Sporocarp-associated fungal co-occurrence networks in a corn field revealed by long-read high-throughput sequencing

Teng Yang , Luyao Song , Xu Liu , Xia Luo , Qiuyan Tan , Cunzhi Zhang , Jonathan M. Adams , Haiyan Chu

Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240245

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Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240245 DOI: 10.1007/s42832-024-0245-3
RESEARCH ARTICLE

Sporocarp-associated fungal co-occurrence networks in a corn field revealed by long-read high-throughput sequencing

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Abstract

In forests, fungal sporocarps house the diverse fungicolous fungi; however, the relationships of sporocarps and associated fungal communities are rarely explored in agroecosystems. In a corn field near Gongzhuling City, Jilin Province, China, we found an epigeous sporocarp with agaricoid morphology that could grow next to the living corn plants. Using PacBio metabarcoding combined with an updated bioinformatic pipeline, we surveyed the fungal community profile along its cap, rhizomorph and hyphosphere soil at a much-improved taxonomic resolution. We identified the sporocarp, at a high probability, as Agrocybe dura, and this mushroom was significantly negatively correlated with Trichoderma hamatum and T. harzianum in the co-occurrence network. Fungal diversity in hyphosphere habitat was significantly higher than that in cap and rhizomorph habitats. Consistent with the pattern in fungal diversity, the node number, edge number, network diameter and average degree were significantly higher in hyphosphere habitat than other habitats. However, both the negative and positive cohesion were significantly higher in rhizomorph habitat than other habitats. Moreover, the z-c plot identified A. dura as the only network hub, linking multiple fungal species. The results give us a glimpse of the ecological relevance of saprobic mushrooms across the extensive northeastern black soil region of China. Our findings will aid in the assessment and forecasting of fungal diversity hotspots and their relationships with soil fertility in the ‘Golden Corn Belt’ of northeast China.

Graphical abstract

Keywords

PacBio metabarcoding / saprobic mushroom / species identification / co-occurrence network / corn field / northeast China

Highlight

● We identified a sporocarp as Agrocybe dura growing next to a living corn using PacBio sequencing.

● The mycoparasitism of Trichoderma spp. on A. dura were revealed by the co-occurrence network analysis.

● For long-read HTS data, we updated a bioinformatic pipeline to enhance fungal taxonomic resolution.

Cite this article

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Teng Yang, Luyao Song, Xu Liu, Xia Luo, Qiuyan Tan, Cunzhi Zhang, Jonathan M. Adams, Haiyan Chu. Sporocarp-associated fungal co-occurrence networks in a corn field revealed by long-read high-throughput sequencing. Soil Ecology Letters, 2024, 6(4): 240245 DOI:10.1007/s42832-024-0245-3

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References

[1]

Baldrian, P., Větrovský, T., Lepinay, C., Kohout, P., 2022. High-throughput sequencing view on the magnitude of global fungal diversity. Fungal Diversity114, 539–547.

[2]

Banerjee, S., Zhao, C., Garland, G., Edlinger, A., García-Palacios, P., Romdhane, S., Degrune, F., Pescador, D.S., Herzog, C., Camuy-Velez, L.A., Bascompte, J., Hallin, S., Philippot, L., Maestre, F.T., Rillig, M.C., Van Der Heijden, M.G.A., 2024. Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe. Nature Communications15, 327.

[3]

Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: an open source software for exploring and manipulating networks. In: Proceedings of the International AAAI Conference on Web and Social Media. San Jose: AAAI, 361–362

[4]

Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods7, 335–336.

[5]

Das, K., Ghosh, A., Chakraborty, D., Datta, S., Bera, I., Layola, R., Banu, F., Vizzini, A., Wisitrassameewong, K., 2023. Four novel species and two new records of boletes from India. Journal of Fungi9, 754.

[6]

Deng, Y., Jiang, Y.H., Yang, Y.F., He, Z.L., Luo, F., Zhou, J.Z., 2012. Molecular ecological network analyses. BMC Bioinformatics13, 113.

[7]

Duan, Y., Chen, L., Li, Y.M., Li, J.Y., Zhang, C.Z., Ma, D.H., Zhou, G.X., Zhang, J.B., 2023. Nitrogen input level modulates straw-derived organic carbon physical fractions accumulation by stimulating specific fungal groups during decomposition. Soil and Tillage Research225, 105560.

