Abstract
We aimed to evaluate the effects of tropical crop systems and phosphorus (P) availability on arbuscular mycorrhizal fungi (AMF) spores’ community composition, and soil chemical properties in a Planosol at Tropical ecosystem from Brazilian Northeast. We collected rhizospheric samples containing soil and root fragments in a 5-year field experiment considering two groups of crop systems, i.e., no-till monocropping and agroforestry system, and testing two factors: the cropping system and the soil P availability. We identified the AMF community composition based on AMF spore’s morphology. We also characterized the soil chemical properties (e.g., soil pH, soil organic carbon, and available P) at samples level. Crop systems and soil P availability influenced the AMF community composition, and soil chemical properties. We found that: i) the abundance of Claroideoglomus claroideum, C. etunicatum, Rhizophagus intraradices, richness, Shannon’s index and Simpson’s index were positively correlated with no-till monocropping systems (Arachis hypogaea, Gossypium hirsutum, and Vigna unguiculata) and with all the studied agroforestry systems at low-P availability; and ii) soil pH, and soil organic carbon were positively correlated with no-till monocropping systems (Arachis hypogaea, Glicine hirsutum, Glicine max, and Sesamum indicum) at high-P availability, and Glicine max, Sesamum indicum, Zea mays, and agroforestry system at low-P availability. Our results highlight the positive effect of high P on AMF spores’ diversity, and the importance to consider both the crop system and soil P availability as key-factors promoting shifts into the AMF community composition and soil chemical properties in Tropical conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alvarado-Herrejón M, Larsen J, Gavito ME, Jaramillo-López PF, Vestberg M, Martínez-Trujillo M, Carreón-Abud Y (2019) Relation between arbuscular mycorrhizal fungi, root-lesion nematodes, and soil characteristics in maize agroecosystems. Appl Soil Ecol 135:1–8. https://doi.org/10.1016/j.apsoil.2018.10.019
Basirat M, Mousavi SM, Abbaszadeh S, Ebrahimi M, Zarebanadkouki M (2019) The rhizosheath: a potential root trait helping plants to tolerate drought stress. Plant Soil 445:565–575. https://doi.org/10.1007/s11104-019-04334-0
Belay Z, Negash M, Kaseva V, Kahiluoto H (2020) Native forests but not agroforestry systems preserve arbuscular mycorrhizal fungal species richness in southern Ethiopia. Mycorrhiza 30:749–759. https://doi.org/10.1007/s00572-020-00984-6
Boutaj H, Meddich A, Chakhchar A, Wahbi S, Alaoui-Talibi Z, Douira A, Filali-Maltouf A, Modafar C (2020) Arbuscular mycorrhizal fungi improve mineral nutrition and tolerance of olive tree to Verticillium wilt. Arch Phytopathol Plant Protect 53:673–689. https://doi.org/10.1080/03235408.2020.1792603
Cavalcanti JFA (2008) Recomendações de adubação para o Estado de Pernambuco. Instituto Agronômico de Pernambuco, Recife
Chave M, Angeon V, Pault R, Collombet R, Tchamitchian M (2019) Codesigning biodiversity-based agrosystems promotes alternatives to mycorrhizal inoculants. Agron Sustain Dev. https://doi.org/10.1007/s13593-019-0594-y
de Stefano A, Jacobson MG (2018) Soil carbon sequestration in agroforestry systems: a meta-analysis. Agrofor Syst 92:285–299. https://doi.org/10.1007/s10457-017-0147-9
Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Maestre FT, Sinhg BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359(6373):320–325. https://doi.org/10.1126/science.aap9516
Deveautour C, Donn S, Bennett AE, Power S, Powell JR (2021) Variability of arbuscular mycorrhizal fungal communities within the root systems of individual plants is high and influenced by host species and root phosphorus. Pedobiologia. https://doi.org/10.1016/j.pedobi.2020.150691
Freschet GT, Kichenin E, Wardle DA (2015) Explaining within-community variation in plant biomass allocation: a balance between organ biomass and morphology above- vs belowground? J Veg Sci 26(3):431–440. https://doi.org/10.1111/jvs.12259
Gao D, Pan X, Zhou X, Wei Z, Li N, Wu F (2020) Phosphorus fertilization and intercropping interactively affect tomato and potato onion growth and rhizosphere arbuscular mycorrhizal fungal community. Arch Agron Soil Sci. https://doi.org/10.1080/03650340.2020.1768530
Gebremikael MT, Steel H, Buchan D, Bert W, Neve S (2016) Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Sci Rep. https://doi.org/10.1038/srep32862
Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46(2):235–244. https://doi.org/10.1016/S0007-1536(63)80079-0
Goto BT, Silva GA, de Assis DMA, Silva DK, Souza RG, Ferreira ACA, Jobim K, Mello CMA, Vieira HEE, Maia LC, Oehl F (2012) Intraornatosporaceae (Gigasporales), a new family with two new genera and two new species. Mycotaxon 119:117–132. https://doi.org/10.5248/119.117
Guo J, Wang G, Wu Y, Shi Y, Feng Y, Cao F (2019) Ginkgo agroforestry practices alter the fungal community structures at different soil depths in eastern China. Environ Sci Pollut Res 26:21253–21263. https://doi.org/10.1007/s11356-019-05293-w
Higo M, Azuma M, Kamiyoshihara Y, Kanda A, Tatewaki Y, Isobe K (2020) Impact of phosphorus fertilization on tomato growth and arbuscular mycorrhizal fungal communities. Microorganisms. https://doi.org/10.3390/microorganisms8020178
Hontoria C, García-Gonzáles I, Quemada M, Roldán A, Alguacil MM (2019) The cover crop determines the AMF community composition in soil and in roots of maize after a ten-year continuous crop rotation. Sci Total Environ 660:913–922. https://doi.org/10.1016/j.scitotenv.2019.01.095
Impastato CJ, Carrington ME (2020) Effects of plant species and soil history on root morphology, arbuscular mycorrhizal colonization of roots, and biomass in four tallgrass prairie species. Plant Ecol 221:117–124. https://doi.org/10.1007/s11258-019-00997-y
Jenkins WR (1964) A rapid centrifugation technique for separating nematodes from soil. Plant Dis Rep 48:692
Kariman K, Scanlan C, Boitt G, Rengel Z (2020) Feremycorrhizal symbiosis confers growth and nutritional benefits to mycorrhizal and non-mycorrhizal crops. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2020.108060
Laurindo LK, de Souza TAF, Silva LJR, Kormann S (2020) Produção primária líquida. In Laurindo LK, Souza T Indicadores da qualidade do solo em sistemas agroflorestais e ecossistemas associados, 1st edn. PPGEAN, Curitibanos, pp. 43–54
Lei H, Liu A, Hou Q, Zhao Q, Guo J, Wang Z (2020) Diversity patterns of soil microbial communities in the Sophora flavescens rhizosphere in response to continuous monocropping. BMC Microbiol. https://doi.org/10.1186/s12866-020-01956-8
Liu S, Xu J, Huang H, Zhu J, Tang J, Chen X (2020) Changes in the mycorrhizal fungal community in host roots over five host generations under low and high phosphorus conditions. Plant Soil 456:27–41. https://doi.org/10.1007/s11104-020-04694-y
