Plant community and soil properties drive arbuscular mycorrhizal fungal diversity: A case study in tropical forests

Jing Zhang, Changxin Quan, Lingling Ma, Guowei Chu, Zhanfeng Liu, Xuli Tang

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Soil Ecology Letters ›› 2021, Vol. 3 ›› Issue (1) : 52-62. DOI: 10.1007/s42832-020-0049-z
RESEARCH ARTICLE
RESEARCH ARTICLE

Plant community and soil properties drive arbuscular mycorrhizal fungal diversity: A case study in tropical forests

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Abstract

The mutual interdependence of plants and arbuscular mycorrhizal fungi (AMF) is important in carbon and mineral nutrient exchange. However, an understanding of how AMF community assemblies vary in different forests and the underlying factors regulating AMF diversity in native tropical forests is largely unknown. We explored the AMF community assembly and the underlying factors regulating AMF diversity in a young (YF) and an old-growth forest (OF) in a tropical area. The results showed that a total of 53 AMF phylogroups (virtual taxa, VTs) were detected, 38±1 in the OF and 34±1 in the YF through high-throughput sequencing of 18S rDNA, and AMF community composition was significantly different between the two forests. A structural equation model showed that the forest traits indirectly influenced AMF diversity via the plant community, soil properties and microbes, which explained 44.2% of the total observed variation in AMF diversity. Plant diversity and biomass were the strongest predictors of AMF diversity, indicating that AMF diversity was dominantly regulated by biotic factors at our study sites. Our study indicated that forest community traits have a predictable effect on the AMF community; plant community traits and soil properties are particularly important for determining AMF diversity in tropical forests.

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Keywords

Arbuscular mycorrhizal fungi / High-throughput sequencing / Microbes / Plant community traits / Soil properties / Tropical forests

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Jing Zhang, Changxin Quan, Lingling Ma, Guowei Chu, Zhanfeng Liu, Xuli Tang. Plant community and soil properties drive arbuscular mycorrhizal fungal diversity: A case study in tropical forests. Soil Ecology Letters, 2021, 3(1): 52‒62 https://doi.org/10.1007/s42832-020-0049-z

