Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

doi:10.1002/ajb2.1436

. 2020 Feb;107(2):219-228.

doi: 10.1002/ajb2.1436. Epub 2020 Feb 18.

Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

Natalie Christian^#^{1

2}, Brian E Sedio^#^{3

4

5}, Ximena Florez-Buitrago^#³, Luis A Ramírez-Camejo^{4

6}, Enith I Rojas³, Luis C Mejía⁴, Sage Palmedo⁷, Autumn Rose⁷, John W Schroeder^{3

8}, Edward Allen Herre³

Affiliations

¹ Department of Plant Biology, School of Integrative Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL, 61801, USA.
² Department of Biology, University of Louisville, 139 Life Sciences Bldg., Louisville, KY, 40208, USA.
³ Smithsonian Tropical Research Institute, Unit 9100 Box 0948, DPO AA 34002-9998, USA.
⁴ Center for Biodiversity and Drug Discovery, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología, Apartado 0843-01103, Ciudad del Saber, Ancón, Republic of Panama.
⁵ Department of Integrative Biology, University of Texas at Austin, 2415 Speedway #C0930, Austin, TX, 78712, USA.
⁶ Department of Botany and Plant Pathology, Purdue University, 915 W. State St., West Lafayette, IN, 47907, USA.
⁷ Department of Ecology and Evolutionary Biology, Princeton University, 106A Guyot Ln., Princeton, NJ, 08544, USA.
⁸ Ecology, Evolution, and Marine Biology, University of California Santa-Barbara, Noble Hall 2116, Santa Barbara, CA, 93106, USA.

^# Contributed equally.

PMID: 32072625
DOI: 10.1002/ajb2.1436

Free article

Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

Natalie Christian et al. Am J Bot. 2020 Feb.

Free article

. 2020 Feb;107(2):219-228.

doi: 10.1002/ajb2.1436. Epub 2020 Feb 18.

Authors

Affiliations

¹ Department of Plant Biology, School of Integrative Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL, 61801, USA.
² Department of Biology, University of Louisville, 139 Life Sciences Bldg., Louisville, KY, 40208, USA.
³ Smithsonian Tropical Research Institute, Unit 9100 Box 0948, DPO AA 34002-9998, USA.
⁴ Center for Biodiversity and Drug Discovery, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología, Apartado 0843-01103, Ciudad del Saber, Ancón, Republic of Panama.
⁵ Department of Integrative Biology, University of Texas at Austin, 2415 Speedway #C0930, Austin, TX, 78712, USA.
⁶ Department of Botany and Plant Pathology, Purdue University, 915 W. State St., West Lafayette, IN, 47907, USA.
⁷ Department of Ecology and Evolutionary Biology, Princeton University, 106A Guyot Ln., Princeton, NJ, 08544, USA.
⁸ Ecology, Evolution, and Marine Biology, University of California Santa-Barbara, Noble Hall 2116, Santa Barbara, CA, 93106, USA.

^# Contributed equally.

PMID: 32072625
DOI: 10.1002/ajb2.1436

Abstract

Premise: Interactions between fungal endophytes and their host plants present useful systems for identifying important factors affecting assembly of host-associated microbiomes. Here we investigated the role of secondary chemistry in mediating host affinity of asymptomatic foliar endophytic fungi using Psychotria spp. and Theobroma cacao (cacao) as hosts.

Methods: First, we surveyed endophytic communities in Psychotria species in a natural common garden using culture-based methods. Then we compared differences in endophytic community composition with differences in foliar secondary chemistry in the same host species, determined by liquid chromatography-tandem mass spectrometry. Finally, we tested how inoculation with live and heat-killed endophytes affected the cacao chemical profile.

Results: Despite sharing a common environment and source pool for endophyte spores, different Psychotria host species harbored strikingly different endophytic communities that reflected intrinsic differences in their leaf chemical profiles. In T. cacao, inoculation with live and heat-killed endophytes produced distinct cacao chemical profiles not found in uninoculated plants or pure fungal cultures, suggesting that endophytes, like pathogens, induce changes in secondary chemical profiles of their host plant.

Conclusions: Collectively our results suggest at least two potential processes: (1) Plant secondary chemistry influences assembly and composition of fungal endophytic communities, and (2) host colonization by endophytes subsequently induces changes in the host chemical landscape. We propose a series of testable predictions based on the possibility that reciprocal chemical interactions are a general property of plant-endophyte interactions.

Keywords: Psychotria; Theobroma cacao; Community assembly; metabolomics; microbiome; species specificity.

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References

LITERATURE CITED

1. Adame-Álvarez, R.-M., J. Mendiola-Soto, and M. Heil. 2014. Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiology Letters 355: 100-107.
1. Apigo, A., and R. Oono. 2018. Dimensions of host specificity in foliar fungal endophytes. In A. M. Pirttilä and A. C. Frank [eds.], Endophytes of forest trees, 15-42. Springer International, Basel, Switzerland.
1. Argout, X., J. Salse, J.-M. Aury, M. J. Guiltinan, G. Droc, J. Gouzy, M. Allegre, et al. 2011. The genome of Theobroma cacao. Nature Genetics 43: 101-108.
1. Arnold, A., L. Mejía, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins, and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
1. Bae, H., R. C. Sicher, M. S. Kim, S.-H. Kim, M. D. Strem, R. L. Melnick, and B. A. Bailey. 2009. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Journal of Experimental Botany 60: 3279-3295.

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[1] Adame-Álvarez, R.-M., J. Mendiola-Soto, and M. Heil. 2014. Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiology Letters 355: 100-107.

[2] Adame-Álvarez, R.-M., J. Mendiola-Soto, and M. Heil. 2014. Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiology Letters 355: 100-107.

[3] Apigo, A., and R. Oono. 2018. Dimensions of host specificity in foliar fungal endophytes. In A. M. Pirttilä and A. C. Frank [eds.], Endophytes of forest trees, 15-42. Springer International, Basel, Switzerland.

[4] Apigo, A., and R. Oono. 2018. Dimensions of host specificity in foliar fungal endophytes. In A. M. Pirttilä and A. C. Frank [eds.], Endophytes of forest trees, 15-42. Springer International, Basel, Switzerland.

[5] Argout, X., J. Salse, J.-M. Aury, M. J. Guiltinan, G. Droc, J. Gouzy, M. Allegre, et al. 2011. The genome of Theobroma cacao. Nature Genetics 43: 101-108.

[6] Argout, X., J. Salse, J.-M. Aury, M. J. Guiltinan, G. Droc, J. Gouzy, M. Allegre, et al. 2011. The genome of Theobroma cacao. Nature Genetics 43: 101-108.

[7] Arnold, A., L. Mejía, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins, and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.

[8] Arnold, A., L. Mejía, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins, and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.

[9] Bae, H., R. C. Sicher, M. S. Kim, S.-H. Kim, M. D. Strem, R. L. Melnick, and B. A. Bailey. 2009. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Journal of Experimental Botany 60: 3279-3295.

[10] Bae, H., R. C. Sicher, M. S. Kim, S.-H. Kim, M. D. Strem, R. L. Melnick, and B. A. Bailey. 2009. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Journal of Experimental Botany 60: 3279-3295.

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Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

Affiliations

Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

Authors

Affiliations

Abstract

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LITERATURE CITED

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Associated data

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

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