Liu W, Zhang Y, Jiang S, Murray PJ, Liao L, Li X, Zhang J (2019) Spatiotemporal differences in the arbuscular mycorrhizal fungi communities in soil and roots in response to long-term organic compost inputs in an intensive agricultural cropping system on the North China plain. J Soils Sediments 19:2520–2533. https://doi.org/10.1007/s11368-019-02244-3
McKenna TP, Crews TE, Kemp L, Sikes BA (2020) Community structure of soil fungi in a novel perennial crop monoculture, annual agriculture, and native prairie reconstruction. PLoSONE 15:e0228202. https://doi.org/10.1371/journal.pone.0228202
Medeiros AS, Goto BT, Ganade G (2021) Ecological restoration methods influence the structure of arbuscular mycorrhizal fungal communities in degraded drylands. Pedobiologia. https://doi.org/10.1016/j.pedobi.2020.150690
Melo PL, Cherubin MR, Gomes TC, Lisboa IP, Satiro LS, Cerri CEP, Siqueira-Neto M (2020) Straw removal effects on sugarcane root system and stalk yield. Agronomy. https://doi.org/10.3390/agronomy10071048
Na X, Ma C, Ma S, Ma X, Zhu X, Xu P, Zhu H, Cao X, Liang W (2019) Monocropping decouples plant-bacteria interaction and strengthens phytopathogenic fungi colonization in the rhizosphere of a perennial plant species. Plant Soil. https://doi.org/10.1007/s11104-019-04311-7
Oehl F, Sieverding E, Palenzuela J, Ineichen K, da Silva GA (2011) Advances in Glomeromycota taxonomy and classification. IMA Fungus 2:191–199. https://doi.org/10.5598/imafungus.2011.02.02.10
Okalebo JR, Gathua KW, Woomer PL (1993) Laboratory methods of plant and soil analysis: a working manual. Technical bulletin n. 1. Nairobi: tropical soil biology and fertility Programme/soil science society East Africa/UNESCO/ROSTA. https://www.worldcat.org/title/laboratory-methods-of-soil-and-plant-analysis-a-working-manual/oclc/51374874
Olsen S, Cole C, Watanabe F, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA circular Nr 939, US Gov. print. Office, Washington
Passos JH, Maia LC, Assis DMA, Silva JA, Oehl F, Silva IR (2020) Arbuscular mycorrhizal fungal community structure in the rhizosphere of three plant species of crystalline and sedimentary areas in the Brazilian dry Forest. Microb Ecol. https://doi.org/10.1007/s00248-020-01557-y
Pires GC, Lima ME, Zanchi CS, Freitas CM, Souza JMA, Camargo TA, Pacheco LP, Wruck FJ, Carneiro MAC, Kemmelmeier K, Moraes A, Souza ED (2020) Arbuscular mycorrhizal fungi in the rhizosphere of soybean in integrated crop livestock systems with intercropping in the pasture phase. Rhizosphere 17:100270. https://doi.org/10.1016/j.rhisph.2020.100270
R Core Team (2018) R version 3.5.0. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ramos AC, Façanha AR, Feijó JA (2008) Proton (H+) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi. New Phytol 178(1):177–188. https://doi.org/10.1111/j.1469-8137.2007.02344.x
Sarto MVM, Borges WLB, Sarto JRW, Pires CAB, Rice CW, Rosolem CA (2020) Soil microbial community and activity in a tropical integrated crop-livestock system. Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2019.08.012
Schmitz D, Schaefer CERG, Putzke J, Francelino MR, Ferrari FR, Corrêa GR, Villa PM (2020) How does the pedoenvironmental gradient shape non-vascular species assemblages and community structures in Maritime Antarctica? Ecol Indic 108:105726. https://doi.org/10.1016/j.ecolind.2019.105726.