References

[1]
Bainard, L.D., Dai, M., Gomez, E.F., Torres-Arias, Y., Bainard, J.D., Sheng, M., Eilers, W., Hamel, C., 2015. Arbuscular mycorrhizal fungal communities are influenced by agricultural land use and not soil type among the Chernozem great groups of the Canadian Prairies. Plant and Soil 387, 351–362
CrossRef Google scholar
[2]
Börstler, B., Renker, C., Kahmen, A., Buscot, F., 2006. Species composition of arbuscular mycorrhizal fungi in two mountain meadows with differing management types and levels of plant biodiversity. Biology and Fertility of Soils 42, 286–298
CrossRef Google scholar
[3]
Bossio, D., Scow, K., 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 35, 265–278
CrossRef Google scholar
[4]
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T.L., 2009. BLAST plus: architecture and applications. BMC Bioinformatics10, 421.
[5]
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, 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., Tumbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336
CrossRef Google scholar
[6]
Chagnon, P., Bradley, R., Klironomos, J., 2014. Plant–fungal symbioses as ecological networks: the need to characterize more than just interaction patterns. Fungal Ecology 12, 10–13
CrossRef Google scholar
[7]
Chaudhary, V.B., Lau, M., Johnson, N., 2008. Macroecology of microbes biogeography of Glomeromycota. In: Varma, A., ed. Mycorrhiza. Berlin: Springer-Verlag, 529–565.
[8]
Cozzolino, V., Di Meo, V., Monda, H., Spaccini, R., Piccolo, A., 2016. The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biology and Fertility of Soils 52, 15–29.
[9]
Dodd, J.C., Boddington, C.L., Rodriguez, A., Gonzalez-Chavez, C., Mansur, I., 2000. Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: form, function and detection. Plant and Soil 226, 131–151
CrossRef Google scholar
[10]
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200
CrossRef Google scholar
[11]
Flores-Renteria, D., Sanchez-Gallen, I., Morales-Rojas, D., Larsen, J., Alvarez-Sanchez, J., 2020. Changes in the abundance and composition of a microbial community associated with land use change in a mexican tropical rain forest. Journal of Soil Science and Plant Nutrition. 1–12.
[12]
Gao, C., Montoya, L., Xu, L., Madera, M., Hollingsworth, J., Purdom, E., Hutmacher, R.B., Dahlberg, J.A., Coleman-Derr, D., Lemaux, P.G., Taylor, J.W., 2019. Strong succession in arbuscular mycorrhizal fungal communities. ISME Journal 13, 214–226
CrossRef Google scholar
[13]
Gosling, P., Mead, A., Proctor, M., Hammond, J.P., Bending, G.D., 2013. Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytologist 198, 546–556
CrossRef Google scholar
[14]
Gosling, P., Proctor, M., Jones, J., Bending, G.D., 2014. Distribution and diversity of Paraglomus spp. in tilled agricultural soils. Mycorrhiza 24, 1–11
CrossRef Google scholar
[15]
Grime, J., Mackey, J., Hillier, S., Read, D., 1987. Floristic diversity in a model system using experimental microcosms. Nature 328, 420–422
CrossRef Google scholar
[16]
Hawkes, C.V., Hartley, I.P., Ineson, P., Fitter, A.H., 2008. Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. Global Change Biology 14, 1181–1190
CrossRef Google scholar
[17]
He, C., Chen, S., Liang, Y., 1982. The soils of Dinghushan biosphere reserve. Tropical and subtropical forest ecosystem 1, 25–38.
[18]
Hiiesalu, I., Pärtel, M., Davison, J., Gerhold, P., Metsis, M., Moora, M., Öpik, M., Vasar, M., Zobel, M., Wilson, S.D., 2014. Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytologist 203, 233–244
CrossRef Google scholar
[19]
Hijri, I., Sýkorová, Z., Oehl, F., Ineichen, K., Mäder, P., Wiemken, A., Redecker, D., 2006. Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Molecular Ecology 15, 2277–2289
CrossRef Google scholar
[20]
Hooper, D., Coughlan, J., Mullen, M., 2008. Structural equation modelling: Guidelines for determining model fit. Electronic Journal of Business Research Methods 6, 53–60.
[21]
Hou, E., Chen, C., Wen, D., Liu, X., 2015. Phosphatase activity in relation to key litter and soil properties in mature subtropical forests in China. Science of the Total Environment 515, 83–91
CrossRef Google scholar
[22]
Houlton, B.Z., Wang, Y.P., Vitousek, P.M., Field, C.B., 2008. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330
CrossRef Google scholar
[23]
Huang, W., Liu, J., Wang, Y.P., Zhou, G., Han, T., Li, Y., 2013. Increasing phosphorus limitation along three successional forests in southern China. Plant and Soil 364, 181–191