[8]

Edgar, R.C., 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods10, 996–998.

[9]

Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics27, 2194–2200.

[10]

Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology10, 538–550.

[11]

Frąc, M., Hannula, S.E., Bełka, M., Jędryczka, M., 2018. Fungal biodiversity and their role in soil health. Frontiers in Microbiology9, 707.

[12]

Friedman, J., Alm, E.J., 2012. Inferring correlation networks from genomic survey data. PLoS Computational Biology8, e1002687.

[13]

Gábor, C., Nepusz, T., 2006. The igraph software package for complex network research. InterJournal Complex Systems1695, 1.

[14]

Gan, H.Y., Li, X.C., Wang, Y.L., Lü, P.P., Ji, N.N., Yao, H., Li, S., Guo, L.D., 2022. Plants play stronger effects on soil fungal than bacterial communities and co-occurrence network structures in a subtropical tree diversity experiment. Microbiology Spectrum10, e00134–22.

[15]

Hatvani, L., Antal, Z., Manczinger, L., Szekeres, A., Druzhinina, I.S., Kubicek, C.P., Nagy, A., Nagy, E., Vágvölgyi, C., Kredics, L., 2007. Green mold diseases of Agaricus and Pleurotus spp. are caused by related but phylogenetically different Trichoderma species. Phytopathology97, 532–537.

[16]

Hernandez, D.J., David, A.S., Menges, E.S., Searcy, C.A., Afkhami, M.E., 2021. Environmental stress destabilizes microbial networks. The ISME Journal15, 1722–1734.

[17]

Herren, C.M., McMahon, K.D., 2017. Cohesion: a method for quantifying the connectivity of microbial communities. The ISME Journal11, 2426–2438.

[18]

Jayasiri, S.C., Hyde, K.D., Ariyawansa, H.A., Bhat, J., Buyck, B., Cai, L., Dai, Y.C., Abd-Elsalam, K.A., Ertz, D., Hidayat, I., Jeewon, R., Jones, E.B.G., Bahkali, A.H., Karunarathna, S.C., Liu, J.K., Luangsa-Ard, J.J., Lumbsch, H.T., Maharachchikumbura, S.S.N., McKenzie, E.H.C., Moncalvo, J.M., Ghobad-Nejhad, M., Nilsson, H., Pang, K.L., Pereira, O.L., Phillips, A.J.L., Raspé, O., Rollins, A.W., Romero, A.I., Etayo, J., Selçuk, F., Stephenson, S.L., Suetrong, S., Taylor, J.E., Tsui, C.K.M., Vizzini, A., Abdel-Wahab, M.A., Wen, T.C., Boonmee, S., Dai, D.Q., Daranagama, D.A., Dissanayake, A.J., Ekanayaka, A.H., Fryar, S.C., Hongsanan, S., Jayawardena, R.S., Li, W.J., Perera, R.H., Phookamsak, R., De Silva, N.I., Thambugala, K.M., Tian, Q., Wijayawardene, N.N., Zhao, R.L., Zhao, Q., Kang, J.C., Promputtha, I., 2015. The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Diversity74, 3–18.

[19]

Karunarathna, S.C., Ashwath, N., Jeewon, R., 2021. Editorial: the potential of fungi for enhancing crops and forestry systems. Frontiers in Microbiology12, 813051.

[20]

Kou, X.C., Morriën, E., Tian, Y.J., Zhang, X.K., Lu, C.Y., Xie, H.T., Liang, W.J., Li, Q., Liang, C., 2023. Exogenous carbon turnover within the soil food web strengthens soil carbon sequestration through microbial necromass accumulation. Global Change Biology29, 4069–4080.

[21]

Krah, F.S., 2023. The unresolved ecological and evolutionary role of fungal fruit body coloration. Frontiers in Ecology and Evolution11, 1326710.

[22]

Liu, X., Zhang, C.Z., Yang, T., Gao, G.F., Shi, Y., Chu, H.Y., 2023. Phylogenetic relatedness enhances the understanding of soil microbial coexistence in alpine wetlands of the Tibetan Plateau. Soil Biology and Biochemistry185, 109160.

