Mycobiome in soils from irrigated, rice-based farming systems in Apalit, Pampanga and Banaue, Ifugao, Philippines: Diversity and potential agro-biotechnological applications determined using targeted metagenomics
Article Sidebar
Main Article Content
Abstract
Mycobiomes of soils from two irrigated, rice-based farming systems in the Philippines, one in Apalit, Pampanga and another in Banaue, Ifugao, were assessed and compared through targeted metagenomics. The different phyla identified in this study were Aphelidiomycota, Ascomycota, Basidiomycota, Chytridiomycota, Entorrhizomycota, Glomeromycota Monoblepharomycota, Mortierellomycota, and Rozellomycota. All except Aphelidomycota were found in both sites. The most abundant fungal genera observed were Arnium, Fusarium, Neurospora, Talaromces, unidentified Pleosporales (Ascomycota), Saitozyma, Westerdykella, Massariosphaeria, Boothiomyces, Nakataea, Penicillium, unidentified Sordariales (Ascomycota), unidentified Sordariomycetes (Ascomycota), unidentified (Rozellomycota), unidentified Chytridiomycota, and the unidentified fungal genus. These phyla and genera had varying relative abundances and dominance across rice cultivations stages in the sites. The unidentified fungal phylum in the sites had sizeable abundances across rice cultivation stages in both sites that indicate its possible importance in these areas. Samples from Banaue, Ifugao had greater species richness and evenness compared to those from Apalit, Pampanga based on Chao1, Fisher, Shannon, and Simpson alpha diversity indices. The fungal diversities of both sites were different based on their weighted and unweighted Unifrac distances and PCoA ordination plot. Soil chemical characteristics did not correlate to fungal diversity collectively in each site but correlated well with specific taxonomic compositions at the phylum and genus levels. The uncovered composition and variation of mycobiomes of soils in these sites may help provide information for those seeking potential solutions to challenges faced in the sites and similar irrigated, rice-based farming systems such as low grain yield, pests, or diseases
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Akoglu, H. (2018). User’s guide to correlation coefficients. Turkish Journal of Emergency Medicine, 18:91-93.
Babu, A. G., Kim, S. W., Yadav, D. R., Hyum, U., Adhikari, M. and Lee, Y. S. (2015). Penicillium menonorum: A Novel Fungus to Promote Growth and Nutrient Management in Cucumber Plants. Mycobiology, 43:49-56.
Bhattacharjee, A., Qafoku, O., Richardson, J. A., Anderson, L. N., Schwarz, K., Bramer, L. M., Lomas, G. X., Orton, D. J., Zhu, Z., Engelhard, M. H., Bowden, M. E., Nelson, W. C., Jumpponen A., Jansson, J. K., Hofmockel, K. S. and Anderton, C. R. (2021). Fungal Mineral Weathering Mechanisms Revealed Through Direct Molecular Visualization. bioRxiv. Retrieved from https://doi.org/10.1101/2021.10.01.462718.
Bolyen., E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J. E., Bittinger, K., Brejnrod, A., Brislawn, C. J., Brown, C. T, Callahan, B. J., Caraballo-Rodríguez, A. M., Chase, J., Cope, E. L., Da Silva, R., Diener, C., Dorrestein, P. C,. Douglas, G. M., Durall, D. M., Duvallet, C., Edwardson, C. F., Ernst, M., Estaki, M., Fouquier, J., Gauglitz, J. M., Gibbons, S. M., Gibson, D. L., Gonzalez, A., Gorlick, K., Guo, J., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G. A., Janssen, S., Jarmusch, A. K, Jiang, L., Kaehler, B. D., Kang, K. B., Keefe, C. R., Keim, P., Kelley, S. T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M. G. I., Lee, J., Ley, R., Liu, X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B. D., Mcdonald, D., Mciver, L. J, Melnik, A. V., Metcalf, J. L, Morgan, S. C, Morton, J. T., Naimey, A. T., Navas-Molina, J. A., Nothias, L. F., Orchanian, S. B., Pearson, T., Peoples, S. L, Petras, D., Preuss, M. L, Pruesse, E., Rasmussen, L. B, Rivers, A., Robeson, M. S., Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S. J., Spear, J. R., Swafford, A., Thompson, L. R., Torres, P. J., Trinh, P., Tripathi, A., Turnbaugh, P. J, Ul-Hasan, S., Van Der Hooft, J. J. J., Vargas, F., Vázquez-Baeza, Y., Vogtmann, E., Von Hippel, M., Walters, W., Wan, Y., Wang, M., Warren J, . Weber, K C., Williamson C. H. D., Willis, A. D., Xu, Z., Zaneveld, J. R., Zhang, Y., Zhu, Q., Knight, R. and Caporaso, J. G. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37:852-857.
