Phylogenetic conservatism of mycoparasitism and its contribution to pathogen antagonism.
Cladosporium
Melampsora
Populus
endophyte
fungal traits
mycoparasitism
pathogen antagonism
phylogenetic signal
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
06
03
2022
received:
30
10
2019
accepted:
16
03
2022
pubmed:
22
3
2022
medline:
18
5
2022
entrez:
21
3
2022
Statut:
ppublish
Résumé
Closely related species are expected to have similar functional traits due to shared ancestry and phylogenetic inertia. However, few tests of this hypothesis are available for plant-associated fungal symbionts. Fungal leaf endophytes occur in all land plants and can protect their host plant from disease by a variety of mechanisms, including by parasitizing pathogens (e.g., mycoparasitism). Here, we tested whether phylogenetic relatedness among species of Cladosporium, a widespread genus that includes mycoparasitic species, predicts the effect of this endophyte on the severity of leaf rust disease. First, we used congruence among different marker sequences (i.e., genealogical concordance phylogenetic species recognition criterion) to delimit species of Cladosporium. Next, in a controlled experiment, we quantified both mycoparasitism and disease modification for the selected Cladosporium species. We identified 17 species of Cladosporium; all the species reduced rust disease severity in our experiment. Cladosporium phylogeny was a significant predictor of mycoparasitism. However, we did not observe a phylogenetic effect on disease severity overall, indicating that other mechanism/s operating independently of shared ancestry also contributed to endophyte effects on disease severity. Indeed, a second experiment showed that Cladosporium endophyte exudates (no live organism) from divergent species groups equally reduced disease severity. Our results reveal that multiple mechanisms contribute to the protective effects of an endophyte against a plant pathogen, but not all traits underlying these mechanisms are phylogenetically conserved.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3018-3030Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Aime, M. C., Matheny, P. B., Henk, D. A., Frieders, E. M., Nilsson, R. H., Piepenbring, M., McLaughlin, D. J., Szabo, L. J., Begerow, D., Sampaio, J. P., & Bauer, R. (2006) An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia, 98, 896-905.
Anderson, F. E., López, S. P. S., Sánchez, R. M., Fuentealba, C. G. R., & Barton, J. (2016). Puccinia araujiae, a promising classical biocontrol agent for moth plant in New Zealand: Biology, host range and hyperparasitism by Cladosporium uredinicola. Biological Control, 95, 23-30. https://doi.org/10.1016/j.biocontrol.2015.12.015
Arnold, A. E., Mejía, L. C., Kyllo, D., Rojas, E. I., Maynard, Z., Robbins, N., & Herre, E. A. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, 100, 15649-15654. https://doi.org/10.1073/pnas.2533483100
Assante, G., Maffi, D., Saracchi, M., Farina, G., Moricca, S., & Ragazzi, A. (2004). Histological studies on the mycoparasitism of Cladosporium tenuissimum on urediniospores of Uromyces appendiculatus. Mycological Research, 108(2), 170-182. https://doi.org/10.1017/S0953756203008852
Azmir, J., Zaidul, I. S., Rahman, M. M., Sharif, K. M., Mohamed, A., Sahena, F., Jahurul, M. H., Ghafoor, K., Norulaini, N. A., & Omar, A. K. (2013). Techniques for extraction of bioactive compounds from plant materials: A review. Journal of Food Engineering, 117(4), 426-436. https://doi.org/10.1016/j.jfoodeng.2013.01.014
Bakker, M. G., Manter, D. K., Sheflin, A. M., Weir, T. L., & Vivanco, J. M. (2012). Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant and Soil, 360, 1-13. https://doi.org/10.1007/s11104-012-1361-x
Barge, E. G., Leopold, D. R., Peay, K. G., Newcombe, G., & Busby, P. E. (2019). Differentiating spatial from environmental effects on foliar fungal communities of Populus trichocarpa. Journal of Biogeography, https://doi.org/10.1111/jbi.13641
Bensch, K., Braun, U., Groenewald, J. Z., & Crous, P. W. (2012). The genus Cladosporium. Studies in Mycology, 72, 1-401. https://doi.org/10.3114/sim0003
Bensch, K., Groenewald, J. Z., Dijksterhuis, J., Starink-Willemse, M., Andersen, B., Summerell, B. A., Shin, H. D., Dugan, F. M., Schroers, H. J., Braun, U., & Crous, P. W. (2010). Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Studies in Mycology, 67, 1-94. https://doi.org/10.3114/sim.2010.67.01
Blomberb, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57(4), 717-745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x
Bürkner, P. C. (2017). brms: An R Package for Bayesian Multilevel Models using Stan. Journal of Statistical Software, 80(1), 1-28. https://doi.org/10.18637/jss.v080.i01
Busby, P. E., Peay, K. G., & Newcombe, G. (2016). Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytologist, 209(4), 1681-1692.