[23]

Ma, Y.J., Gao, W.Q., Zhang, F., Zhu, X.T., Kong, W.B., Niu, S.Q., Gao, K., Yang, H.Q., 2022. Community composition and trophic mode diversity of fungi associated with fruiting body of medicinal Sanghuangporus vaninii. BMC Microbiology22, 251.

[24]

Ma, Y.Y., Zhang, H.C., Wang, D.Z., Guo, X.S., Yang, T., Xiang, X.J., Walder, F., Chu, H.Y., 2021. Differential responses of arbuscular mycorrhizal fungal communities to long-term fertilization in the wheat rhizosphere and root Endosphere. Applied and Environmental Microbiology87, e0034921.

[25]

Maurice, S., Arnault, G., Nordén, J., Botnen, S.S., Miettinen, O., Kauserud, H., 2021. Fungal sporocarps house diverse and host-specific communities of fungicolous fungi. The ISME Journal15, 1445–1457.

[26]

Mešić, A., Šamec, D., Jadan, M., Bahun, V., Tkalčec, Z., 2020. Integrated morphological with molecular identification and bioactive compounds of 23 Croatian wild mushrooms samples. Food Bioscience37, 100720.

[27]

Mikryukov, V., Dulya, O., Zizka, A., Bahram, M., Hagh-Doust, N., Anslan, S., Prylutskyi, O., Delgado-Baquerizo, M., Maestre, F.T., Nilsson, H., Pärn, J., Öpik, M., Moora, M., Zobel, M., Espenberg, M., Mander, Ü., Khalid, A.N., Corrales, A., Agan, A., Vasco-Palacios, A.M., Saitta, A., Rinaldi, A., Verbeken, A., Sulistyo, B., Tamgnoue, B., Furneaux, B., Duarte Ritter, C., Nyamukondiwa, C., Sharp, C., Marín, C., Gohar, D., Klavina, D., Sharmah, D., Dai, D.Q., Nouhra, E., Biersma, E.M., Rähn, E., Cameron, E., De Crop, E., Otsing, E., Davydov, E., Albornoz, F., Brearley, F., Buegger, F., Zahn, G., Bonito, G., Hiiesalu, I., Barrio, I., Heilmann-Clausen, J., Ankuda, J., Doležal, J., Kupagme, J., Maciá-Vicente, J., Djeugap Fovo, J., Geml, J., Alatalo, J., Alvarez-Manjarrez, J., Põldmaa, K., Runnel, K., Adamson, K., Bråthen, K.A., Pritsch, K., Tchan Issifou, K., Armolaitis, K., Hyde, K., Newsham, K.K., Panksep, K., Lateef, A.A., Hansson, L., Lamit, L., Saba, M., Tuomi, M., Gryzenhout, M., Bauters, M., Piepenbring, M., Wijayawardene, N.N., Yorou, N., Kurina, O., Mortimer, P., Meidl, P., Kohout, P., Puusepp, R., Drenkhan, R., Garibay-Orijel, R., Godoy, R., Alkahtani, S., Rahimlou, S., Dudov, S., Põlme, S., Ghosh, S., Mundra, S., Ahmed, T., Netherway, T., Henkel, T., Roslin, T., Nteziryayo, V., Fedosov, V., Onipchenko, V., Yasanthika, W.A.E., Lim, Y., Van Nuland, M., Soudzilovskaia, N., Antonelli, A., Kõljalg, U., Abarenkov, K., Tedersoo, L., 2023. Connecting the multiple dimensions of global soil fungal diversity. Science Advances9, eadj8016.

[28]

Mukherjee, P.K., Mendoza-Mendoza, A., Zeilinger, S., Horwitz, B.A., 2022. Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biology Reviews39, 15–33.

[29]

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., Abarenkov, K., 2019. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research47, D259–D264.

[30]

Olesen, J.M., Bascompte, J., Dupont, Y.L., Jordano, P., 2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America104, 19891–19896.

[31]

Ondov, B.D., Bergman, N.H., Phillippy, A.M., 2011. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics12, 385.

[32]

Ovaskainen, O., Schigel, D., Ali-Kovero, H., Auvinen, P., Paulin, L., Nordén, B., Nordén, J., 2013. Combining high-throughput sequencing with fruit body surveys reveals contrasting life-history strategies in fungi. The ISME Journal7, 1696–1709.

