Skip to main navigation menu Skip to main content Skip to site footer

SECTION B: LIFE SCIENCES

Vol. 14 No. 1 (2022)

Endophyte microbiome characterization in banana leaf and its variation in presence of Black Sigatoka pathogen (Pseudocercospora fijiensis)

DOI
https://doi.org/10.18272/aci.v14i1.2299
Submitted
May 15, 2021
Published
2022-05-12

Abstract

We describe the bacterial and fungal microbiome of the banana (Musa x paradisiaca) leaf in healthy and necrotic phases of Black Sigatoka or black leaf streak disease (Pseudocercospora fijiensis), evaluated under organic and conventional agronomic management in El Oro province, Ecuador. Samples were collected for subsequent DNA sequencing and analysis of the 16S (V3-V4) and ITS markers. This study suggests that the fungal microbiome from the organic farming system decreases its diversity due to pathogen's presence while diversity increases upon conventional practices. Also, we observed that bacteria from the genus Pseudomonas fluorescens was more abundant in the healthy organic leaf, a known beneficial microorganism for plants. The banana"™s phyllosphere endophyte microbiome depends on the cultivation system, and diseased conditions significantly change the microbiome in the presence of black leaf streak disease.

Key words: necrotic, sequencing, diversity, ASV, phyllosphere

viewed = 829 times

References

  1. Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. y Singh, B. K. (2020). Plant-microbiome interactions: from community assembly to plant health. Nature Reviews Microbiology, 18(11), 607-621. doi: https://doi.org/10.1038/s41579-020-0412-1
  2. Liu, H., Brettell, L. E. y Singh, B. (2020). Linking the Phyllosphere Microbiome to Plant Health. Trends in Plant Science, 25(9), 841-844. doi: https://doi.org/10.1016/j.tplants.2020.06.003
  3. Vorholt, J. A. (2012). Microbial life in the phyllosphere. Nature Reviews. Microbiology, 10(12), 828-840. doi: https://doi.org/10.1038/nrmicro2910
  4. Marchesi, J. R. y Ravel, J. (2015). The vocabulary of microbiome research: a proposal. Microbiome, 31(3). doi: https://doi.org/10.1186/s40168-015-0094-5
  5. Kim, M., Singh, D., Lai-Hoe, A., Go, R., Rahim, R. A., Ainuddin, A. N., Chun, J. y Adams, J. M. (2012). Distinctive Phyllosphere Bacterial Communities in Tropical Trees. Microbial Ecology, 63(3), 674-681. doi: https://doi.org/10.1007/s00248-011-9953-1
  6. Humphrey, P. T. y Whiteman, N. K. (2020). Insect herbivory reshapes a native leaf microbiome. Nature Ecology and Evolution, 4(2), 221-229. doi: https://doi.org/10.1038/s41559-019-1085-x
  7. Liu, H., Carvalhais, L. C., Crawford, M., Singh, E., Dennis, P. G., Pieterse, C. M. J. y Schenk, P. M. (2017). Inner plant values: Diversity, colonization and benefits from endophytic bacteria. Frontiers in Microbiology, 8(DEC), 1-17. doi: https://doi.org/10.3389/fmicb.2017.02552
  8. Bodenhausen, N., Somerville, V., Desirò, A., Walser, J. C., Borghi, L., Van Der Heijden, M. G. A. y Schlaeppi, K. (2019). Petunia- And Arabidopsis-specific root microbiota responses to phosphate supplementation. Phytobiomes Journal, 3(2), 112-124. doi: https://doi.org/10.1094/PBIOMES-12-18-0057-R