Sieverding E, da Silva GA, Berndt R, Oehl F (2011) Rhizoglomus, a new genus of the Glomeraceae. Mycotaxon 129(2):373–386. https://doi.org/10.5248/129.373
Šmilauer P, Košnar J, Kotilínek M, Šmilauerová M (2019) Contrasting effects of host identity, plant community, and local species pool on the composition and colonisation levels of arbuscular mycorrhizal fungal community in a temperate grassland. New Phytol 225(1):461–473. https://doi.org/10.1111/nph.16112
Soonvald L, Loit K, Runno-Paurson E, Astover A, Tedersoo L (2020) Characterizing the effect of crop species and fertilization treatment on root fungal communities. Scientific Report 10(18741). https://doi.org/10.1038/s41598-020-74952-7
Souza T (2015) Handbook of arbuscular mycorrhizal fungi. Springer
Souza TAF, Freitas H (2017) Arbuscular mycorrhizal fungal community assembly in the Brazilian tropical seasonal dry forest. Ecol Process 6(2):2–10. https://doi.org/10.1186/s13717-017-0072-x
Souza TAF, Rodrígues AF, Marques LF (2015)Long-term effects of alternative and conventional fertilization I: effects on arbuscular mycorrhizal fungi community composition. Russ Agricult Sci 41(6):454–461. https://doi.org/10.3103/S1068367415060245
Souza TAF, Santos D (2018) Effects of using different host plants and long-term fertilization systems on population sizes of infective arbuscular mycorrhizal fungi. Symbiosis 76:139–149. https://doi.org/10.1007/s13199-018-0546-3
Tadersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367(6480). https://doi.org/10.1126/science.aba1223
Tsiknia M, Tsikou D, Papadopoulou KK, Ehaliotis C (2020)Multi-species relationships in legume roots: from pairwise legume-symbiont interactions to the plant – microbiome - soil continuum. FEMS Microbiol Ecol 97(2). https://doi.org/10.1093/femsec/fiaa222
Van’t Padje A, Werner GD, Kiers ET (2020) Mycorrhizal fungi control value of phosphorus in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability. New Phytol 229(5):2933–2944. https://doi.org/10.1111/nph.17055
Vergara C, Araujo KEC, Souza SR, Schultz N, Saggin Júnior OJ, Sperandio MVL, Zilli JÉ (2019)Plant-mycorrhizal fungi interaction and response to inoculation with different growth-promoting fungi. Pesq Agrop Brasileira 58(0). https://doi.org/10.1590/s1678-3921.pab2019.v54.25140
Wang C, Zheng MM, Song WS, Chen RF, Zhao XQ, Wen SL, Zheng ZS, Shen RF (2021) Biogeographic patterns and co-occurrence networks of diazotrophic and arbuscular mycorrhizal fungal communities in the acidic soil ecosystem of southern China. Applied Soil Ecology:158. https://doi.org/10.1016/j.apsoil.2020.103798
Wang J, Ren C, Cheng H, Zou Y, Bughio MA, Li Q (2017) Conversion of rainforest into agroforestry and monoculture plantation in China: consequences for soil phosphorus forms and microbial community. Sci Total Environ 595(1):769–778. https://doi.org/10.1016/j.scitotenv.2017.04.012
Wei L, Vosátka M, Cai B, Ding J, Lu C, Xu J, Yan W, Li Y, Liu C (2019) The role of arbuscular mycorrhiza Fungi in the decomposition of fresh residue and soil organic carbon: a Mini-review. Soil Science Society pf America Journal 83(3):511–517. https://doi.org/10.2136/sssaj2018.05.0205
WRB (2006) World soil resources report, FAO, Rome
Yang Q, Biere A, Harvey JA, Ding J, Siemann (2020) Antagonistic interactions between above- and belowground biota reduce their negative effects on a tree species. Plant Soil 454:379–393. https://doi.org/10.1007/s11104-020-04642-w
Zhang J, Quan C, Ma L, Chu G, Liu Z, Tang X (2020) Plant community and soil properties drive arbuscular mycorrhizal fungal diversity: a case study in tropical forests. Soil Ecology Letters 3:52–62. https://doi.org/10.1007/s42832-020-0049-z
Acknowledgments
The authors wish to thank Valdemir Ribeiro Cavalcante (EMEPA), Andre Julio do Amaral (EMBRAPA), and João Henrique Zonta (EMBRAPA) for their assistance.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
We declare that all the authors made substantial contributions to the conception, design, acquisition, analysis, and interpretation of the data. All the authors participate in drafting the article, revising it critically for important intellectual content; and finally, the authors gave final approval of the version to be submitted to Biologia.
Corresponding author
Ethics declarations
Ethics approval
We confirm that this manuscript that not been published elsewhere and is not under consideration by another journal. All Authors have approved the manuscript and agree with submission to Biologia. We have read and have abided by the statement of ethical standards for manuscripts submitted to Biologia.
Competing interests
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
da Silva, S.I.A., de Souza, T.A.F., de Lucena, E.O. et al. High phosphorus availability promotes the diversity of arbuscular mycorrhizal spores’ community in different tropical crop systems. Biologia 76, 3211–3220 (2021). https://doi.org/10.1007/s11756-021-00874-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00874-y