[33]

Põlme, S., Abarenkov, K., Henrik Nilsson, R., Lindahl, B.D., Clemmensen, K.E., Kauserud, H., Nguyen, N., Kjøller, R., Bates, S.T., Baldrian, P., Frøslev, T.G., Adojaan, K., Vizzini, A., Suija, A., Pfister, D., Baral, H.O., Järv, H., Madrid, H., Nordén, J., Liu, J.K., Pawlowska, J., Põldmaa, K., Pärtel, K., Runnel, K., Hansen, K., Larsson, K.H., Hyde, K.D., Sandoval-Denis, M., Smith, M.E., Toome-Heller, M., Wijayawardene, N.N., Menolli, N., Reynolds, N.K., Drenkhan, R., Maharachchikumbura, S.S.N., Gibertoni, T.B., Læssøe, T., Davis, W., Tokarev, Y., Corrales, A., Soares, A.M., Agan, A., Machado, A.R., Argüelles-Moyao, A., Detheridge, A., De Meiras-Ottoni, A., Verbeken, A., Dutta, A.K., Cui, B.K., Pradeep, C.K., Marín, C., Stanton, D., Gohar, D., Wanasinghe, D.N., Otsing, E., Aslani, F., Griffith, G.W., Lumbsch, T.H., Grossart, H.P., Masigol, H., Timling, I., Hiiesalu, I., Oja, J., Kupagme, J.Y., Geml, J., Alvarez-Manjarrez, J., Ilves, K., Loit, K., Adamson, K., Nara, K., Küngas, K., Rojas-Jimenez, K., Bitenieks, K., Irinyi, L., Nagy, L.G., Soonvald, L., Zhou, L.W., Wagner, L., Aime, M.C., Öpik, M., Mujica, M.I., Metsoja, M., Ryberg, M., Vasar, M., Murata, M., Nelsen, M.P., Cleary, M., Samarakoon, M.C., Doilom, M., Bahram, M., Hagh-Doust, N., Dulya, O., Johnston, P., Kohout, P., Chen, Q., Tian, Q., Nandi, R., Amiri, R., Perera, R.H., Dos Santos Chikowski, R., Mendes-Alvarenga, R.L., Garibay-Orijel, R., Gielen, R., Phookamsak, R., Jayawardena, R.S., Rahimlou, S., Karunarathna, S.C., Tibpromma, S., Brown, S.P., Sepp, S.K., Mundra, S., Luo, Z.H., Bose, T., Vahter, T., Netherway, T., Yang, T., May, T., Varga, T., Li, W., Coimbra, V.R.M., De Oliveira, V.R.T., De Lima, V.X., Mikryukov, V.S., Lu, Y.Z., Matsuda, Y., Miyamoto, Y., Kõljalg, U., Tedersoo, L., 2020. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity105, 1–16.

[34]

R Core Team., 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. available at the website of R-project.org.

[35]

Royse, D.J., Baars, J., Tan, Q., 2017. Current Overview of Mushroom Production in the World. In: Diego, C.Z., Pardo-Giménez, A., eds. Edible and Medicinal Mushrooms: Technology and Applications. Hoboken: John Wiley & Sons, 5–13

[36]

Runnel, K., Abarenkov, K., Copoț, O., Mikryukov, V., Kõljalg, U., Saar, I., Tedersoo, L., 2022. DNA barcoding of fungal specimens using PacBio long-read high-throughput sequencing. Molecular Ecology Resources22, 2871–2879.

[37]

Sahithya K., Mouli T., Ankita B., Mercy Scorlet T., 2022. Remediation potential of mushrooms and their spent substrate against environmental contaminants: an overview. Biocatalysis and Agricultural Biotechnology 42, 102323

[38]

Sharma, R., 2017. Ectomycorrhizal mushrooms: their diversity, ecology and practical applications, In: Varma, A., Prasad, R., Tuteja, N., eds. Mycorrhiza - Function, Diversity, State of the Art. 4th ed. Cham: Springer, 99–131

[39]

Shendure, J., Balasubramanian, S., Church, G.M., Gilbert, W., Rogers, J., Schloss, J.A., Waterston, R.H., 2017. DNA sequencing at 40: past, present and future. Nature550, 345–353.