CrossRef Google scholar
[24]
Husband, R., Herre, E., Turner, S., Gallery, R., Young, J., 2002. Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Molecular Ecology 11, 2669–2678
CrossRef Google scholar
[25]
Jiang, S., Liu, Y., Luo, J., Qin, M., Johnson, N.C., Opik, M., Vasar, M., Chai, Y., Zhou, X., Mao, L., Du, G., An, L., Feng, H., 2018. Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytologist 220, 1222–1235
CrossRef Google scholar
[26]
Johnson, N.C., 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185, 631–647
CrossRef Google scholar
[27]
Joner, E., 2000. The effect of long-term fertilization with organic or inorganic fertilizers on mycorrhiza-mediated phosphorus uptake in subterranean clover. Biology and Fertility of Soils 32, 435–440
CrossRef Google scholar
[28]
Khade, S.W., Rodrigues, B.F., Sharma, P.K., 2010. Arbuscular mycorrhizal status and root phosphatase activities in vegetative Carica papaya L. varieties. Acta Physiologiae Plantarum 32, 565–574
CrossRef Google scholar
[29]
Kivlin, S.N., Hawkes, C.V., Treseder, K.K., 2011. Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biology & Biochemistry 43, 2294–2303
CrossRef Google scholar
[30]
Koch, A.M., Antunes, P.M., Klironomos, J.N., 2012. Diversity effects on productivity are stronger within than between trophic groups in the arbuscular mycorrhizal symbiosis. PLoS One 7, e36950
CrossRef Google scholar
[31]
Koide, R.T., Kabir, Z., 2000. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytologist 148, 511–517
CrossRef Google scholar
[32]
Li, X., Zhang, J., Gai, J., Cai, X., Christie, P., Li, X., 2015. Contribution of arbuscular mycorrhizal fungi of sedges to soil aggregation along an altitudinal alpine grassland gradient on the Tibetan Plateau. Environmental Microbiology 17, 2841–2857
CrossRef Google scholar
[33]
Liu, G., Jiang, N., Zhang, L., Liu, Z., 1996. Soil physical and chemical analysis and description of soil profiles. Beijing: China Standard Methods Press.
[34]
Lovelock, C.E., Ewel, J.J., 2005. Links between tree species, symbiotic fungal diversity and ecosystem functioning in simplified tropical ecosystems. New Phytologist 167, 219–228
CrossRef Google scholar
[35]
Lu, X., Mao, Q., Gilliam, F.S., Luo, Y., Mo, J., 2014. Nitrogen deposition contributes to soil acidification in tropical ecosystems. Global Change Biology 20, 3790–3801
CrossRef Google scholar
[36]
Lumini, E., Orgiazzi, A., Borriello, R., Bonfante, P., Bianciotto, V., 2010. Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land‐use gradient using a pyrosequencing approach. Environmental Microbiology 12, 2165–2179.
[37]
Mahanta, D., Rai, R., Dhar, S., Varghese, E., Raja, A., Purakayastha, T., 2018. Modification of root properties with phosphate solubilizing bacteria and arbuscular mycorrhiza to reduce rock phosphate application in soybean-wheat cropping system. Ecological Engineering 111, 31–43
CrossRef Google scholar
[38]
Moora, M., 2014. Mycorrhizal traits and plant communities: perspectives for integration. Journal of Vegetation Science 25, 1126–1132
CrossRef Google scholar
[39]
Morton, J.B., Redecker, D., 2001. Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93, 181–195
CrossRef Google scholar
[40]
Negrete-Yankelevich, S., Cultidmedina, C.A., Fuentespangtay, T., Alvarezsanchez, J., Cram, S., Garciaperez, J.A., Fragoso, C., Martinezromero, E., Rojas, P., Varelafregoso, L., Bueno-Villegas, J., Barois, I., 2020. Disentangling the effects of legacies from those of current land use on soil properties in Los Tuxtlas Biosphere Reserve, Mexico. Applied Soil Ecology 153, 103578
CrossRef Google scholar
[41]
Niu, J., 1990. An investigation on mycorrhiza from Dinghu Shan. Tropical and Subtropical Forest Ecosystem Research 6, 37–40.
[42]
Oehl, F., Sieverding, E., Ineichen, K., Mader, P., Boller, T., Wiemken, A., 2003. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Applied and Environmental Microbiology 69, 2816–2824
CrossRef Google scholar
[43]
Opik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J.M., Reier, U., Zobel, M., 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist 188, 223–241
CrossRef Google scholar
[44]
Öpik, M., Zobel, M., Cantero, J.J., Davison, J., Facelli, J.M., Hiiesalu, I., Jairus, T., Kalwij, J.M., Koorem, K., Leal, M.E., Liira, J., Metsis, M., Neshataeva, V., Paal, J., Phosri, C., Põlme, S., Reier, Ü., Saks, Ü., Schimann, H., Thiéry, O., Vasar, M., Moora, M., 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23, 411–430