Cai, S., Lv, W., Zhu, H., Zhang, D., Fu, Z., Zhang, H. and Xu S. (2019). Effect of nitrogen application rate on soil fungi community structure in a rice-fish mutualistic system. Scientific Reports, 9:16188.
Canini, F., Geml, J., D’acqui, L. P., Selbmann, L., Onofri, S., Ventura, S. and Zucconi, L. (2020). Exchangeable cations and pH drive diversity and functionality of fungal communities in biological soil crusts from coastal sites of Victoria Land, Antarctica. Fungal Ecology, 45:100923.
Chaer, G., Fernandes, M., Myrold, D. and Bottomley, P. (2009). Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils. Microbial Ecolology, 58:414-424.
Chao, A. and Chiu, C. H. (2014). Species Richness: Estimation and Comparison. Wiley StatsRef: Statistics Reference Online 1-26. Retrieved from https://doi.org/10.1002/9781118445112.stat03432.pub2.
Chethana, K. W. T., Jayawardena, R. S. and Hyde, K. D. (2020). Hurdles in fungal taxonomy: Effectiveness of recent methods in discriminating taxa. Megataxa, 001:114-122.
Dalefield, R. (2017). Mycotoxins and Mushrooms. In: Dalefield, R. (ed.) Veterinary Toxicology for Australia and New Zealand. Elsevier. pp. 373-419.
De Mattos-Shipley, K. M. J., Ford, K. L, Alberti, F., Banks, A. M., Bailey, G. D. and Foster, G. D. (2016). The good, the bad and the tasty: The many roles of mushrooms. Studies in Mycology, 85:125-127.
De Vries, F. T., Bloem, J., Van Eekeren, N., Brusaard, L. and Hoffland, E. (2007). Fungal biomass in pastures increases with age and reduced N input. Soil Biology and Biochemistry, 39:1620-1630.
Deb, D., Khan, A. and Dey, N. (2020). Phoma diseases: Epidemiology and control. Plant Pathoogy, 69:1203-1217.
Dellagi, A., Quillere, I., and Hirel, B. (2020). Beneficial soil-borne bacteria and fungi: a promising way to improve plant nitrogen acquisition. Journal of Experimental Botany 71:4469-4479.
Eide, D. J. (2006). Zinc transporters and the cellular trafficking of zinc. Biochimica et Biophysica Acta (BBA) –Molecular Cell Research, 1763:711-722.
Fisher, R., Corbet, A. and Williams, C. (1943). The relation between the number of species and the number of individuals in a random sample of an animal population. Journal of Animal Ecology, 12:42-58.
Flannigan, B. and Miller, J. D. (2001). Microbial growth in indoor environments. In: Flannigan, B., Samson R. A., Miller, J. D. (eds) Microorganisms in Home and Indoor Work Environments: Diversity, Health Impacts, Investigation and Control. New York: Taylor and Francis, pp.35-67.
Fogle, M. R., Douglas, D. R., Jumper, C. A. and Straus, D. C. (2008). Growth and mycotoxin production by Chaetomium globosum is favored in a neutral pH. International Journal of Molecular Sciences, 9:2357-2365.
Garbeva, P., Van Veen, J. A. and Van Elsas, J. D. (2004). Microbial Diversity in Soil: Selection of Microbial Populations by Plant and Soil Type and Implications for Disease Suppressiveness. Annual Review of Phytopathology, 42:243-270.
Garcia, S., Pezzani, F. and Rodriguez-Blanco, A. (2017). Long-term phosphorus fertilization effects on arbuscular mycorrhizal fungal diversity in Uruguayan grasses. Journal of Soil Science and Plant Nutrition, 17:1013-1027.
