytes; Plant Roots; Arabidopsis; Ascomycota; Physiology; Agronomy and Crop Science; General Medicine

Abstract :

[en] Cyanodermella asteris is a fungal endophyte from Aster tataricus, a perennial plant from the northern part of Asia. Here, we demonstrated an interaction of C. asteris with Arabidopsis thaliana, Chinese cabbage, rapeseed, tomato, maize, or sunflower resulting in different phenotypes such as shorter main roots, massive lateral root growth, higher leaf and root biomass, and increased anthocyanin levels. In a variety of cocultivation assays, it was shown that these altered phenotypes are caused by fungal CO2, volatile organic compounds, and soluble compounds, notably astins. Astins A, C, and G induced plant growth when they were individually included in the medium. In return, A. thaliana stimulates the fungal astin C production during cocultivation. Taken together, our results indicate a bilateral interaction between the fungus and the plant. A stress response in plants is induced by fungal metabolites while plant stress hormones induced astin C production of the fungus. Interestingly, our results not only show unidirectional influence of the fungus on the plant but also vice versa. The plant is able to influence growth and secondary metabolite production in the endophyte, even when both organisms do not live in close contact, suggesting the involvement of volatile compounds.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Disciplines :

Biotechnology

Author, co-author :

Jahn, Linda ; Plant Physiology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, Germany

Storm-Johannsen, Lisa; Plant Physiology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, Germany

Seidler, Diana; Plant Physiology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, Germany

Noack, Jasmin; Plant Physiology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, Germany

Gao, Wei; Biopsychology, Faculty of Psychology, Technische Universität Dresden, 01062 Dresden, Germany

Schafhauser, Thomas; Plant Physiology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, Germany ; Interfaculty Institute of Microbiology and Infection Medicine, Microbiology and Biotechnology, Eberhard Karls Universität Tübingen, 72076 Tübingen, Germany

Wohlleben, Wolfgang; Interfaculty Institute of Microbiology and Infection Medicine, Microbiology and Biotechnology, Eberhard Karls Universität Tübingen, 72076 Tübingen, Germany

van Berkel, Willem J H; Laboratory of Biochemistry, Wageningen University Dreijenlaan 3, 6703 HA Wageningen, The Netherlands

Jacques, Philippe ; Université de Liège - ULiège > Département GxABT > Microbial, food and biobased technologies

Kar, Tambi ; Université de Liège - ULiège > TERRA Research Centre > Microbial, food and biobased technologies ; Lipofabrik, Cité Scientifique, Bât. Polytech-Lille, Avenue Langevin 59 655, Villeneuve d'Ascq, France

Piechulla, Birgit; Institute for Biological Science, Biochemistry, University of Rostock, 18059 Rostock, Germany

Ludwig-Müller, Jutta ; Plant Physiology, Faculty of Biology, Technische Universität Dresden, 01062 Dresden, Germany

Language :

English

Title :

The Endophytic Fungus Cyanodermella asteris Influences Growth of the Nonnatural Host Plant Arabidopsis thaliana.

Publication date :

January 2022

Journal title :

Molecular Plant-Microbe Interactions

ISSN :

0894-0282

eISSN :

1943-7706

Publisher :

American Phytopathological Society, United States

Volume :

Issue :

Pages :

49-63

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI-03-21-0072-R

Funders :

ERA-IB
Sächsische Aufbaubank
Institutional Strategy of the University of Tübingen
BMBF - Bundesministerium für Bildung und Forschung
NWO - Netherlands Organisation for Scientific Research

Funding text :

Funding: Financial support was provided by the European Union (European Regional Development Fund, ERA-IB Project Astinprod ERA-IB-15-039) and the Free State of Saxony (S€achsische Aufbaubank grants 100271404 and 100271410). L. Jahn, T. Schafhauser, and J. Ludwig-Muller were funded by the S€achsische Aufbaubank. T. Schafhauser was supported by the Institutional Strategy of the University of Tubingen (Project ZUK63). W. Wohlleben was funded by the Bundesministerium fur Bildung und Forschung (grant 0315934). W. J. H. van Berkel was supported by the Netherlands Organisation for Scientific Research (Project ACTS 053.80.713).