CrossRef Google scholar
[45]
Peng, S., Wang, B., 1983. Analysis on the forest communities of Dinghushan: I. Species diversity. Ecologic Science 1, 11–17.
[46]
Pivato, B., Offre, P., Marchelli, S., Barbonaglia, B., Mougel, C., Lemanceau, P., Berta, G., 2009. Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza 19, 81–90
CrossRef Google scholar
[47]
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 of London. Series B, Biological Sciences 276, 4237–4245
CrossRef Google scholar
[48]
Qin, H., Chen, J., Wu, Q., Niu, L., Li, Y., Liang, C., Shen, Y., Xu, Q., 2017. Intensive management decreases soil aggregation and changes the abundance and community compositions of arbuscular mycorrhizal fungi in Moso bamboo (Phyllostachys pubescens) forests. Forest Ecology and Management 400, 246–255
CrossRef Google scholar
[49]
Redecker, D., Schüßler, A., Stockinger, H., Stürmer, S.L., Morton, J.B., Walker, C., 2013. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23, 515–531
CrossRef Google scholar
[50]
Rodríguez-Echeverría, S., Teixeira, H., Correia, M., Timóteo, S., Heleno, R., Öpik, M., Moora, M., 2017. Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure. New Phytologist 213, 380–390
CrossRef Google scholar
[51]
Scheublin, T.R., Sanders, I.R., Keel, C., Van Der Meer, J.R., 2010. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME Journal 4, 752–763
CrossRef Google scholar
[52]
Schneider, K., Turrión, M.B., Gallardo, J.F., 2000. Modified method for measuring acid phosphatase activities in forest soils with high organic matter content. Communications in Soil Science and Plant Analysis 31, 3077–3088
CrossRef Google scholar
[53]
Sheldrake, M., Rosenstock, N.P., Mangan, S., Revillini, D., Sayer, E.J., Olsson, P.A., Verbruggen, E., Tanner, E.V.J., Turner, B.L., Wright, S.J., 2018. Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest. ISME Journal 12, 2433–2445
CrossRef Google scholar
[54]
Sheldrake, M., Rosenstock, N.P., Revillini, D., Olsson, P.A., Mangan, S., Sayer, E.J., Wallander, H., Turner, B.L., Tanner, E.V., 2017. Arbuscular mycorrhizal fungal community composition is altered by long‐term litter removal but not litter addition in a lowland tropical forest. New Phytologist 214, 455–467
CrossRef Google scholar
[55]
Shen, C., Yi, W., Sun, Y., Xing, C., Yang, Y., Yuan, C., Li, Z., Peng, S., An, Z., Liu, T., 2001. Distribution of 14C and 13C in forest soils of the Dinghushan Biosphere Reserve. Radiocarbon 43, 671–678
CrossRef Google scholar
[56]
Smith, S.E., Read, D.J., 2008. Mycorrhizal symbiosis. Cambridge: Academic Press.
[57]
Solis-Rodriguez, U.R.J., Ramos-Zapata, J.A., Hernandez-Cuevas, L., Salinas-Peba, L., Guadarrama, P., 2020. Arbuscular mycorrhizal fungi diversity and distribution in tropical low flooding forest in Mexico. Mycological Progress 19, 195–204
CrossRef Google scholar
[58]
Sun, X., Su, Y., Zhang, Y., Wu, M., Zhang, Z., Pei, K., Sun, L., Wan, S., Liang, Y., 2013. Diversity of arbuscular mycorrhizal fungal spore communities and its relations to plants under increased temperature and precipitation in a natural grassland. Chinese Science Bulletin 58, 4109–4119
CrossRef Google scholar
[59]
Tang, X., Wang, Y.P., Zhou, G., Zhang, D., Liu, S., Liu, S., Zhang, Q., Liu, J., Yan, J., 2011. Different patterns of ecosystem carbon accumulation between a young and an old-growth subtropical forest in Southern China. Plant Ecology 212, 1385–1395
CrossRef Google scholar
[60]
Treseder, K.K., 2005. Nutrient Acquisition Strategies of Fungi and Their Relation to Elevated Atmospheric CO2, The Fungal Community: Its Organization and Role in the Ecosystem, pp. 713–731.
[61]
Treseder, K.K., Vitousek, P.M., 2001. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82, 946–954
CrossRef Google scholar
[62]
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, 69–72
CrossRef Google scholar
[63]
Vasar, M., Andreson, R., Davison, J., Jairus, T., Moora, M., Remm, M., Young, J., Zobel, M., Öpik, M., 2017. Increased sequencing depth does not increase captured diversity of arbuscular mycorrhizal fungi. Mycorrhiza 27, 761–773
CrossRef Google scholar
[64]
Veresoglou, S.D., Caruso, T., Rillig, M.C., 2013. Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families. Plant and Soil 368, 507–518
CrossRef Google scholar
