Mycobiome of low maintenance iconic landscape plant boxwood under repeated treatments of contact and systemic fungicides

  • Leach, J. E., Triplett, L. R., Argueso, C. T. & Trivedi, P. Communication in the phytobiome. Cell 169, 587–596 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Stone, B. W. G., Weingarten, E. A. & Jackson, C. R. The role of the phyllosphere microbiome in plant health and function. in Annual Plant Reviews Online 533–556 (John Wiley & Sons, Ltd, https://doi.org/10.1002/9781119312994.apr0614 (2018).

  • Rodriguez, R. J. & Redman, R. S. Fungal life-styles and ecosystem dynamics: biological aspects of plant pathogens, plant endophytes and saprophytes. in Advances in Botanical Research (eds Andrews, J. H., Tommerup, I. C. & Callow, J. A.) vol. 24 169–193 (Academic, (1997).

  • Baron, N. C. & Rigobelo, E. C. Endophytic fungi: a tool for plant growth promotion and sustainable agriculture. Mycology 13, 39–55 (2022).

    PubMed 

    Google Scholar 

  • Di Francesco, A. et al. Biocontrol activity and plant growth promotion exerted by Aureobasidium pullulans strains. J. Plant. Growth Regul. 40, 1233–1244 (2021).

    Google Scholar 

  • Albrectsen, B. R. et al. Endophytic fungi in European Aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance. Fungal Divers. 41, 17–28 (2010).

    Google Scholar 

  • Cambon, M. C. et al. Drought tolerance traits in Neotropical trees correlate with the composition of phyllosphere fungal communities. Phytobiomes J. 7:2, 244-258 (2023). https://doi.org/10.1094/PBIOMES-04-22-0023-R

    Google Scholar 

  • Bettenfeld, P., Fontaine, F., Trouvelot, S., Fernandez, O. & Courty, P. E. Woody plant declines. What’s wrong with the microbiome? Trends Plant. Sci. 25, 381–394 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Noel, Z. A. et al. Non-target impacts of fungicide disturbance on phyllosphere yeasts in conventional and no-till management. ISME Commun. 2, 19 (2022).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Castañeda, L. E., Miura, T., Sánchez, R. & Barbosa, O. Effects of agricultural management on phyllosphere fungal diversity in vineyards and the association with adjacent native forests. PeerJ 6, e5715 (2018).

  • Varanda, C. M. R. et al. Fungal endophytic communities associated to the phyllosphere of grapevine cultivars under different types of management. Fungal Biol. 120, 1525–1536 (2016).

    PubMed 

    Google Scholar 

  • Paasch, B. C. & He, S. Y. Toward Understanding microbiota homeostasis in the plant Kingdom. PLoS Pathog. 17, e1009472 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Prior, R., Mittelbach, M. & Begerow, D. Impact of three different fungicides on fungal epi- and endophytic communities of common bean (Phaseolus vulgaris) and broad bean (Vicia faba). J. Environ. Sci. Health B. 52, 376–386 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Lin, H. A. & Mideros, S. X. The effect of Septoria Glycines and fungicide application on the soybean phyllosphere mycobiome. Phytobiomes J. 7:2, 220-232 (2023). https://doi.org/10.1094/PBIOMES-12-21-0075-R

    Google Scholar 

  • Bertelsen, J. R., De Neergaard, E. & Smedegaard-Petersen, V. Fungicidal effects of azoxystrobin and Epoxiconazole on phyllosphere fungi, senescence and yield of winter wheat. Plant. Pathol. 50, 190–205 (2001).

    CAS 

    Google Scholar 

  • Perazzolli, M. et al. Resilience of the natural phyllosphere microbiota of the grapevine to chemical and biological pesticides. Appl. Environ. Microbiol. 80, 3585–3596 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Karlsson, I., Friberg, H., Steinberg, C. & Persson, P. Fungicide effects on fungal community composition in the wheat phyllosphere. PLoS ONE. 9, e111786 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Knorr, K., Jørgensen, L. N. & Nicolaisen, M. Fungicides have complex effects on the wheat phyllosphere mycobiome. PLOS ONE. 14, e0213176 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sapkota, R., Knorr, K., Jørgensen, L. N., O’Hanlon, K. A. & Nicolaisen, M. Host genotype is an important determinant of the cereal phyllosphere mycobiome. New. Phytol. 207, 1134–1144 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Milazzo, C. et al. High-throughput metabarcoding characterizes fungal endophyte diversity in the phyllosphere of a barley crop. Phytobiomes J. 5, 316–325 (2021).