Available on ORBi :

since 31 March 2022

Statistics

Number of views

58 (3 by ULiège)

Number of downloads

34 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abdelaziz, M. E., Kim, D., Ali, S., Fedoroff, N. V., and Al-Babili, S. 2017. The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na+/K+ homeostasis under salt stress conditions. Plant Sci. 263:107-115.
Ali, S., Charles, T. C., and Glick, B. R. 2017. Endophytic phytohormones and their role in plant growth promotion. Pages 89-105 in: Functional Importance of the Plant Microbiome. S. L. Doty, ed. Springer International Publishing, Cham, Switzerland.
Anke, T., Oberwinkler, F., Steglich, W., and Schramm, G. 1977. The strobilurins-New antifungal antibiotics from the basidiomycete Strobilurus tenacellus. J. Antibiot. (Tokyo) 30:806-810.
Arnon, D. I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24:1-15.
Bilal, L., Asaf, S., Hamayun, M., Gul, H., Iqbal, A., Ullah, I., Lee, I.-J., and Hussain, A. 2018. Plant growth promoting endophytic fungi Aspergillus fumigatus TS1 and Fusarium proliferatum BRL1 produce gibberellins and regulates plant endogenous hormones. Symbiosis 76:117-127.
Boyes, D. C., Zayed, A. M., Ascenzi, R., McCaskill, A. J., Hoffman, N. E., Davis, K. R., and Görlach, J. 2001. Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13:1499-1510.
Broekaert, W. F., Delaure, S. L., De Bolle, M. F. C., and Cammue, B. P. A. 2006. The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopathol. 44:393-416.
Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., and Dong, X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57-63.
Casarrubia, S., Sapienza, S., Fritz, H., Daghino, S., Rosenkranz, M., Schnitzler, J.-P., Martin, F., Perotto, S., and Martino, E. 2016. Ecologically different fungi affect Arabidopsis development: Contribution of soluble and volatile compounds. PLoS One 11:e0168236.
Chalker-Scott, L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70:1-9.
Chhabra, S., and Dowling, D. N. 2017. Endophyte-promoted nutrient acquisition: Phosphorus and iron. Pages 21-42 in: Functional Importance of the Plant Microbiome. S. L. Doty, ed. Springer International Publishing, Cham, Switzerland.
Contesto, C., Milesi, S., Mantelin, S., Zancarini, A., Desbrosses, G., Varoquaux, F., Bellini, C., Kowalczyk, M., and Touraine, B. 2010. The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455-1470.
Contreras-Cornejo, H. A., Macias-Rodriguez, L., Cortes-Penagos, C., and Lopez-Bucio, J. 2009. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 149: 1579-1592.
Dobbelaere, S., Croonenborghs, A., Thys, A., Vande Broek, A., and Vanderleyden, J. 1999. Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:153-162.
Dovana, F., Mucciarelli, M., Mascarello, M., and Fusconi, A. 2015. In vitro morphogenesis of Arabidopsis to search for novel endophytic fungi modulating plant growth. PLoS One 10:e0143353.
Dunlap, J. R., Kresovich, S., and McGee, R. E. 1986. The effect of salt concentration on auxin stability in culture media. Plant Physiol. 81:934-936.
Friedrich, L., Vernooij, B., Gaffney, T., Morse, A., and Ryals, J. 1995. Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol. Biol. 29:959-968.
Gamble, R. L., Qu, X., and Schaller, G. E. 2002. Mutational analysis of the ethylene receptor ETR1. Role of the histidine kinase domain in dominant ethylene insensitivity. Plant Physiol. 128:1428-1438.