[40]

Sun, J.Z., Liu, X.Z., McKenzie, E.H.C., Jeewon, R., Liu, J.K., Zhang, X.L., Zhao, Q., Hyde, K.D., 2019. Fungicolous fungi: terminology, diversity, distribution, evolution, and species checklist. Fungal Diversity95, 337–430.

[41]

Tedersoo, L., Albertsen, M., Anslan, S., Callahan, B., 2021a. Perspectives and benefits of high-throughput long-read sequencing in microbial ecology. Applied and Environmental Microbiology87, e0062621.

[42]

Tedersoo, L., Anslan, S., 2019. Towards PacBio-based pan-eukaryote metabarcoding using full-length ITS sequences. Environmental Microbiology Reports11, 659–668.

[43]

Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N.S., Wijesundera, R., Villarreal Ruiz, L., Vasco-Palacios, A.M., Thu, P.Q., Suija, A., Smith, M.E., Sharp, C., Saluveer, E., Saitta, A., Rosas, M., Riit, T., Ratkowsky, D., Pritsch, K., Põldmaa, K., Piepenbring, M., 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., Anslan, S., Abell, S., Abarenkov, K., 2014. Fungal biogeography. Global diversity and geography of soil fungi. Science346, 1256688.

[44]

Tedersoo, L., Bahram, M., Zinger, L., Nilsson, R.H., Kennedy, P.G., Yang, T., Anslan, S., Mikryukov, V., 2022. Best practices in metabarcoding of fungi: From experimental design to results. Molecular Ecology31, 2769–2795.

[45]

Tedersoo, L., Mikryukov, V., Anslan, S., Bahram, M., Khalid, A.N., Corrales, A., Agan, A., Vasco-Palacios, A.M., Saitta, A., Antonelli, A., Rinaldi, A.C., Verbeken, A., Sulistyo, B.P., Tamgnoue, B., Furneaux, B., Ritter, C.D., Nyamukondiwa, C., Sharp, C., Marín, C., Dai, D.Q., Gohar, D., Sharmah, D., Biersma, E.M., Cameron, E.K., De Crop, E., Otsing, E., Davydov, E.A., Albornoz, F.E., Brearley, F.Q., Buegger, F., Gates, G., Zahn, G., Bonito, G., Hiiesalu, I., Hiiesalu, I., Zettur, I., Barrio, I.C., Pärn, J., Heilmann-Clausen, J., Ankuda, J., Kupagme, J.Y., Sarapuu, J., Maciá-Vicente, J.G., Fovo, J.D., Geml, J., Alatalo, J.M., Alvarez-Manjarrez, J., Monkai, J., Põldmaa, K., Runnel, K., Adamson, K., Bråthen, K.A., Pritsch, K., Tchan, K.I., Armolaitis, K., Hyde, K.D., Newsham, K.K., Panksep, K., Adebola, L.A., Lamit, L.J., Saba, M., Da Silva Cáceres, M.E., Tuomi, M., Gryzenhout, M., Bauters, M., Bálint, M., Wijayawardene, N., Hagh-Doust, N., Yorou, N.S., Kurina, O., Mortimer, P.E., Meidl, P., Nilsson, R.H., Puusepp, R., Casique-Valdés, R., Drenkhan, R., Garibay-Orijel, R., Godoy, R., Alfarraj, S., Rahimlou, S., Põlme, S., Dudov, S.V., Mundra, S., Ahmed, T., Netherway, T., Henkel, T.W., Roslin, T., Fedosov, V.E., Onipchenko, V.G., Yasanthika, W.A.E., Lim, Y.W., Piepenbring, M., Klavina, D., Kõljalg, U., Abarenkov, K., 2021b. The global soil Mycobiome consortium dataset for boosting fungal diversity research. Fungal Diversity111, 573–588.

[46]

Tian, M., Whalley, W.R., Zhou, H., Ren, T.S., Gao, W.D., 2023. Does no-tillage mitigate the negative effects of harvest compaction on soil pore characteristics in Northeast China? Soil and Tillage Research 233, 105787

[47]

Torbati, M., Arzanlou, M., Da Silva Santos, A.C., 2021. Fungicolous Fusarium species: ecology, diversity, isolation, and identification. Current Microbiology78, 2850–2859.