    Google Scholar 

  • Win, P. M., Matsumura, E. & Fukuda, K. Effects of pesticides on the diversity of endophytic fungi in tea plants. Microb. Ecol. 82, 62–72 (2021).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Doherty, J. R., Botti-Marino, M., Kerns, J. P., Ritchie, D. F. & Roberts, J. A. Response of microbial populations on the creeping bentgrass phyllosphere to periodic fungicide applications. Plant. Health Prog. 18, 44–49 (2017).

    Google Scholar 

  • Katsoula, A., Vasileiadis, S., Sapountzi, M. & Karpouzas, D. G. The response of soil and phyllosphere microbial communities to repeated application of the fungicide iprodione: accelerated biodegradation or toxicity? FEMS Microbiol. Ecol. 96, fiaa056 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Baumann, A. J. et al. High tolerance and degradation of fungicides by fungal strains isolated from contaminated soils. Mycologia 114, 813–824 (2022).

    CAS 
    PubMed 

    Google Scholar 

  • Batdorf, L. R. Boxwood Handbook: A Practical Guide To Knowing and Growing Boxwood (American Boxwood Society, 1995).

  • Ivors, K. L. et al. First report of Boxwood blight caused by Cylindrocladium pseudonaviculatum in the united States. Plant. Dis. 96, 1070–1070 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Daughtrey, M. L. Boxwood blight: threat to ornamentals. Annu. Rev. Phytopathol. 57, 189–209 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Hong, C. Fighting plant pathogens together. Science 365, 229–229 (2019).

    ADS 
    PubMed 

    Google Scholar 

  • LaMondia, J. A. Management of Calonectria pseudonaviculata in Boxwood with fungicides and less susceptible host species and varieties. Plant. Dis. 99, 363–369 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • LaMondia, J. A. Fungicide efficacy against Calonectria pseudonaviculata, causal agent of Boxwood blight. Plant. Dis. 98, 99–102 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • LaMondia, J. A. Curative fungicide activity against Calonectria pseudonaviculata, the Boxwood blight pathogen. J. Environ. Hortic. 38, 44–49 (2020).

    CAS 

    Google Scholar 

  • Singh, R. & Doyle, V. P. Boxwood dieback caused by Colletotrichum theobromicola: A diagnostic guide. Plant. Health Prog. 18, 174–180 (2017).

    Google Scholar 

  • Kaur, H., Singh, R., Doyle, V. & Valverde, R. A diagnostic TaqMan real-time PCR assay for in planta detection and quantification of Colletotrichum theobromicola, causal agent of Boxwood dieback. Plant. Dis. 105, 2395–2401 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Yang, X. et al. A diagnostic guide for volutella blight affecting Buxaceae. Plant. Health Prog. 22, 578–590 (2021).

    Google Scholar 

  • Baysal-Gurel, F., Bika, R., Avin, F. A., Jennings, C. & Simmons, T. Occurrence of volutella blight caused by Pseudonectria foliicola on Boxwood in Tennessee. Plant. Dis. 105, 2014 (2021).

    Google Scholar 

  • Shin, S., Kim, J. E. & Son, H. Identification and characterization of fungal pathogens associated with Boxwood diseases in the Republic of Korea. Plant. Pathol. J. 38, 304–312 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Akıllı Şimşek, S., Katırcıoğlu, Y. Z., Çakar, D., Rigling, D. & Maden, S. Impact of fungal diseases on common box (Buxus sempervirens L.) vegetation in Turkey. Eur. J. Plant. Pathol. 153, 1203–1220 (2019).