Gill, S. S., Gill, R., Trivedi, D. K., Anjum, N. A., Sharma, K. K., Ansari, M. W., Ansari, A. A., Johri, A. K., Prasad, R., Pereira, E., Varma, A., and Tuteja, N. 2016. Piriformospora indica: Potential and significance in plant stress tolerance. Front. Microbiol. 7:332.
Gonzalez, M. C., Anaya, A. L., Glenn, A. E., Saucedo-Garcia, A., Macias-Rubalcava, M. L., and Hanlin, R. T. 2007. A new endophytic ascomycete from El Eden Ecological Reserve, Quintana Roo, Mexico. Mycotaxon 101:251.
Gonzalez-Perez, E., Ortega-Amaro, M. A., Salazar-Badillo, F. B., Bautista, E., Douterlungne, D., and Jimenez-Bremont, J. F. 2018. The Arabidopsis-Trichoderma interaction reveals that the fungal growth medium is an important factor in plant growth induction. Sci. Rep. 8:16427.
Halim, V. A., Vess, A., Scheel, D., and Rosahl, S. 2006. The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol. 8:307-313.
Hutner, S. H., Provasoli, L., Schatz, A., and Haskins, C. P. 1950. Some approaches to the study of the role of metals in the metabolism of microorganisms. Proc. Am. Philos. Soc. 94:152-170.
Itokawa, H., Morita, H., Nagashima, S., and Takeya, K. 1994. Cyclic peptides from higher plants. Part 8. Three novel cyclic pentapeptides, astins F, G and H from Aster tataricus. Heterocycles 38:2247-2252.
Jahn, L., Hofmann, U., and Ludwig-Müller, J. 2021. Indole-3-acetic acid is synthesized by the endophyte Cyanodermella asteris by a tryptophan-dependent and -independent way and mediates the interaction with a non-host plant. Int. J. Mol. Sci. 22:2651.
Jahn, L., Schafhauser, T., Pan, S., Weber, T., Wohlleben, W., Fewer, D., Sivonen, K., Flor, L., van Pee, K.-H., Caradec, T., Jacques, P., Huijbers, M. E., Berkel, W. H., and Ludwig-Müller, J. 2017.
Cyanodermella asteris sp. nov. (Ostropales) from the inflorescence axis of Aster tataricus. Mycotaxon 132:107-123.
Jäschke, D., Dugassa-Gobena, D., Karlovsky, P., Vidal, S., and Ludwig-Müller, J. 2010. Suppression of clubroot (Plasmodiophora brassicae) development in Arabidopsis thaliana by the endophytic fungus Acremonium alternatum. Plant Pathol. 59:100-111.
Junker, C., Draeger, S., and Schulz, B. 2012. A fine line-Endophytes or pathogens in Arabidopsis thaliana. Fungal Ecol. 5:657-662.
Kai, M., and Piechulla, B. 2009. Plant growth promotion due to rhizobacterial volatiles-An effect of CO2?. FEBS Lett. 583:3473-3477.
Kishimoto, K., Matsui, K., Ozawa, R., and Takabayashi, J. 2006a. Analysis of defensive responses activated by volatile allo-ocimene treatment in Arabidopsis thaliana. Phytochemistry 67:1520-1529.
Kishimoto, K., Matsui, K., Ozawa, R., and Takabayashi, J. 2006b. Components of C6-aldehyde-induced resistance in Arabidopsis thaliana against a necrotrophic fungal pathogen, Botrytis cinerea. Plant Sci. 170:715-723.
Kishimoto, K., Matsui, K., Ozawa, R., and Takabayashi, J. 2007. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J. Gen. Plant Pathol. 73:35-37.
Kochar, M., Upadhyay, A., and Srivastava, S. 2011. Indole-3-acetic acid biosynthesis in the biocontrol strain Pseudomonas fluorescens Psd and plant growth regulation by hormone overexpression. Res. Microbiol. 162: 426-435.
Lahrmann, U., Ding, Y., Banhara, A., Rath, M., Hajirezaei, M. R., Döhlemann, S., von Wiren, N., Parniske, M., and Zuccaro, A. 2013. Hostrelated metabolic cues affect colonization strategies of a root endophyte. Proc. Natl. Acad. Sci. U.S.A. 110:13965-13970.
