Abstract
Plant–microbe interactions affect ecosystem function, and plant species influence relevant microorganisms. However, the different genotypes of maize that shape the structure and function of the rhizosphere microbial community remain poorly investigated. During this study, the structures of the rhizosphere microbial community among three genotypes of maize were analyzed at the seedling and maturity stages using high-throughput sequencing and bioinformatics analysis. The results demonstrated that Tiannuozao 60 (N) showed higher bacterial and fungal diversity in both periods, while Junlong1217 (QZ) and Fujitai519 (ZL) had lower diversity. The bacterial community structure among the three varieties was significantly different; however, fewer differences were found in the fungal community. The bacterial community composition of N and QZ was similar yet different from ZL at the seedling stage. The bacterial networks of the three cultivars were more complex than the fungal networks, and the networks of the mature stages were more complex than those of the seedling stages, while the opposite was true for the fungi. FAPROTAX functional and FUNGuild functional predictions revealed that different varieties of maize were different in functional abundance at the genus level, and these differences were related to breeding characteristics. This study suggested that different maize genotypes regulated the rhizosphere bacterial and fungal communities, which would help guide practices.
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The datasets of the paper is deposited in NCBI under accession number PRJNA775859.
References
Agler MT et al (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14:e1002352. https://doi.org/10.1371/journal.pbio.1002352
Bakker P, Doornbos RF, Zamioudis C, Berendsen RL, Pieterse C (2013) Induced systemic resistance and the rhizosphere microbiome. Plant Pathol J 29:136–143. https://doi.org/10.5423/PPJ.SI.07.2012.0111
Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. Isme j 6:343–351. https://doi.org/10.1038/ismej.2011.119
Barillot CDC, Sarde CO, Bert V, Tarnaud E, Cochet N (2013) A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. Ann Microbiol 63:471–476. https://doi.org/10.1007/s13213-012-0491-y
Berendsen RL et al (2018) Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496–1507. https://doi.org/10.1038/s41396-018-0093-1
Berg M, Koskella B (2018) Nutrient- and dose-dependent microbiome-mediated protection against a plant pathogen. Curr Biol 28:2487. https://doi.org/10.1016/j.cub.2018.05.085
Bouchotroch S, Quesada E, Izquierdo I, Rodríguez M, Béjar V (2000) Bacterial exopolysaccharides produced by newly discovered bacteria belonging to the genus Halomonas, isolated from hypersaline habitats in Morocco. J Ind Microbiol Biotechnol 24:374–378. https://doi.org/10.1038/sj.jim.7000002
Brughmans T (2013) Thinking through networks: a review of formal network methods in archaeology. J Archaeol Method Theory 20:623–662. https://doi.org/10.1007/s10816-012-9133-8
Bulgarelli D et al (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403. https://doi.org/10.1016/j.chom.2015.01.011
Caldera EJ, Chevrette MG, Mcdonald BR, Currie CR (2019) Local adaptation of bacterial symbionts within a geographic mosaic of antibiotic coevolution. Appl Environ Microbiol 85:e01580-e1619. https://doi.org/10.1128/AEM.01580-19
Chandel R (2018) Response of maize (Zea mays L.): crop to different planters. Poljoprivredna Tehnika 2:61–72
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chi Y et al (2019) Structure and molecular morphology of a novel moisturizing exopolysaccharide produced by Phyllobacterium sp. 921F. Int J Biol Macromol 135:998–1005. https://doi.org/10.1016/j.ijbiomac.2019.06.019
Chibucos MC, Tyler BM (2009) Common themes in nutrient acquisition by plant symbiotic microbes, described by the Gene Ontology. BMC Microbiol 9:S6. https://doi.org/10.1186/1471-2180-9-S1-S6
Cline LC, Zak DR (2016) Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96:3374–3385. https://doi.org/10.1890/15-0184.1
Collado S, Oulego P, Suarez-Iglesias O, Diaz M (2019) Leachates and natural organic matter. A review of their biotreatment using fungi. Waste Manage 96:108–120. https://doi.org/10.1016/j.wasman.2019.07.018
Delgado-Baquerizo M et al (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Delmont TO et al (2011) Accessing the soil metagenome for studies of microbial diversity. Appl Environ Microbiol 77:1315–1324. https://doi.org/10.1128/AEM.01526-10
Deng Y et al (2012) Molecular ecological network analyses. BMC Bioinform 13:113. https://doi.org/10.1186/1471-2105-13-113
Deng Y et al (2016) Network succession reveals the importance of competition in response to emulsified vegetable oil amendment for uranium bioremediation. Environ Microbiol 18:205–218. https://doi.org/10.1111/1462-2920.12981
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/NMETH.2604
Etesami H, Hosseini HM, Alikhani HA (2014) Bacterial biosynthesis of 1-aminocyclopropane-1-caboxylate (ACC) deaminase, a useful trait to elongation and endophytic colonization of the roots of rice under constant flooded conditions. Physiol Mol Biol Plants 20:425–434. https://doi.org/10.1007/s12298-014-0251-5