    Google Scholar 

  • Vettraino, A. M., Franceschini, S. & Vannini, A. First report of Buxus rotundifolia root and collar rot caused by Phytophthora Citrophthora in Italy. Plant. Dis. 94, 272–272 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Parajuli, M., Neupane, S., Liyanapathiranage, P. & Baysal-Gurel, F. Comparative performance of fungicides in management of Phytophthora root rot on Boxwood. (2023). https://doi.org/10.21273/HORTSCI17227-23

  • Boxwood blight task force. (2024). https://www.ext.vt.edu/content/ext_vt_edu/en/agriculture/commercial-horticulture/boxwood-blight.html. Accessed July 1.

  • Edgington, L. V. Systemic fungicides: A perspective after 10 years. Plant. Dis. 64, 19 (1980).

    CAS 

    Google Scholar 

  • Morakotkarn, D. et al. Taxonomic characterization of Shiraia-like fungi isolated from bamboos in Japan. Mycoscience 49, 258–265 (2008).

    CAS 

    Google Scholar 

  • Cheng, T. F., Jia, X. M., Ma, X. H., Lin, H. & Zhao, Y. H. Phylogenetic study on Shiraia bambusicola by rDNA sequence analyses. J. Basic. Microbiol. 44, 339–350 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Zhu, D., Wang, J., Zeng, Q., Zhang, Z. & Yan, R. A novel endophytic huperzine A–producing fungus, Shiraia sp. Slf14, isolated from Huperzia serrata. J. Appl. Microbiol. 109, 1469–1478 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Lin, X. et al. Transferrin-modified nanoparticles for photodynamic therapy enhance the antitumor efficacy of hypocrellin A. Front Pharmacol 8:815 (2017).

  • Kong, P., Sharifi, M., Bordas, A. & Hong, C. Differential tolerance to Calonectria pseudonaviculata of english Boxwood plants associated with the complexity of culturable fungal and bacterial endophyte communities. Plants 10, 2244 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Alves, J. L., Woudenberg, J. H. C., Duarte, L. L., Crous, P. W. & Barreto, R. W. Reappraisal of the genus Alternariaster (Dothideomycetes). Persoonia 31, 77–85 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • LeBlanc, N. & Crouch, J. A. Prokaryotic taxa play keystone roles in the soil Microbiome associated with Woody perennial plants in the genus Buxus. Ecol. Evol. 9, 11102–11111 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248 (2016).

    Google Scholar 

  • Kurzawińska, H., Mazur, S. & Nawrocki, J. Microorganisms colonizing the leaves, shoots and roots of Boxwood (Buxus sempervirens L). Acta Sci. Pol. Hortorum Cultus. 18, 149–154 (2019).

    Google Scholar 

  • Smedegaard-Petersen, V. Increased demand for respiratory energy of barley leaves reacting hypersensitively against Erysiphe graminis, Pyrenophora Teres and Pyrenophora Graminea. J. Phytopathol. 99, 54–62 (1980).

    Google Scholar 

  • Boddy, L. & Hiscox, J. Fungal ecology: principles and mechanisms of colonization and competition by saprotrophic fungi. Microbiol Spectr 4:10.1128/microbiolspec.funk-0019-2016 (2016). https://doi.org/10.1128/microbiolspec.funk-0019-2016

  • Liu, F. et al. Correlation between the synthesis of Pullulan and melanin in Aureobasidium Pullulans. Int. J. Biol. Macromol. 177, 252–260 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Mannaa, M. et al. Aureobasidium pullulans treatment mitigates drought stress in Abies Koreana via rhizosphere Microbiome modulation. Plants 12, 3653 (2023).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • van Nieuwenhuijzen, E. J. & Aureobasidium Academic Press, Oxford,. in Encyclopedia of Food Microbiology (Second Edition) (eds. Batt, C. A. & Tortorello, M. L.) 105–109 (2014). https://doi.org/10.1016/B978-0-12-384730-0.00017-3

  • Wang, M. & Cernava, T. Overhauling the assessment of agrochemical-driven interferences with microbial communities for improved global ecosystem integrity. Environ. Sci. Ecotechnol. 4, 100061 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Arnault, G., Mony, C. & Vandenkoornhuyse, P. Plant microbiota dysbiosis and the Anna karenina principle. Trends Plant. Sci. 28, 18–30 (2022).