Lee, S., Behringer, G., Hung, R., and Bennett, J. 2019. Effects of fungal volatile organic compounds on Arabidopsis thaliana growth and gene expression. Fungal Ecol. 37:1-9.
Lenhard, W., and Lenhard, A. 2016. Calculation of effect sizes. Psychometrica, Bibergau, Germany. http://www.psychometrica.de/effectsize.htlm
Lopez-Bucio, J., Campos-Cuevas, J. C., Hernandez-Calderon, E., Velasquez-Becerra, C., Farias-Rodriguez, R., Macias-Rodriguez, L. I., and Valencia-Cantero, E. 2007. Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 20:207-217.
Ludwig-Müller, J., Auer, S., Jülke, S., and Marschollek, S. 2017. Manipulation of auxin and cytokinin balance during the Plasmodiophora brassicae-Arabidopsis thaliana interaction. Pages 41-60 in: Methods in Molecular Biology. T. Dandekar and M. Naseem, eds. Springer, New York, NY, U.S.A.
Macias-Rubalcava, M. L., Ruiz-Velasco Sobrino, M. E., Melendez-Gonzalez, C., and Hernandez-Ortega, S. 2014. Naphthoquinone spiroketals and organic extracts from the endophytic fungus Edenia gomezpompae as potential herbicides. J. Agric. Food Chem. 62:3553-3562.
Madhu, M., and Hatfield, J. L. 2013. Dynamics of plant root growth under increased atmospheric carbon dioxide. Agron. J. 105:657-669.
MaiMed. 2011. Technical Data Sheet: MaiMed-pore. https://maimed. de/technical-data-sheets/?lang=en
Makino, A., and Mae, T. 1999. Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol. 40:999-1006.
Mancinelli, A. L., and Schwartz, O. M. 1984. The photoregulation of anthocyanin synthesis IX. The photosensitivity of the response in dark and light-grown tomato seedlings. Plant Cell Physiol. 25:93-105.
Mandyam, K. G., Roe, J., and Jumpponen, A. 2013. Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization. Fungal Biol. 117:250-260.
McClure, J. W. 1979. The physiology of phenolic compounds in plants. Pages 525-556 in: Recent Advances in Phytochemistry. T. Swain, J. B.
Harbone, and C. F. Van Sumere, eds. Springer, Boston, MA, U.S.A. Mercier, J., and Manker, D. C. 2005. Biocontrol of soil-borne diseases and plant growth enhancement in greenhouse soilless mix by the volatile-producing fungus Muscodor albus. Crop Prot. 24:355-362.
Minerdi, D., Bossi, S., Maffei, M. E., Gullino, M. L., and Garibaldi, A. 2011. Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol. Ecol. 76:342-351.
Morath, S. U., Hung, R., and Bennett, J. W. 2012. Fungal volatile organic compounds: A review with emphasis on their biotechnological potential. Fungal Biol. Rev. 26:73-83.
Morita, H., Nagashima, S., Shirota, O., Takeya, K., and Itokawa, H. 1993a. Two novel monochlorinated cyclic pentapeptides, astins D and E from Aster tataricus. Chem. Lett. 22:1877-1880.
Morita, H., Nagashima, S., Takeya, K., and Itokawa, H. 1993b. Astins A and B, antitumor cyclic pentapeptides from Aster tataricus. Chem. Pharm. Bull. (Tokyo) 41:992-993.
Morita, H., Nagashima, S., Takeya, K., and Itokawa, H. 1994. A novel cyclic pentapeptide with b-hydroxy-c-chloroproline from Aster tataricus. Chem. Lett. 23:2009-2010.
Morita, H., Nagashima, S., Takeya, K., and Itokawa, H. 1995. Structure of a new peptide, astin J, from Aster tataricus. Chem. Pharm. Bull. (Tokyo) 43:271-273.
Morrison, E. N., Knowles, S., Hayward, A., Thorn, R. G., Saville, B. J., and Emery, R. J. N. 2015. Detection of phytohormones in temperate forest fungi predicts consistent abscisic acid production and a common pathway for cytokinin biosynthesis. Mycologia 107:245-257.