Feng K et al (2017) Biodiversity and species competition regulate the resilience of microbial biofilm community. Mol Ecol 26:6170–6182. https://doi.org/10.1111/mec.14356
Ferrando L, Scavino AF (2015) Strong shift in the diazotrophic endophytic bacterial community inhabiting rice (Oryza sativa) plants after flooding. FEMS Microbiol Ecol 91:fiv104. https://doi.org/10.1093/femsec/fiv104
Gardener B, Weller DM (2001) Changes in populations of rhizosphere bacteria associated with take-all disease of wheat. Appl Environ Microbiol 67:4414–4425. https://doi.org/10.1128/AEM.67.10.4414-4425.2001
Graham EB et al (2014) Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes. Soil Biol Biochem 68:279–282. https://doi.org/10.1016/j.soilbio.2013.08.023
Griffiths BS et al (2000) Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity–ecosystem function relationship. Oikos 90:279–294. https://doi.org/10.1034/j.1600-0706.2000.900208.x
Haney CH, Samuel BS, Bush J, Ausubel FM (2015) Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat Plants 1:15051. https://doi.org/10.1038/NPLANTS.2015.51
Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–190. https://doi.org/10.1038/nature05947
Heng S, Sutheeworapong AS, Prommeenate BP, Cheevadhanarak CS, Kosugi BA (2019) Complete genome sequence of Halocella sp. Strain SP3-1, an extremely halophilic, glycoside hydrolase- and bacteriocin-producing bacterium isolated from a salt evaporation pond. Microbiol Resour Announce 8:e01696-e11618. https://doi.org/10.1128/MRA.01696-18
Hou D et al (2018) Cultivar-specific response of bacterial community to cadmium contamination in the rhizosphere of rice (Oryza sativa L.). Environ Pollut 241:63–73. https://doi.org/10.1016/j.envpol.2018.04.121
Jiang Y et al (2017) Plant cultivars imprint the rhizosphere bacterial community composition and association networks. Soil Biol Biochem 109:145–155. https://doi.org/10.1016/j.soilbio.2017.02.010
Junker BH, Schreiber F (2010) Analysis of biological networks. J Anat 215:473. https://doi.org/10.1111/j.1469-7580.2009.01132.x
Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320. https://doi.org/10.1007/BF02602840
Koeck DE et al (2016) Complete genome sequence of Herbinix luporum SD1D, a new cellulose-degrading bacterium isolated from a Thermophilic Biogas Reactor. Genome Announc 4:e00687-e716. https://doi.org/10.1128/genomeA.00687-16
Kong X et al (2020) Maize (Zea mays L. Sp.) varieties significantly influence bacterial and fungal community in bulk soil, rhizosphere soil, and phyllosphere. FEMS Microbiol Ecol 96:3. https://doi.org/10.1093/femsec/fiaa020
Layeghifard M, Hwang DM, Guttman DS (2017) Disentangling interactions in the microbiome: a network perspective. Trends Microbiol 25:217–228. https://doi.org/10.1016/j.tim.2016.11.008
Liu H, Macdonald CA, Cook J, Anderson IC, Singh BK (2019) An ecological loop: host microbiomes across multitrophic interactions. Trends Ecol Evol 34:1118–1130. https://doi.org/10.1016/j.tree.2019.07.011
Lu T et al (2018) Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome 6:231. https://doi.org/10.1186/s40168-018-0615-0
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Mansotra P, Sharma P, Sharma S (2015) Bioaugmentation of Mesorhizobium cicer, Pseudomonas spp. and Piriformospora indica for sustainable chickpea production. Physiol Mol Biol Plants 21:385–393. https://doi.org/10.1007/s12298-015-0296-0
Mendes R et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. https://doi.org/10.1126/science.1203980
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. https://doi.org/10.1111/1574-6976.12028
Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587. https://doi.org/10.1038/ismej.2014.17
Müller DB, Vogel C, Bai Y, Vorholt Julia A (2016) The plant microbiota: systems-level insights and perspectives. Annu Rev Genet 50:211–234. https://doi.org/10.1146/annurev-genet-120215-034952
Nguyen NW et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Peiffer JA et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553. https://doi.org/10.1073/pnas.1302837110
Pietikainen J, Pettersson M, Baath E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58. https://doi.org/10.1016/j.femsec.2004.10.002
Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. https://doi.org/10.1016/j.pbi.2007.05.004
Raaijmakers JM, Mazzola M (2016) Soil immune responses. Science 352:1392–1393. https://doi.org/10.1126/science.aaf3252
Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403–424. https://doi.org/10.1146/annurev-phyto-082712-102342
Ritpitakphong U et al (2016) The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol 210:1033–1043. https://doi.org/10.1111/nph.13808
Rolli E et al (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. https://doi.org/10.1111/1462-2920.12439
Saleem M, Law AD, Moe LA (2016) Nicotiana roots recruit rare rhizosphere taxa as major root-inhabiting microbes. MicEc 71:469–472. https://doi.org/10.1007/s00248-015-0672-x
Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V (2017) Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. Mbio 8:e00764-e1717. https://doi.org/10.1128/mBio.00764-17
Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci USA 111:585–592. https://doi.org/10.1073/pnas.1321597111
Simonin M et al (2020) Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils. FEMS Microbiol Ecol 96:fiaa067. https://doi.org/10.1093/femsec/fiaa067
Sohn SI et al (2021) Dynamics of bacterial community structure in the rhizosphere and root nodule of soybean: impacts of growth stages and varieties. Int J Mol Sci 22:5577. https://doi.org/10.3390/ijms22115577
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849
Taguchi YH, Oono Y (2005) Relational patterns of gene expression via nonmetric multidimensional scaling analysis. Bioinformatics 21:730–740. https://doi.org/10.1093/bioinformatics/bti067
Teste FP et al (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Sci 355:173. https://doi.org/10.1126/science.aai8291
Timm CM et al (2018) Abiotic stresses shift belowground populus—associated bacteria toward a core stress microbiome. mSystems 3:e00070. https://doi.org/10.1128/mSystems.00070-17
Vivanco L, Rascovan N, Austin AT (2018) Plant, fungal, bacterial, and nitrogen interactions in the litter layer of a native Patagonian forest. PeerJ 6:e4754. https://doi.org/10.7717/peerj.4754
Wagg C, Bender SF, Widmer F, van der Heijden M (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA 111:5266–5270. https://doi.org/10.1073/pnas.1320054111
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang M, Chen S, Chen L, Wang D (2019) Responses of soil microbial communities and their network interactions to saline-alkaline stress in Cd-contaminated soils. Environ Pollut 252:1609–1621. https://doi.org/10.1016/j.envpol.2019.06.082
Wu R, Cheng X, Zhou W, Han H (2019) Microbial regulation of soil carbon properties under nitrogen addition and plant inputs removal. PeerJ 7:e7343. https://doi.org/10.7717/peerj.7343
Xu L et al (2015) Effects of interactions of auxin-producing bacteria and bacterial-feeding nematodes on regulation of peanut growths. PLoS ONE 10:e0124361. https://doi.org/10.1371/journal.pone.0124361
Xun W et al (2021) Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome 9:35. https://doi.org/10.1186/s40168-020-00985-9
Yu K, Pieterse C, Bakker P, Berendsen RL (2019) Beneficial microbes going underground of root immunity. Plant Cell Environ 42:2860–2870. https://doi.org/10.1111/pce.13632
Yuan J et al (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:156. https://doi.org/10.1186/s40168-018-0537-x
Zachow C, Muller H, Tilcher R, Berg G (2014) Differences between the rhizosphere microbiome of Beta vulgaris ssp. maritima—ancestor of all beet crops—and modern sugar beets. Front Microbiol 5:415. https://doi.org/10.3389/fmicb.2014.00415
Zgadzaj R et al (2016) Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. Proc Natl Acad Sci USA 113:E7996–E8005. https://doi.org/10.1073/pnas.1616564113
Zhalnina K et al (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480. https://doi.org/10.1038/s41564-018-0129-3
Zhan P et al (2021) Plant litter decomposition in wetlands is closely associated with phyllospheric fungi as revealed by microbial community dynamics and co-occurrence network. Sci Total Environ 753:142194. https://doi.org/10.1016/j.scitotenv.2020.142194
Zhang Y, Hu A, Zhou J, Zhang W, Li P (2020) Comparison of bacterial communities in soil samples with and without tomato bacterial wilt caused by Ralstonia solanacearum species complex. BMC Microbiol 20:89. https://doi.org/10.1186/s12866-020-01774-y
Zhao QZ, Wang YF, Cui XY, Hao YB, Yu ZS (2018) Research progress of the influence factors of soil microbial diversity in grasslandin (in chinese). Ecological Science 37:204–212
Zhou J et al (2020) Characterization of the core microbiome in tobacco leaves during aging. Microbiologyopen 9:e984. https://doi.org/10.1002/mbo3.984
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The data were analyzed on the free online platform of Majorbio Cloud Platform (www.majorbio.com).
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This research was funded by the Key Research and Development Projects in Heilongjiang, China (GA21B007 and GZ20210014) and the Basic Research Fees of Universities in Heilongjiang Province, China (No. 135409103).
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Conceptualization, YL and ZW; methodology, YL and ZW; software, YL and ZQ; validation, ZQ, WX, YH, WC and ZW; resources, ZW, YH and WC; data curation, YL; writing—original draft preparation, YL; writing—review and editing, YL and ZW; visualization, YL and ZQ; supervision, ZW and WX; project administration, ZW and WX; funding acquisition, ZW. All authors contributed to the article and approved the submitted version. All authors have read and agreed to the published version of the manuscript.
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Li, Y., Qu, Z., Xu, W. et al. Maize (Zea mays L.) genotypes induce the changes of rhizosphere microbial communities. Arch Microbiol 204, 321 (2022). https://doi.org/10.1007/s00203-022-02934-6
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DOI: https://doi.org/10.1007/s00203-022-02934-6