    PubMed 

    Google Scholar 

  • Berg, G. et al. Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol. Ecol 93:5, fix050 (2017). https://doi.org/10.1093/femsec/fix050

  • Runge, P., Ventura, F., Kemen, E. & Stam, R. Distinct phyllosphere Microbiome of wild tomato species in central Peru upon dysbiosis. Microb. Ecol. 85, 168–183 (2023).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Lichiheb, N. et al. Measuring leaf penetration and volatilization of Chlorothalonil and Epoxiconazole applied on wheat leaves in a laboratory-scale experiment. J. Environ. Qual. 44, 1782–1790 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Pinto, C. et al. Unravelling the diversity of grapevine Microbiome. PLOS ONE. 9, e85622 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sumbula, V., Kurian, P. S., Girija, D. & Cherian, K. A. Impact of foliar application of fungicides on tomato leaf fungal community structure revealed by metagenomic analysis. Folia Microbiol. 67, 103–108 (2022).

    CAS 

    Google Scholar 

  • Sieber, T. N. Chapter 6 – The phyllosphere mycobiome of woody plants. in Forest Microbiology (eds. Asiegbu, F. O. & Kovalchuk, A.) 111–132Academic Press, (2021). https://doi.org/10.1016/B978-0-12-822542-4.00003-6

  • Santra, H. K. & Banerjee, D. Fungal endophytes: A source for biological control agents. in Agriculturally Important Fungi for Sustainable Agriculture: Volume 2: Functional Annotation for Crop Protection (eds Yadav, A. N., Mishra, S., Kour, D., Yadav, N. & Kumar, A.) 181–216 (Springer International Publishing, Cham, doi:https://doi.org/10.1007/978-3-030-48474-3_6. (2020).

    Google Scholar 

  • McNab, E. & Hsiang, T. Naturally occurring propiconazole-tolerant fungal isolates in the phyllosphere of Agrostis stolonifera. J. Plant. Dis. Prot. 131, 1195–1201 (2024).

    CAS 

    Google Scholar 

  • Baćmaga, M., Wyszkowska, J. & Kucharski, J. The influence of Chlorothalonil on the activity of soil microorganisms and enzymes. Ecotoxicology 27, 1188–1202 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sjokvist, E. et al. Dissection of Ramularia leaf spot disease by integrated analysis of barley and Ramularia collo-cygni transcriptome responses. Mol. Plant. Microbe Interact. 32, 176–193 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Thach, T., Munk, L., Hansen, A. L. & Jørgensen, L. N. Disease variation and chemical control of Ramularia leaf spot in sugar beet. Crop Prot. 51, 68–76 (2013).

    CAS 

    Google Scholar 

  • Cairney, J. W. G. Basidiomycete mycelia in forest soils: dimensions, dynamics and roles in nutrient distribution. Mycol. Res. 109, 7–20 (2005).

    PubMed 

    Google Scholar 

  • Tripathi, M. & Joshi, Y. What are lichenized fungi? in Endolichenic Fungi: Present and Future Trends (eds Tripathi, M. & Joshi, Y.) 1–26 (Springer, Singapore, doi:https://doi.org/10.1007/978-981-13-7268-1_1. (2019).

    Google Scholar 

  • Yan, Z., Xiong, C., Liu, H. & Singh, B. K. Sustainable agricultural practices contribute significantly to one health. J. Sustain. Agr Environ. 1, 165–176 (2022).

    Google Scholar 

  • Saunders, R., Saunders, T., Saunders, B. & Saunders, J. Boxwood Guide (Saunders Brothers, 2018).

  • Avenot, H. F., King, C., Edwards, T. P., Baudoin, A. & Hong, C. X. Effects of inoculum dose, temperature, cultivar, and interrupted leaf wetness period on infection of Boxwood by Calonectria pseudonaviculata. Plant. Dis. 101, 866–873 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Avenot, H. F., Baudoin, A. & Hong, C. Conidial production and viability of Calonectria pseudonaviculata on infected Boxwood leaves as affected by temperature, wetness, and dryness periods. Plant. Pathol. 71, 696–701 (2022).