Busby, P. E., Ridout, M., & Newcombe, G. (2016). Fungal endophytes: modifiers of plant disease. Plant Molecular Biology, 90, 645-655. https://doi.org/10.1007/s11103-015-0412-0
Busby, P. E., Soman, C., Wagner, M. R., Friesen, M. L., Kremer, J., Bennett, A., Morsy, M., Eisen, J. A., Leach, J. E., & Dangl, J. L. (2017). Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biology, 15(3), e2001793. https://doi.org/10.1371/journal.pbio.2001793
Chaverri, P., & Samuels, G. J. (2013). Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution, 67, 2823-2837. https://doi.org/10.1111/evo.12169
Chen, Y., Frazzitta, A. E., Litvintseva, A. P., Fang, C., Mitchell, T. G., Springer, D. J., Ding, Y., Yuan, G., & Perfect, J. R. (2015). Next generation multilocus sequence typing (NGMLST) and the analytical software program MLSTEZ enable efficient, cost-effective, high-throughput, multilocus sequencing typing. Fungal Genetics and Biology, 75, 64-71. https://doi.org/10.1016/j.fgb.2015.01.005
Clark, K., Karsch-Mizrachi, I., Lipman, D., Ostell, J., & Sayers, E. W. (2016). GenBank. Nucleic Acids Research, 44, 67-72. https://doi.org/10.1093/nar/gkv1276
Cregger, M. A., Veach, A. M., Yang, Z., Crouch, M. J., Vilgalys, R., Tuskan, G. A., & Schadt, C. W. (2018). The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome, 6, 31.
de Vienne, D. M., Hood, M. E., & Giraud, T. (2009). Phylogenetic determinants of potential host shifts in fungal pathogens. Journal of Evolutionary Biology, 22, 2532-2541. https://doi.org/10.1111/j.1420-9101.2009.01878.x
Dolińska, A., Bartkowska, T. M., & Schollenberge, M. (2011). Light and scanning microscope observations of Cladosporium uredinicola growth on rust fungi. Phytopathologia, 61, 37-44.
Dunlap, J. M., & Stettler, R. F. (1996). Genetic variation and productivity of Populus trichocarpa and its hybrids. IX. Phenology and Melampsora rust incidence of native black cottonwood clones from four river valleys in Washington. Forest Ecology and Management, 87(1), 233-256.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792-1797. https://doi.org/10.1093/nar/gkh340
Fontana, D. C., de Paula, S., Torres, A. G., de Souza, V. H. M., Pascholati, S. F., Schmidt, D., & Dourado Neto, D. (2021). Endophytic Fungi: Biological Control and Induced Resistance to Phytopathgens and Abiotic Stresses. Pathogens, 10, 570. https://doi.org/10.3390/pathogens10050570
Fravel, D., Olivain, C., & Alabouvette, C. (2003). Fusarium oxysporum and its biocontrol. New Phytologist, 157(3), 493-502.
Gabry, J., Simpson, D., Vehtari, A., Betancourt, M., & Gelman, A. (2019). Visualization in Bayesian workflow. Journal of the Royal Statistical Society: Series A (Statistics in Society), 182(2), 389-402. https://doi.org/10.1111/rssa.12378
Gelman, A., & Hill, J. (2007). Data analysis using regression and multilevel/hierarchical models. Cambridge University Press.
Gelman, A., Jakulin, A., Pittau, M. G., & Su, Y. S. (2008). A weakly informative default prior distribution for logistic and other regression models. Annals of Applied Statistics, 2(4), 1360-1383. https://doi.org/10.1214/08-AOAS191
Giauque, H., Connor, E. W., & Hawkes, C. V. (2019). Endophyte traits relevant to stress tolerance, resource use and habitat of origin predict effects on host plants. New Phytologist, 221(4), 2239-2249. https://doi.org/10.1111/nph.15504
Goberna, M., & Verdu, M. (2016). Predicting microbial traits with phylogenies. The ISME Journal, 10, 959-967. https://doi.org/10.1038/ismej.2015.171
Hacquard, S., Spaepen, S., Garrido-Oter, R., & Schulze-Lefert, P. (2017). Interplay between innate immunity and the plant microbiota. Annual Review of Phytopathology, 55, 565-589. https://doi.org/10.1146/annurev-phyto-080516-035623
Hanada, R. E., Pomella, A. W. V., Costa, H. S., Bezerra, J. L., Loguercio, L. L., & Pereira, J. O. (2010). Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology, 114, 901-910.
Heuchert, B., Braun, U., & Schubert, K. (2005). Morphotaxonomic revision of fungicolous Cladosporium species (hyphomycetes). Schlechtendalia, 13, 1-78.