  9. Castrillo, G., Teixeira, P. J. P. L., Paredes, S. H., Law, T. F., De Lorenzo, L., Feltcher, M. E., Finkel, O. M., Breakfield, N. W., Mieczkowski, P., Jones, C. D., Paz-Ares, J. y Dangl, J. L. (2017). Root microbiota drive direct integration of phosphate stress and immunity. Nature, 543(7646), 513-518. doi: https://doi.org/10.1038/nature21417
  10. Lu, T., Ke, M., Lavoie, M., Jin, Y., Fan, X., Zhang, Z., Fu, Z., Sun, L., Gillings, M., Peñuelas, J., Qian, H. y Zhu, Y. G. (2018). Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome, 6(1), 1-12. doi: https://doi.org/10.1186/s40168-018-0615-0
  11. Cha, J. Y., Han, S., Hong, H. J., Cho, H., Kim, D., Kwon, Y., Kwon, S. K., Crusemann, M., Bok Lee, Y., Kim, J. F., Giaever, G., Nislow, C., Moore, B. S., Thomashow, L. S., Weller, D. M. y Kwak, Y. S. (2016). Microbial and biochemical basis of a Fusarium wilt-suppressive soil. ISME Journal, 10(1), 119-129. doi: https://doi.org/10.1038/ismej.2015.95
  12. Rastogi, G., Coaker, G. L. y Leveau, J. H. J. (2013). New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiology Letters, 348(1), 1-10. doi: https://doi.org/10.1111/1574-6968.12225
  13. Fitzpatrick, C. R., Mustafa, Z. y Viliunas, J. (2019). Soil microbes alter plant fitness under competition and drought. Journal of Evolutionary Biology, 32(5), 438-450. doi: https://doi.org/10.1111/jeb.13426
  14. Eida, A. A., Ziegler, M., Lafi, F. F., Michell, C. T., Voolstra, C. R., Hirt, H. y Saad, M. M. (2018). Desert plant bacteria reveal host influence and beneficial plant growth properties. PLoS ONE, 13(12), 1-20. https://doi.org/10.1371/journal.pone.0208223
  15. Lei, L. (2020). Phyllosphere dysbiosis. Nature Plants, 6(5), 434. doi: https://doi.org/10.1038/s41477-020-0674-7
  16. Chen, T., Nomura, K., Wang, X., Sohrabi, R., Xu, J., Yao, L., Paasch, B. C., Ma, L., Kremer, J., Cheng, Y., Zhang, L., Wang, N., Wang, E., Xin, X. F. y He, S. Y. (2020). A plant genetic network for preventing dysbiosis in the phyllosphere. Nature, 580(7805), 653-657. doi: https://doi.org/10.1038/s41586-020-2185-0
  17. Purahong, W., Orrù, L., Donati, I., Perpetuini, G., Cellini, A., Lamontanara, A., Michelotti, V., Tacconi, G. y Spinelli, F. (2018). Plant microbiome and its link to plant health: Host species, organs and pseudomonas syringae pv. Actinidiae infection shaping bacterial phyllosphere communities of kiwifruit plants. Frontiers in Plant Science, 871(November), 1-16. doi: https://doi.org/10.3389/fpls.2018.01563
  18. Smets, W. y Koskella, B. (2020). Microbiome: Insect Herbivory Drives Plant Phyllosphere Dysbiosis. Current Biology, 30(9), R412-R414. https://doi.org/10.1016/j.cub.2020.03.039
  19. Li, P., Xu, J., Wang, Z. y Li, H. (2020). Phyllosphere Microbiome in Response to Citrus Melanose. 1-26. doi: https://doi.org/10.21203/rs.3.rs-51076/v1
  20. Evans, E. y Ballen, F. (2018). Banana Market. University of Florida. IFAS Extension, 1-9. http://edis.ifas.ufl.edu/pdffiles/FE/FE90100.pdf
  21. Churchill, A. C. L. (2011). Mycosphaerella fijiensis, the black leaf streak pathogen of banana: progress towards understanding pathogen biology and detection, disease development, and the challenges of control. Molecular Plant Pathology, 12(4), 307-328. doi: https://doi.org/10.1111/j.1364-3703.2010.00672.x