Garcia-Aroca, T., Price, P. P, Tomaso-Peterson, M., Allen, T. W., Wilkerson, T. H., Spurlock, T. N., Faske, T. R., Bluhm, B., Conner, K., Sikora E., Guyer, R., Kelly, H., Squiers, B. M. and Doyle, V. P. (2021). Xylaria necrophora, sp. nov., is an emerging root-associated pathogen responsible for taproot decline of soybean in the southern United States. Mycologia, 113:326-347.
Gorte, O., Kugel, M. and Ochsenreither, K. (2020). Optimization of carbon source efficiency for lipid production with the oleaginous yeast Saitozyma podzolica DSM 27192 applying automated continuous feeding. Biotechnology for Biofuels, 13:181.
Guarro, J., Gené, J., Stchigel, A. M. and Figueras, M. J. (2012). Atlas of Soil Ascomycetes in: Samson, R. A., M. van den Hoeven-Verweij, R. Begerow, U. Braun, P. Cannon, L. Carris, P. W. Crous, D. M. Geiser, J. Z. Groenewald, D. S. Hibbett, L. L. Norvell, E. Parmasto, A. J. L Phillips, A. Y. Rossman, K. A. Seifert, H. D. Shin, R. Shivas, M. Stadler, J. K. Stone, R. C. Summerbell, B. Summerell and U. Thrane, eds., CBS Biodiversity Series 10, Utrecht, The Netherlands: CBS-KNAW Fungal Biodiversity Centre. 486 pp.
Jiang, G-Z., Gao, F., Zhu, G-Y., Zhang, Y-K., Duan B., Zhou, M., Liu, Y-X., and Cai, Z.Y. (2017). First Report of Leaf Spot Disease Caused by Chaetomium sp. on Hevea brasiliensis in Yunnan, China. Plant Disease, 102:453-453.
Kanse, O. S., Whitelaw-Weckert, M., Kadam, T. A. and Bhosale, H. J. (2015). Phosphate solubilization by stress-tolerant soil fungus Talaromyces funiculosus SLS8 isolated from the Neem rhizosphere. Annals of Microbiology, 65:85-93.
Khan, A. L. and Lee, I. J. (2013). Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L growth during copper stress. BMC Plant Biology, 131:86.
Khare, K. B., Otanga, R. R. N., Achwanya, O. S. and Otaye, D. O. (2012). Effect of Media, pH and temperature and sporulation of Cercospora zeae-maydies, the causal agent of grey leaf spot of maize. International Journal of Food, Agriculture and Veterinary Sciences, 2:87-90.
Kobayashi, T., Suto, Y. and De Guzman, E. D. (1979). Cercospora needle blight of pines in the Philippines. European Journal of Forest Pathology, 9:166-175.
Kõljalg, U., Nilsson, H. R., Schigel, D., Tedersoo, L., Larsson, K. H., May, T. W., Taylor, A. F. S., Jeppesen, T. S., Frøslev, T. G., Lindahl, B. D., Põldmaa, K., Saar, I., Suija, A., Savchenko, A., Yatsiuk, I., Adojaan, K., Ivanov, F., Piirmann, T., Pöhönen, R., Zirk, A. and Abarenkov, K. (2020). The Taxon Hypothesis Paradigm—On the Unambiguous Detection and Communication of Taxa. Microorganisms, 8:1910.
Lee, S. H, Lee, S. O., Jang, K. L. and Lee, T. H. (1995). Microbial flocculant from Arcuadendron sp. TS-49. Biotechnology Letters, 17:95-100.
Lekberg, Y., Arnillas, C. A., Borer, E. T., Bullington, L. S., Fierer, N., Kennedy, P. G., Leff, J. W., Luis, A. D., Seabloom, E. W. and Henning, J. A. (2021). Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils. Nature Communications, 12:3484.
Li, R., Li, M., Ashraf, U., Liu, S. and Zhang, J. (2019). Exploring the relationships between yield and yield-related traits for rice varieties released in China from 1978 to 2017. Frontiers in Plant Science, 10:543.
Li, Y., Steenwyk, J. L., Chang, Y., Wang, Y., James, T. Y., Stajich, J. E., Spatafora, J. W., Groenewald, M., Dunn, C. W., Hittinger, C. T., Shen, X-X. and Rokas, A. (2021). A genome-scale phylogeny of the kingdom Fungi. Current Biology, 31:1653-1665.