Murashige, T., and Skoog, F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15:473-497.
Nissen, S. J., and Sutter, E. G. 1990. Stability of IAA and IBA in nutrient medium to several tissue culture procedures. HortScience 25:800-802.
Ortiz-Castro, R., Valencia-Cantero, E., and Lopez-Bucio, J. 2008. Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal. Behav. 3:263-265.
Peskan-Berghöfer, T., Shahollari, B., Giong, P. H., Hehl, S., Markert, C., Blanke, V., Kost, G., Varma, A., and Oelmüller, R. 2004. Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol. Plant. 122:465-477.
Piechulla, B., Lemfack, M. C., and Kai, M. 2017. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ. 40:2042-2067.
Piechulla, B., and Schnitzler, J.-P. 2016. Circumvent CO2 effects in volatilebased microbe-plant interactions. Trends Plant Sci. 21:541-543.
Pons, S., Fournier, S., Chervin, C., Becard, G., Rochange, S., Frei Dit Frey, N., and Puech Pages, V. 2020. Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis. PLoS One 15: E0240886.
Proença, D. N., Schwab, S., Vidal, M. S., Baldani, J. I., Xavier, G. R., and Morais, P. V. 2019. The nematicide Serratia plymuthica M24T3 colonizes Arabidopsis thaliana, stimulates plant growth, and presents plant beneficial potential. Braz. J. Microbiol. 50:777-789.
Prusty, R., Grisafi, P., and Fink, G. R. 2004. The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 101:4153-4157.
Rabino, I., and Mancinelli, A. L. 1986. Light, temperature, and anthocyanin production. Plant Physiol. 81:922-924.
Reineke, G., Heinze, B., Schirawski, J., Buettner, H., Kahmann, R., and Basse, C. W. 2008. 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. 9:339-355.
Resende, M. P., Jakoby, I. C. M. C., dos Santos, L. C. R., Soares, M. A., Pereira, F. D., Souchie, E. L., and Silva, F. G. 2014. Phosphate solubilization and phytohormone production by endophytic and rhizosphere Trichoderma isolates of guanandi (Calophyllum brasiliense Cambess). Afr. J. Microbiol. Res. 8:2616-2623.
Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Wei, H.-X., Pare, P. W., and Kloepper, J. W. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100:4927-4932.
Salas-Marina, M. A., Silva-Flores, M. A., Cervantes-Badillo, M. G., Rosales-Saavedra, M. T., Islas-Osuna, M. A., and Casas-Flores, S. 2011. The plant growth-promoting fungus Aspergillus ustus promotes growth and induces resistance against different lifestyle pathogens in Arabidopsis thaliana. J. Microbiol. Biotechnol. 21:686-696.
Schafhauser, T., Jahn, L., Kirchner, N., Kulik, A., Flor, L., Lang, A., Caradec, T., Fewer, D. P., Sivonen, K., van Berkel, W. J. H., Jacques, P., Weber, T., Gross, H., van Pee, K.-H., Wohlleben, W., and Ludwig-Müller, J. 2019. Antitumor astins originate from the fungal endophyte Cyanodermella asteris living within the medicinal plant Aster tataricus. Proc. Natl. Acad. Sci. U.S.A. 116:26909-26917.
Schramm, G., Steglich, W., Anke, T., and Oberwinkler, F. 1978. Antibiotika aus Basidiomyceten, III. Strobilurin A und B, antifungische Stoffwechselprodukte aus Strobilurus tenacellus. Chem. Ber. 111:2779-2784.
Schulz, B., and Boyle, C. 2005. The endophytic continuum. Mycol. Res. 109:661-686.
Shahzad, R., Khan, A. L., Bilal, S., Waqas, M., Kang, S.-M., and Lee, I.-J. 2017. Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environ. Exp. Bot. 136:68-77.