Hoeksema, J. D., Bever, J. D., Chakraborty, S., Chaudhary, V. B., Gardes, M., Gehring, C. A., Hart, M. M., Housworth, E. A., Kaonongbua, W., Klironomos, J. N., & Lajeunesse, M. J. (2018). Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Communications Biology, 1(1), 116. https://doi.org/10.1038/s42003-018-0120-9
Houterman, P. M., Cornelissen, B. J. C., & Rep, M. (2008). Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Path, 4, e1000061. https://doi.org/10.1371/journal.ppat.1000061
Isobe, K., Allison, S. D., Khalili, B., Martiny, A. C., & Martiny, J. B. H. (2019). Phylogenetic conservation of bacterial responses to soil nitrogen addition across continents. Nature Communications, 10, 2499. https://doi.org/10.1038/s41467-019-10390-y
Keck, F., Rimet, F., Bouchez, A., & Franc, A. (2016). phylosignal: an R package to measure, test, and explore the phylogenetic signal. Ecology and Evolution, 6(9), 2774-2780. https://doi.org/10.1002/ece3.2051
Kia, S. H., Glynou, K., Nau, T., Thines, M., Piepenbring, M., & Maciá-Vicente, J. G. (2017). Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants. The ISME Journal, 11(3), 777. https://doi.org/10.1038/ismej.2016.140
Kruschke, J. (2014). Doing bayesian data analysis: A tutorial with r, jags, and stan. Academic Press.
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34(3), 772-773. https://doi.org/10.1093/molbev/msw260
Larson, P. R., & Isebrands, J. G. (1971). The plastochron index as applied to developmental studies of cottonwood. Canadian Journal of Forest Research, 1, 1-11. https://doi.org/10.1139/x71-001
Lenth, R. V. (2021). emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.6.1. https://CRAN.R-project.org/package=emmeans
Leopold, D. R., & Busby, P. E. (2020). Host genotype and colonist arrival order jointly govern plant microbiome composition and function. Current Biology, 30, 3260-3266. https://doi.org/10.1016/j.cub.2020.06.011
Lücking, R., Aime, M. C., Robbertse, B. et al (2020). Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus, 11, 14. https://doi.org/10.1186/s43008-020-00033-z
Makowski, D., Ben-Shachar, M. S., & Chen, S. H. A. (2019). Lüdecke D (2019) Indices of Effect Existence and Significance in the Bayesian Framework. Frontiers in Psychology, 10, 2767. https://doi.org/10.3389/fpsyg.2019.02767
Martiny, A. C., Treseder, K., & Pusch, G. (2013). Phylogenetic conservatism of functional traits in microorganisms. ISME Journal, 7, 830-838.
McElreath, R. (2018). Statistical rethinking: A bayesian course with examples in r and stan. Hall/CRC.
McGuire, K. L., Bent, E., Borneman, J., Majumder, A., Allison, S. D., & Treseder, K. K. (2010). Functional diversity in resource use by fungi. Ecology, 91(8), 2324-2332. https://doi.org/10.1890/09-0654.1
Mejia, L. C., Herre, E. A., Sparks, J. P., Winter, K., Garcia, M. N., Van Bael, S. A., Stitt, J., Shi, Z., Zhang, Y., Guiltinan, M. J., & Maximova, S. N. (2014). Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Frontiers in Microbiology, 5, 479. https://doi.org/10.3389/fmicb.2014.00479
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp. 1-8.
Morgan-Jones, G., & McKemy, J. M. (1990). Studies in the genus Cladosporium sensu lato. I. Concerning Cladosporium uredinicola, occurring on telial columns of Cronartium quercuum and other rusts. Mycotaxon, 39, 185-200.
Moricca, S., Ragazzi, A., & Assante, G. (2005). Biocontrol of Rust Fungi by Cladosporium tenuissimum. In M. H. Pei, & A. R. McCracken (Eds.), Rust diseases of willow and poplar (pp. 213-229). CABI.
Moricca, S., Ragazzi, A., Mitchelson, K. R., & Assante, G. (2001). Antagonism of the two-needle pine stem rust fungi Cronartium flaccidum and Peridermium pini by Cladosporium tenuissimum in vitro and in planta. Phytopathology, 91(5), 457-468.
Nasini, G., Arnone, A., Assante, G., Bava, A., Moricca, S., & Ragazzi, A. (2004). Secondary mould metabolites of Cladosporium tenuissimum, a hyperparasite of rust fungi. Phytochemistry, 65(14), 2107-2111. https://doi.org/10.1016/j.phytochem.2004.03.013
Newcombe, G. (1998). Association of Mmd1, a major gene for resistance to Melampsora medusae f. sp. deltoidae, with quantitative traits in poplar rust. Phytopathology, 88, 114-121.