Liu, D., Liu, G., Chen, G., Wang, J. and Zhang, L. (2018). Soil pH determines fungal diversity along an elevation gradient in Southwestern China. Science China Life Sciences, 61:718-726.
Luo, X., Liu, J., Shen, Y., Yao, G., Yang, W., Mortimer, P. E. and Gui, H. (2021). Fungal Community Composition and Diversity Vary with Soil Horizons in a Subtropical Forest. Frontiers in Microbiology, 12:650440.
Maru, R., Leo, M. N. Z., Rahim, S. and Basram, N. F. (2016). Oldeman Climate Zoning for the Agricultural Area. Proceedings of ICMSTEA 2016: International Conference on Mathematics, Science, Technology, Education, and their Applications, Makassar, Indonesia, 3rd – 4th October 2016. pp.511-521.
Medeiros, A., Duarte, S., Pascoal, C., Cássio, F. and Graça, M. (2010). Effects of Zn, Fe and Mn on leaf litter breakdown by aquatic fungi: a microcosm study. International Review of Hydrobiology, 95:2-26.
Moreira, G. A. M. and Vale, H. M. M. (2018). Occurrence of yeast species in soils under native and modified vegetation in an iron mining area. Revista Brasileira de Ciênca do Solo, 42:e0170375.
Mostrom, M. (2011). Trichothecenes and zearalenone. In: Gupta, R.C. (ed.) Reproductive and Developmental Toxicology. pp: 739-751.
Naraghi, L., Heydari, A., Rezaee, S. and Razavi, M. (2012). Biocontrol Agent Talaromyces flavus Stimulates the Growth of Cotton and Potato. Journal of Plant Growth Regulation, 31:471-477.
Nearing, G., Atheendradas, Y., Crow, S., Zhan, W., Liu, X. J. and Chen, F. (2018). The efficiency of data assimilation. Water Resources Research, 54:6374-6392.
Nicoletti, R. and Becchimanzi, A. (2022). Talaromyces–Insect Relationships. Microorganisms, 10:45.
Nilsson, R. H., Larsson, K. H., Taylor, A. F. S., Bengtsson-Palme, J., Jeppesen, T. S., Schigel, D., Kennedy, P., Picard, K., Glöckner, F. O., Tedersoo, L., Saar, I., Kõljalg, U. and Abarenkov, K. (2018). The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research, 47:D259-D264.
Ortega, H. E., Torres-Mendoza, D. and Cubilla-Rios, L. (2020). Patents on Endophytic Fungi for Agriculture and Bio- and Phytoremediation Applications. Microorganisms 8:1237.
Outten, C. E., O'halloran, T. V. (2001). Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science, 292:2488-2492.
Pagani, M. A., Casamayor, A., Serrano, R., Atrian, S. and Arino, J. (2007). Disruption of iron homeostasis in Saccharomyces cerevisiae by high zinc levels: a genome-wide study. Molecular Microbiology, 65:521-537.
Palanog, A. D, Calayugan, M. I. C., Descalsota-Empleo, G. I., Amparado, A., Inabangan-Asilo, M. A., Arocena, E. C., Sta Cruz, P. C., Borromeo, T. H., Lalusin, A., Hernandez, J. E., Acuin, C. and Swamy, B. P. M. (2019). Zinc and iron nutrition status in the Philippines population and local soils. Frontiers in Nutrition, 6:81.
Pan, C. C., Liu, C. A., Zhao, H. L. and Wang, Y. (2013). Changes of soil physico-chemical properties and enzyme activities in relation to grassland salinization. European Journal of Soil Biology, 55:13-19.
Park, J-H., Cox-Ganser, J. M., Kreiss, K., White, S. K. and Rao, C. Y. (2008). Hydrophilic Fungi and Ergosterol Associated with Respiratory Illness in a Water-Damaged Building. Environmental Health Perspectives, 116:45-50.
Petrovič, U., Gunde-Cimerman, N. and Zalar, P. (2000). Xerotolerant mycobiota from high altitude Anapurna soil, Nepal, FEMS Microbiology Letters, 182:339-342.