  22. Manzo-Sánchez, G., Orozco-Santos, M., Islas-Flores, I., Martínez-Bolaños, L., Guzmán-González, S., Leopardi-Verde, C. L. y Canto-Canché, B. (2019). Genetic variability of Pseudocercospora fijiensis, the black Sigatoka pathogen of banana (Musa spp.) in Mexico. Plant Pathology, 68(3), 513-522. doi: https://doi.org/10.1111/ppa.12965
  23. Kimunye, J. N., Muzhinji, N., Mostert, D., Viljoen, A., van der Merwe, A. E. y Mahuku, G. (2020). Genetic Diversity and Mating Type Distribution of Pseudocercospora fijiensis on Banana in Uganda and Tanzania. Phytopathology®. doi: https://doi.org/10.1094/PHYTO-04-20-0138-R
  24. Lu-Irving, P., HarenÄár, J. G., Sounart, H., Welles, S. R., Swope, S. M., Baltrus, D. A. y Dlugosch, K. M. (2019). Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria. MSphere, 4(2). doi: https://doi.org/10.1128/mSphere.00088-19
  25. Jiao, J.-Y., Wang, H.-X., Zeng, Y. y Shen, Y.-M. (2006). Enrichment for microbes living in association with plant tissues. Journal of Applied Microbiology, 100(4), 830-837. doi: https://doi.org/10.1111/j.1365-2672.2006.02830.x
  26. Finkel, O. M., Salas-González, I., Castrillo, G., Spaepen, S., Law, T. F., Teixeira, P. J. P. L., Jones, C. D., y Dangl, J. L. (2019). The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLOS Biology, 17(11), 1-34. https://doi.org/10.1371/journal.pbio.3000534
  27. Yourstone, S.M., Lundberg, D.S., Dangl, J.L. y Jones, C.D. (2014). MT-Toolbox: improved amplicon sequencing using molecule tags. BMC Bioinformatics, 15. doi: https://doi.org/10.1186/1471-2105-15-284
  28. Joshi, N. y Sickle, F. (2011). No Title. A Sliding-Window, Adaptive, Quality-Based Trimming Tool for FastQ Files (Version 1.33). https://github.com/najoshi/sickle
  29. Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A. y Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-583. doi: https://doi.org/10.1038/nmeth.3869
  30. Prodan, A., Tremroli, V., Brolin, H., Zwinderman, A., Nieuwdrop. M. y Levin, E. (2020). Comparing bioinformatic pipelines for microbial 16S rRNA amplicon sequencing. PLoS ONE 15(1): e0227434. doi: https://doi.org/10.1371/journal.pone.0227434
  31. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J. y Weber, C. F. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537-7541. doi: https://doi.org/10.1128/AEM.01541-09
  32. Gu, Z. (2020). ComplexHeatmap Complete Reference. ComplexHeatmap Complete Reference. https://jokergoo.github.io/ComplexHeatmap-reference/book/
  33. Kolde, R. (2019). pheatmap: Pretty Heatmaps. Pheatmap: Pretty Heatmaps. https://cran.r-project.org/web/packages/pheatmap/index.html
  34. Adhikari, A., Nandi, S., Bhattacharya, I., Roy, M. De, Mandal, T. y Dutta, S. (2015). Phylogenetic analysis based evolutionary study of 16S rRNA in known Pseudomonas sp. Bioinformation, 11(10), 474-480. doi: https://doi.org/10.6026/97320630011474
  35. Perazzolli, M., Antonielli, L., Storari, M., Puopolo, G., Pancher, M., Giovannini, O., Pindo, M. y Pertot, I. (2014). Resilience of the natural phyllosphere microbiota of the grapevine to chemical and biological pesticides. Applied and Environmental Microbiology, 80(12), 3585-3596. doi: https://doi.org/10.1128/AEM.00415-14