Oliva, J., Ridley, M., Redondo, M. A., & Caballol, M. (2004). Competitive exclusion amongst endophytes determines shoot blight severity on pine. Functional Ecology, 35(1), 239-254. https://doi.org/10.1111/1365-2435.13692
Ostry, M. E., Wilson, L. F., McNabb, H. S., & Moore, L. M. (1989). A guide to insect, disease, and animal pests of poplars. U.S. Department of Agriculture Agriculture Handbook 677.
Pandey, R. R., Arora, D. K., & Dubey, R. C. (1993). Antagonistic interactions between fungal pathogens and phylloplane fungi of guava. Mycopathologia, 124, 31-39. https://doi.org/10.1007/BF01103054
Perello, A., Simon, M. R., & Arambarri, A. M. (2002). Interactions between foliar pathogens and the saprophytic microflora of the wheat (Triticum aestivum L.) phylloplane. Journal of Phytopathology, 150, 232-243. https://doi.org/10.1046/j.1439-0434.2002.00747.x
Powell, J. R., Parrent, J. L., Hart, M. M., Klironomos, J. N., Rillig, M. C., & Maherali, H. (2009). Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proceedings of the Royal Society B: Biological Sciences, 276(1676), 4237-4245.
R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Raghavendra, A. K., & Newcombe, G. (2013). The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytologist, 197(3), 909-918.
Rodriguez, R. J., Henson, J., Van Volkenburgh, E., Hoy, M., Wright, L., Beckwith, F., Kim, Y. O., & Redman, R. S. (2008). Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal, 2(4), 404. https://doi.org/10.1038/ismej.2007.106
Rodriguez, R. J., White, J. F. Jr, Arnold, A. E., & Redman, A. R. (2009). Fungal endophytes: diversity and functional roles. New Phytologist, 182(2), 314-330. https://doi.org/10.1111/j.1469-8137.2009.02773.x
Rothfels, C. J., Pryer, K. M., & Li, F. W. (2016). Next-generation polyploid phylogenetics: rapid resolution of hybrid polyploid complexes using PacBio single-molecule sequencing. New Phytologist, 213(1), 413-429.
Schubert, K., Groenwald, J. Z., Braun, U., Dijksterhuis, J., Starink, M., Hill, C. F., Zalar, P., De Hoog, G. S., & Crous, P. W. (2007). Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Studies in Mycology, 58, 105-156. https://doi.org/10.3114/sim.2007.58.05
Sharma, I. K., & Heather, W. A. (1988). Light and electron microscope studies of Cladosporium tenuissimum, mycoparasitic on poplar leaf rust, Melampsora larici-populina. Transactions of the British Mycological Society, 90, 125-131.
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313. https://doi.org/10.1093/bioinformatics/btu033
Stokstad, E. (2007). Plant pathology. Deadly wheat fungus threatens world’s breadbaskets. Science, 315, 1786-1787. https://doi.org/10.1126/science.315.5820.1786
Stone, J., Bacon, C., & White, J. (2000). An overview of endophytic microbes: endophytism defined. In C. Bacon, & J. White (Eds.), Microbial endophytes (pp. 3-29). Marcel Dekker.
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., & Fisher, M. C. (2000). Phylogenetic species recognition and species concepts in Fungi. Fungal Genetics and Biology, 31, 21-32. https://doi.org/10.1006/fgbi.2000.1228
Torres, D. E., Rojas-Martínez, R. I., Zavaleta-Mejía, E., Guevara-Fefer, P., Márquez-Guzmán, G. J., & Pérez-Martínez, C. (2017). Cladosporium cladosporioides and Cladosporium pseudocladosporioides as potential new fungal antagonists of Puccinia horiana Henn., the causal agent of chrysanthemum white rust. PLoS One, 12(1), e0170782.
Van Der Heijden, M. G., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., & Sanders, I. R. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396(6706), 69. https://doi.org/10.1038/23932
Widin, K. D., & Schipper, A. L. (1981). Effect of Melampsora medusae leaf rust infection on yield of hybrid poplars in north-central United States. European Journal of Forest Pathology, 11, 438-448.
Zanne, A. E., Abarenkov, K., Afkhami, M. E., Aguilar-Trigueros, C. A., Bates, S., Bhatnagar, J. M., Busby, P. E., Christian, N., Cornwell, W., Crowther, T. W., & Moreno, H. F. (2019). Fungal functional ecology: Bringing a trait-based approach to plant-associated fungi. Biological Reviews, 95, 409-433.
Zhan, G., Tian, Y., Wang, F., Chen, X., Guo, J., Jiao, M., Huang, L., & Kang, Z. (2014). A novel fungal hyperparasite of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One, 9(11), e111484.