Philippine Statistics Authority [PSA]. (2019). Rice and Corn Situation Outlook, January 2019 Round. Retrieved from https://psa.gov.ph/content/rice-and-corn-situation-and-outlook-reports.
Philippine Statistics Authority [PSA]. (2020). Palay and Corn Quarterly Bulletin, January 2020. Retrieved from https://psa.gov.ph/content/rice-and-corn-situation-and-outlook-reports.
Pietro-Souza, W., Mello, I. S., Vendruscullo, S. J., Da Silva, G. F., Da Cunha, C. N., White, J. F. and Soares, M. A. (2017). Endophytic fungal communities of Polygonum acuminatum and Aeschynomene fluminensis are influenced by soil mercury contamination. PLoS One, 12: e0182017. doi: 10.1371/J..pone.0182017.
PPQ. (2021). Cooperative Agricultural Pest Survey (CAPS) Pest Datasheet for Magnaporthiopsis maydis (Magnaporthaceae): Late wilt of corn. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine USDA-APHIS-PPQ, Raleigh, NC. Retrieved from http://download.ceris.purdue.edu/file/4121.
Radhakrishnan, R., Kang, S. M., Baek, I. Y. and Lee, I. J. (2014). Characterization of plant growth-promoting traits of Penicillium species against the effects of high soil salinity and root disease. Journal of Plant Interactions, 9:754-762.
Rodríguez-Andrade, E., Stchigel, A. M., Terrab, A. and Cano-Lira, J. F. (2019). Diversity of xerotolerant and xerophilic fungi in honey. IMA Fungus, 10:20.
Rousk, J., Brookes, P. C. and Bååth, E. (2009). Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Applied and environmental microbiology, 75:1589-1596.
Ryberg, M. and Nilsson, R. H. (2018). New light on names and naming of dark taxa. MycoKeys, 23:31-39.
Samson, R. A., Houbraken, J., Thrane, U., Frisvad, J. C. and Andersen, B. (2010). Food and Indoor Fungi, In: CBS Laboratory Manual Series. CBS KNAW Fungal Biodiversity Center. 390 pp.
Schulte, E. E. (2004). Soil and Applied Zinc. Wisconsin Corn Agronomy. Retrieved from http://corn.agronomy.wisc.edu/Management/pdfs/a2528.pdf.
Shannon, C. E. (1948). A mathematical theory of communication. The Bell System Technical Journal, 27:379-423.
Simpson, E. H. (1949). Measurement of diversity. Nature, 163:688.
Stošić, S., Ristić, D., Gašić, K., Starović, M., Ljaljević Grbić, M., Vukojević, J. and Živković, S. (2020). Talaromyces minioluteus: New Postharvest Fungal Pathogen in Serbia. Plant Disease, 104:656-667.
Tančić Živanov, S., Nešić, L., Jevtic, R., Belić, M., Ćirić, V., Lalošević, M. and Veselić, J. (2017). Fungal diversity as influenced by soil characteristics. Zemdirbyste-Agriculture, 104:305-310.
Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Youru, N. S., Wijesundera, R., Villarreal, L., Vasco-Palacios, R. M., Thu, P. Q, Suija, A., Smith, M. E., Sharp, C., Saluveer, E., Saitta, A., Rosas, M., Riit, T., Ratkowsky, D., Pritsch, K., Põldma, K., Piepenbring, A., Phosri, C., Peterson, M., Parts, K., Pärtel, K., Otsing, E., Nouhra, E., Njouonkou, A. L., Nilsson, R. H, Morgado, L. N, Mayor, J., May, T. W., Majuakim, L., Lodge, D. J., Lee, S. S., Larsson, K-H., Kohout, P., Hosaka, K., Hiiesalu, I., Henkel, T. W., Harend, H., Guo, L-D., Greslebin, A., Grelet, G., Geml, J., Gates, G., Dunstan, W., Dunk, C., Drenkhan, R., Dearnaley, J., De Kesel, A., Dang, T., Chen X., Buegger, F., Brearley, F. Q., Bonito, G., Anslans Sabell, A. and Abarenkov, K. (2014). Global diversity and geography of soil fungi. Science, 346:1256688–1256688
Thiem, D., Gołębiewski, M., Hulisz, P., Piernik, A. and Hrynkiewicz, K. (2018). How Does Salinity Shape Bacterial and Fungal Microbiomes of Alnus glutinosa Roots? Frontiers in Microbiology, 9:651.