  36. Gdanetz, K. y Trail, F. (2017). The wheat microbiome under four management strategies, and potential for endophytes in disease protection. Phytobiomes Journal, 1(3), 158-168. doi: https://doi.org/10.1094/PBIOMES-05-17-0023-R
  37. Wagner, M. R., Busby, P. E. y Balint-Kurti, P. (2020). Analysis of leaf microbiome composition of near-isogenic maize lines differing in broad-spectrum disease resistance. New Phytologist, 225(5), 2152-2165. doi: https://doi.org/10.1111/nph.16284
  38. Griffiths, S. M., Galambao, M., Rowntree, J., Goodhead, I., Hall, J., O"™Brien, D., Atkinson, N. y Antwis, R. E. (2020). Complex associations between cross-kingdom microbial endophytes and host genotype in ash dieback disease dynamics. Journal of Ecology, 108(1), 291-309. doi: https://doi.org/10.1111/1365-2745.13302
  39. Luo, L., Zhang, Z., Wang, P., Han, Y., Jin, D., Su, P., Tan, X., Zhang, D., Muhammad-Rizwan, H., Lu, X. y Liu, Y. (2019). Variations in phyllosphere microbial community along with the development of angular leaf-spot of cucumber. AMB Express, 9(1). doi: https://doi.org/10.1186/s13568-019-0800-y
  40. Zhang, Z., Kong, X., Jin, D., Yu, H., Zhu, X., Su, X., Wang, P., Zhang, R., Jia, M. y Deng, Y. (2019). Euonymus japonicus phyllosphere microbiome is significantly changed by powdery mildew. Archives of Microbiology, 201(8), 1099-1109. https://doi.org/10.1007/s00203-019-01683-3
  41. Zhang, Z., Luo, L., Tan, X., Kong, X., Yang, J., Wang, D., Zhang, D., Jin, D., y Liu, Y. (2018). Pumpkin powdery mildew disease severity influences the fungal diversity of the phyllosphere. PeerJ, 2018(4), 1-16. doi: https://doi.org/10.7717/peerj.4559
  42. Hesse, C., Schulz, F., Bull, C. T., Shaffer, B. T., Yan, Q., Shapiro, N., Hassan, K. A., Varghese, N., Elbourne, L. D. H., Paulsen, I. T., Kyrpides, N., Woyke, T. y Loper, J. E. (2018). Genome-based evolutionary history of Pseudomonas spp. Environmental Microbiology, 20(6), 2142-2159. doi: https://doi.org/10.1111/1462-2920.14130
  43. Katagiri, F., Thilmony, R. y He, S. Y. (2002). The Arabidopsis thaliana-pseudomonas syringae interaction. The Arabidopsis Book, 1, e0039. doi: https://doi.org/10.1199/tab.0039
  44. Selvaraj, S., Ganeshamoorthi, P., Anand, T., Raguchander, T., Seenivasan, N., & Samiyappan, R. (2014). Evaluation of a liquid formulation of Pseudomonas fluorescens against Fusarium oxysporum f. sp. cubense and Helicotylenchus multicinctus in banana plantation. BioControl, 59, 345-355. doi: https://doi.org/10.1007/s10526-014-9569-8
  45. Bubici, G., Kaushal, M., Prigigallo, M. I., Gómez-Lama Cabanás, C. y Mercado-Blanco, J. (2019). Biological Control Agents Against Fusarium Wilt of Banana. Frontiers in Microbiology, 10, 616. doi: https://doi.org/10.3389/fmicb.2019.00616
  46. Akila, R., Rajendran, L., Harish, S., Saveetha, K., Raguchander, T. y Samiyappan, R. (2011). Combined application of botanical formulations and biocontrol agents for the management of Fusarium oxysporum f. sp. cubense (Foc) causing Fusarium wilt in banana. Biological Control, 57(3), 175-183. doi: https://doi.org/10.1016/j.biocontrol.2011.02.010