[48]

Větrovský, T., Morais, D., Kohout, P., Lepinay, C., Algora, C., Awokunle Hollá, S., Bahnmann, B.D., Bílohnědá, K., Brabcová, V., D'Alò, F., Human, Z.R., Jomura, M., Kolařík, M., Kvasničková, J., Lladó, S., López-Mondéjar, R., Martinović, T., Mašínová, T., Meszárošová, L., Michalčíková, L., Michalová, T., Mundra, S., Navrátilová, D., Odriozola, I., Piché-Choquette, S., Štursová, M., Švec, K., Tláskal, V., Urbanová, M., Vlk, L., Voříšková, J., Žifčáková, L., Baldrian, P., 2020. GlobalFungi, a global database of fungal occurrences from high-throughput-sequencing metabarcoding studies. Scientific Data7, 228.

[49]

Wang, C., Wang, X., Zhang, Y., Morrissey, E., Liu, Y., Sun, L.F., Qu, L.R., Sang, C.P., Zhang, H., Li, G.C., Zhang, L.L., Fang, Y.T., 2023a. Integrating microbial community properties, biomass and necromass to predict cropland soil organic carbon. ISME Communications3, 86.

[50]

Wang, G.W., Jin, Z.X., George, T.S., Feng, G., Zhang, L., 2023b. Arbuscular mycorrhizal fungi enhance plant phosphorus uptake through stimulating hyphosphere soil microbiome functional profiles for phosphorus turnover. New Phytologist238, 2578–2593.

[51]

Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology73, 5261–5267.

[52]

Wang, S., Huang, X.L., Zhang, Y., Yin, C.B., Richel, A., 2021. The effect of corn straw return on corn production in Northeast China: an integrated regional evaluation with meta-analysis and system dynamics. Resources, Conservation and Recycling167, 105402.

[53]

Wen, D.Z., Liang, W.J., 2001. Soil fertility quality and agricultural sustainable development in the black soil region of northeast China. Environment, Development and Sustainability3, 31–43.

[54]

Wen, Y.A., Li, X.C., Mu, H.W., Zhong, L.H., Chen, H., Zeng, Y.L., Miao, S.X., Su, W., Gong, P., Li, B.G., Huang, J.X., 2022. Mapping corn dynamics using limited but representative samples with adaptive strategies. ISPRS Journal of Photogrammetry and Remote Sensing190, 252–266.

[55]

Wu, D., Ma, Y.Y., Yang, T., Gao, G.F., Wang, D.Z., Guo, X.S., Chu, H.Y., 2022. Phosphorus and zinc are strongly associated with belowground fungal communities in wheat field under long-term fertilization. Microbiology Spectrum10, e0011022.

[56]

Xiong, C., Singh, B.K., He, J.Z., Han, Y.L., Li, P.P., Wan, L.H., Meng, G.Z., Liu, S.Y., Wang, J.T., Wu, C.F., Ge, A.H., Zhang, L.M., 2021. Plant developmental stage drives the differentiation in ecological role of the maize microbiome. Microbiome9, 171.

[57]

Xue, R., Wang, C., Zhao, L., Cao, J., Liu, M.L., Zhang, D., 2023. Agricultural intensification weakens soil multifunctionality by reducing fungal diversity. Applied Soil Ecology189, 104900.

[58]

Yang, T., Tedersoo, L., Liu, X., Gao, G.F., Dong, K., Adams, J.M., Chu, H.Y., 2022. Fungi stabilize multi-kingdom community in a high elevation timberline ecosystem. iMeta1, e49.

[59]

Yang, T., Tedersoo, L., Soltis, P.S., Soltis, D.E., Sun, M., Ma, Y.Y., Ni, Y.Y., Liu, X., Fu, X., Shi, Y., Lin, H.Y., Zhao, Y.P., Fu, C.X., Dai, C.C., Gilbert, J.A., Chu, H.Y., 2023. Plant and fungal species interactions differ between aboveground and belowground habitats in mountain forests of eastern China. Science China Life Sciences66, 1134–1150.

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