Tian, Y-H., Peng, H-Y., Wang, D-H., Li, X-F., He, B-L. and Gao, K-X. (2020). Biocontrol potential of Talaromyces purpurogenus and its regulation on soil microbial community. Ying Yong Sheng Tai Xue Bao, 3255-3266.
Tilman, D., Balzer, C., Hill, J. and Befort, B. L. (2011). Global food demand and the sustainable intensification of agriculture. Proceedings of the National Academy of Sciences of the United States of America, 108:20260-20264.
Toghueo, R. M. K. and Boyom, F. F. (2020). Endophytic Penicillium species and their agricultural, biotechnological, and pharmaceutical applications. 3 Biotech, 10:107.
Wang, C., Chen, D., Shen, J., Yuan, Q., Fan, F., Wei, W., Li, Y. and Wu, J. (2021). Biochar alters soil microbial communities and potential functions 3–4 years after amendment in a double rice cropping system. Agriculture, Ecosystems & Environment, 311:107291.
Watanabe, K., Matsui, M., Honjo, H., Ole Becker J. and Fukui, R. (2011). Effects of soil pH on rhizoctonia damping-off of sugar beet and disease suppression induced by soil amendment with crop residues. Plant Soil, 347:255.
Whitelaw, M. A., Harden, T. J. and Helyar, K. R. (1999). Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biology & Biochemistry, 31:655-665.
Yamagiwa Y, Toyoda K, Inagaki Y, Ichinose Y, Hyakumachi M. and Shiraishi T. (2011). Talaromyces wortmannii FS2 emits β-caryophyllene, which promotes plant growth and induces resistance. Journal of General Plant Pathology, 77:336-341.
Yan, N., Marschner, P., Cao, W., Zuo, C. and Qin, W. (2015). Influence of salinity and water content on soil microorganisms. International Soil and Water Conservation Research, 3:316-323.
Yi, X-W., He, J., Sun, L-T., Liu, J-K., Wang, G-K. and Feng, T. (2021). 3-Decalinoyltetramic acids from kiwi-associated fungus Zopfiella sp. and their antibacterial activity against Pseudomonas syringae. RSC Advances, 11:18827-18831.
Yilmaz, N., López-Quintero, C. A., Vasco-Palacios, A. N., Frisvad, J. C., Theelen, B., Boekhout, T., Samson, R. A. and Houbraken, J. (2016). Four novel Talaromyces species isolated from leaf litter from Colombian Amazon rain forests. Mycological Progress, 15:1041-1056.
Yurkov, A. M. (2018). Yeasts of soil – obscure but precious. Yeast, 35:369-378.
Zhang, J. Y, He, J., Li, Z. H., Feng, T. and Liu, J. K. (2021). Zopfiellasins A-D, Two Pairs of Epimeric Cytochalasins from Kiwi-Associated Fungus Zopfiella sp. and their Antibacterial Assessment. Molecules, 26:5611.
Zhang, T., Chen, H. and Ruan, H. (2018). Global negative effects of nitrogen deposition on soil microbes. The ISME Journal, 12:1817-1825.
Zhao, C., Liu, B., Piao, S., Wang, X., Lobell, D.B., Huang, Y., Huang, M., Yao, Y., Bassu, S., Ciais, P., Durand, J-L., Elliott, J., Ewert, F., Janssens, I. A., Li, T., Lin, E., Liu, Q., Martre, P., Müller, C., Peng, S., Peñuelas, J., Ruane, A. C., Wallach, D., Wang, T., Wu, D., Liu, Z., Zhu, Y., Zhu, Z. and Asseng, S. (2017). Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences of the United States of America, 114:9326-9331.
Zhao, L., Zhao, W. and Deng, H. (2021). Effects of Talaromyces purpureogenus on Cucumber Growth Promotion and Its Mechanism. Journal of Bacteriology and Mycology, 8: 1173.
Žifčáková, L., Větrovský, T., Howe, A. and Baldrian, P. (2016). Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environmental Microbiology, 18:288-301.