    Google Scholar 

  • Gehesquière, B. Cylindrocladium buxicola nom. cons. prop. (syn. Calonectria pseudonaviculata) on Buxus: molecular characterization, epidemiology, host resistance and fungicide controlGhent University, Belgium,. (2014).

  • Li, X. et al. Characterization of Boxwood shoot bacterial communities and potential impact from fungicide treatments. Microbiol. Spectr. 0, e04163–e04122 (2023).

    Google Scholar 

  • Martin, K. J. & Rygiewicz, P. T. Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol. 5, 28 (2005).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, X. NanoPrep. https://github.com/xpli2020/NanoPrep. Accessed July 1. (2024).

  • Cuscó, A., Catozzi, C., Viñes, J., Sanchez, A. & Francino, O. Microbiota profiling with long amplicons using Nanopore sequencing: full-length 16S rRNA gene and the 16S-ITS-23S of the rrn operon. F1000Rsearch vol. 7 1755 Preprint at https://doi.org/10.12688/f1000research.16817.2 (2019).

  • Abarenkov, K. et al. Full UNITE + INSD dataset for Fungi. UNITE Community. https://doi.org/10.15156/BIO/1281531 (2021).

    Google Scholar 

  • Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Callahan, B. J., McMurdie, P. J. & Holmes, S. P. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 11, 2639–2643 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Lahti, L. & Shetty, S. Tools for Microbiome analysis in R. (2017). http://microbiome.github.com/microbiome

  • Dunn, O. J. Multiple comparisons among means. J. Am. Stat. Assoc. 56, 52–64 (1961).

    MathSciNet 
    MATH 

    Google Scholar 

  • Liu, C., Cui, Y., Li, X. & Yao, M. Microeco: an R package for data mining in microbial community ecology. FEMS Microbiol. Ecol. 97, fiaa255 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Jaccard, P. The distribution of the flora in the alpine zone. New. Phytol. 11, 37–50 (1912).

    Google Scholar 

  • Legendre, P. & Gallagher, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280 (2001).

    ADS 
    PubMed 

    Google Scholar 

  • Legendre, P. & Borcard, D. Box–Cox-chord transformations for community composition data prior to beta diversity analysis. Ecography 41, 1820–1824 (2018).

    ADS 

    Google Scholar 

  • McMurdie, P. J. & Holmes, S. Phyloseq: an R package for reproducible interactive analysis and graphics of Microbiome census data. PLOS ONE. 8, e61217 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Oksanen, J. et al. vegan: Community ecology package. https://github.com/vegandevs/vegan (2019).

  • Bray, J. R. & Curtis, J. T. An ordination of the upland forest communities of Southern Wisconsin. Ecol. Monogr. 27, 325–349 (1957).

    Google Scholar 

  • Mallick, H. et al. Multivariable association discovery in population-scale meta-omics studies. PLOS Comput. Biol. 17, e1009442 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R Stat. Soc. Ser. B (Methodoll). 57, 289–300 (1995).

    MathSciNet 
    MATH 

    Google Scholar 

  • Martin, V. M. et al. Longitudinal disease-associated gut Microbiome differences in infants with food protein-induced allergic Proctocolitis. Microbiome 10, 154 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Peschel, S., Müller, C. L., von Mutius, E., Boulesteix, A. L. & Depner, M. NetCoMi: network construction and comparison for Microbiome data in R. Brief. Bioinform. 22, bbaa290 (2021).

    PubMed 

    Google Scholar 

  • Yoon, G., Gaynanova, I. & Müller, C. L. Microbial networks in SPRING – Semi-parametric Rank-Based correlation and partial correlation Estimation for quantitative Microbiome data. Front Genet 10:516 (2019). https://doi.org/10.3389/fgene.2019.00516

  • Csardi, G. & Tamas nepusz. The Igraph software package for complex network research. InterJournal, Complex Systems, 1695 (2006).

  • Jaccard, P. Nouvelles recherches Sur La distribution Florale. (1908). https://doi.org/10.5169/SEALS-268384

  • Hubert, L. & Arabie, P. Comparing partitions. J. Classif. 2, 193–218 (1985).

    Google Scholar 

  • Benjamini, Y. & Hochberg, Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 25, 60–83 (2000).

    Google Scholar 

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