[65]
Veresoglou, S.D., Liu, L., Xu, T.L., Rillig, M.C., Wang, M.E., Wang, J.T., Chen, Y.L., Hu, Y.J., Hao, Z.P., Chen, B.D., 2019. Biogeographical constraints in Glomeromycotinan distribution across forest habitats in China. Journal of Ecology 107, 684–695
CrossRef Google scholar
[66]
Vogelsang, K.M., Reynolds, H.L., Bever, J.D., 2006. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytologist 172, 554–562
CrossRef Google scholar
[67]
Vosatka, M., Dodd, J.C., 1998. The role of different arbuscular mycorrhizal fungi in the growth of Calamagrostis villosa and Deschampsia flexuosa, in experiments with simulated acid rain. Plant and Soil 200, 251–263
CrossRef Google scholar
[68]
Wang, K., He, X., Xie, L., Zhao, L., 2018. Arbuscular mycorrhizal fungal community structure and diversity are affected by host plant species and soil depth in the Mu Us Desert, northwest China. Arid Land Research and Management 32, 198–211
CrossRef Google scholar
[69]
Wang, Y., Li, T., Li, Y., Bjoern, L.O., Rosendahl, S., Olsson, P.A., Li, S., Fu, X., 2015. Community dynamics of arbuscular mycorrhizal fungi in high-input and intensively irrigated rice cultivation systems. Applied and Environmental Microbiology 81, 2958–2965
CrossRef Google scholar
[70]
Wang, Y.Y., Vestberg, M., Walker, C., Hurme, T., Zhang, X., Lindström, K., 2008. Diversity and infectivity of arbuscular mycorrhizal fungi in agricultural soils of the Sichuan Province of Chinese mainland. Mycorrhiza 18, 59–68
CrossRef Google scholar
[71]
Wen, D., Wei, P., Kong, G., Zhang, Q., Huang, Z., 1997. Biomass study of the community of Castanopsis chinessis + Cryptocarya concinna +Schima superby in a southern China reserve. Acta Ecologica Sinica 17, 497–504.
[72]
White, T.J., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, PCR protocols: a guide to methods and applications. Academic Press, pp. 315–322.
[73]
Wilson, G.W., Rice, C.W., Rillig, M.C., Springer, A., Hartnett, D.C., 2009. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long‐term field experiments. Ecology Letters 12, 452–461
CrossRef Google scholar
[74]
Wright, S., Upadhyaya, A., 1998. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil 198, 97–107
CrossRef Google scholar
[75]
Wu, H., Deng, H., Zheng, L., Liu, Y., 1982. Physico-geographical features of Dinghushan and their dynamic analyses. Tropical and Subtropical Forest Ecosystem Research 1, 1–10.
[76]
Xiang, D., Verbruggen, E., Hu, Y., Veresoglou, S.D., Rillig, M.C., Zhou, W., Xu, T., Li, H., Hao, Z., Chen, Y., Chen, B., 2014. Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytologist 204, 968–978
CrossRef Google scholar
[77]
Zhang, J., Tang, X., Zhong, S., Yin, G., Gao, Y., He, X., 2017. Recalcitrant carbon components in glomalin-related soil protein facilitate soil organic carbon preservation in tropical forests. Scientific Reports 7, 2391
CrossRef Google scholar
[78]
Zhao, A., Liu, L., Xu, T., Shi, L., Xie, W., Zhang, W., Fu, S., Feng, H., Chen, B., 2018. Influences of canopy nitrogen and water addition on AM fungal biodiversity and community composition in a mixed deciduous forest of China. Frontiers of Plant Science 9, 9
CrossRef Google scholar
[79]
Zheng, K., Tang, X., Zhang, J., Han, T., 2013. Mycorrhizae respond to plant diversity in monsoon evergreen broadleaved forest succession choronsequence. Ecology and Environmental Sciences 22, 729–738.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31770491, 31270499 and 41430529), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0408), the Youth Innovation Promotion Association, CAS and Natural Science Foundation of Guangdong Province of China (2019A1515011486). The authors thank Prof. Hakan Wallander (Lund University, Sweden) for writing advice. Mr. Mingzhi Li (Genepioneer Biotechnologies, Nanjing 210014, China) and Dr. Mingsen Qin (Lanzhou University, China) are thanked for providing bioinformatics analysis.

Conflict of interest

The authors declare that they have no conflict of interest.

Author contributions

J.Z. and X.T. designed the research, J.Z., C.Q and. G.C. collected the samples, J.Z. and Z.L. performed the experiments and analyzed the data and J.Z., C.Q., L.M. and X.T. wrote the manuscript.

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Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-020-0049-z and is accessible for authorized users.

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