Shao, Y., Ho, C. T., Chin, C. K., Poobrasert, O., Yang, S. W., and Cordell, G. A. 1997a. Asterlingulatosides C and D, cytotoxic triterpenoid saponins from Aster lingulatus. J. Nat. Prod. 60:743-746.
Shao, Y., Ho, C.-T., Chin, C.-K., Rosen, R. T., Hu, B., and Qin, G.-W. 1997b. Triterpenoid saponins from Aster lingulatus. Phytochemistry 44:337-340.
Shi, C.-L., Park, H.-B., Lee, J. S., Ryu, S., and Ryu, C.-M. 2010. Inhibition of primary roots and stimulation of lateral root development in Arabidopsis thaliana by the rhizobacterium Serratia marcescens 90-166 is through both auxin-dependent and -independent signaling pathways. Mol. Cells 29:251-258.
Shirota, O., Morita, H., Takeya, K., Itokawa, H., and Iitaka, Y. 1997. Cytotoxic triterpenes from Aster tataricus. Nat. Med. 51:170-172.
Singh, A., Singh, A., Kumari, M., Rai, M. K., and Varma, A. 2003. Biotechnological importance of Piriformospora indica Verma et al.-A novel symbiotic mycorrhiza-like fungus: An overview. Indian J. Biotechnol. 2:65-75.
Singhal, U., Prasad, R., and Varma, A. 2017. Piriformospora indica (Serendipita indica): The novel symbiont. Pages 349-364 in: Mycorrhiza- Function, Diversity, State of the Art. Publishing. A. Varma, R. Prasad, and N. Tuteja, eds. Springer, Cham, Switzerland.
Sirrenberg, A., Göbel, C., Grond, S., Czempinski, N., Ratzinger, A., Karlovsky, P., Santos, P., Feussner, I., and Pawlowski, K. 2007. Piriformospora indica affects plant growth by auxin production. Physiol. Plant. 131:581-589.
Staswick, P. E., Su, W., and Howell, S. H. 1992. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. U.S.A. 89: 6837-6840.
Strobel, G. A., Dirkse, E., Sears, J., and Markworth, C. 2001. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiol. Read. 147:2943-2950.
Teng, S., Keurentjes, J., Bentsink, L., Koornneef, M., and Smeekens, S. 2005. Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol. 139:1840-1852.
Vadassery, J., Ritter, C., Venus, Y., Camehl, I., Varma, A., Shahollari, B., Novak, O., Strnad, M., Ludwig-Müller, J., and Oelmüller, R. 2008. The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol. Plant-Microbe Interact. 21:1371-1383.
Van der Kooij, L. A. W., De Kok, L. J., and Stulen, I. 1999. Biomass production and carbohydrate content of Arabidopsis thaliana at atmospheric CO2 concentrations from 390 to 1680 μl l-1. Plant Biol. 1:482-486.
Van Dingenen, J., Antoniou, C., Filippou, P., Pollier, J., Gonzalez, N., Dhondt, S., Goossens, A., Fotopoulos, V., and Inze, D. 2017. Strobilurins as growth-promoting compounds: How Stroby regulates Arabidopsis leaf growth. Plant Cell Environ. 40:1748-1760.
Verma, S., Varma, A., Rexer, K.-H., Hassel, A., Kost, G., Sarbhoy, A., Bisen, P., Bütehorn, B., and Franken, P. 1998. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896-903.
Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565.
Worapong, J., Strobel, G., Ford, E. J., Li, J. Y., Baird, G., and Hess, W. M. 2001. Muscodor albus anam. gen. et sp. nov., an endophyte from Cinnamomum zeylanicum. Mycotaxon 79:67-79.
Xu, H.-M., Zeng, G.-Z., Zhou, W.-B., He, W.-J., and Tan, N.-H. 2013. Astins K-P, six new chlorinated cyclopentapeptides from Aster tataricus. Tetrahedron 69:7964-7969.
Xu, L., Wu, C., Oelmüller, R., and Zhang, W. 2018. Role of phytohormones in Piriformospora indica-induced growth promotion and stress tolerance in plants: More questions than answers. Front. Microbiol. 9:1646.