Abstract
Few studies have investigated the effect of environment on the root-associated microbiome, especially for woody plants in their native environment. The roots and rhizosphere soils of a native woody species (Broussonetia papyrifera) sampled across four different climate types in China were used to elucidate the influence of environment on the root-associated microbiome. Our results showed that the B. papyrifera root-associated microbiome contained abundant Proteobacteria and Basidiomycota, especially Pseudomonas and Rhizobium. The root-associated microbiomes were found to be significantly different under different climate types except for the bacterial community in the rhizosphere, and the proportion of bacterial operational taxonomic units (OTUs) shared among different climate types was lower than that of fungi. More than 50% of the total variance between microbiomes could be explained by 15 environmental factors, six of which, especially soil concentration phosphate and nitrate, had a significant effect. This study provided a comprehensive understanding of the root-associated microbiome of B. papyrifera and further confirmed the effect of environment on the root-associated microbiome of B. papyrifera under different climate types, with some exceptions in the rhizobacterial community and fungal OTUs. Our findings advanced knowledge of the effect of environment through an exploration of environmental factors and found that the nitrogen and phosphorus content represented the key factors.
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Asemaninejad A, Thorn RG, Lindo Z (2017) Experimental climate change modifies degradative succession in boreal peatland fungal communities. Microb Ecol 73(3):521–531. https://doi.org/10.1007/s00248-016-0875-9
Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, Bengtsson-Palme J, Anslan S, Coelho LP, Harend H, Huerta-Cepas J, Medema MH, Maltz MR, Mundra S, Olsson PA, Pent M, Polme S, Sunagawa S, Ryberg M, Tedersoo L, Bork P (2018) Structure and function of the global topsoil microbiome. Nature 560(7717):233–237. https://doi.org/10.1038/s41586-018-0386-6
Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Münch PC, Spaepen S, Remus-Emsermann M, Hüttel B, McHardy AC, Vorholt JA, Schulze-Lefert P (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–369. https://doi.org/10.1038/nature16192
Beckers B, De Beeck MO, Weyens N, Acker RV, Van Montagu M, Boerjan W, Vangronsveld J (2015) Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome. Proc Natl Acad Sci U S A 113(8):2312–2317. https://doi.org/10.1073/pnas.1523264113
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bouffaud ML, Kyselková M, Gouesnard B, Grundmann G, Muller D, Moënne-Loccoz Y (2012) Is diversification history of maize influencing selection of soil bacteria by roots? Mol Ecol 21:195–206. https://doi.org/10.1111/j.1365-294X.2011.05359.x
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Chang CS, Liu HL, Moncada X, Seelenfreund A, Seelenfreund D, Chung KF (2015) A holistic picture of Austronesian migrations revealed by phylogeography of Pacific paper mulberry. Proc Natl Acad Sci U S A 112(44):13537–13542. https://doi.org/10.1073/pnas.1503205112
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209(2):798–811. https://doi.org/10.1111/nph.13697
Dastmalchi M, Chapman P, Yu J, Austin RS, Dhaubhadel S (2017) Transcriptomic evidence for the control of soybean root isoflavonoid content by regulation of overlapping phenylpropanoid pathways. BMC Genomics 18(1):70–86. https://doi.org/10.1186/s12864-016-3463-y
De Zelicourt A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 6(2):242–245. https://doi.org/10.1093/mp/sst028
Desgarennes D, Garrido E, Torres-Gomez MJ, Pena-Cabriales JJ, Partida-Martinez LP (2014) Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species. FEMS Microbiol Ecol 90(3):844–857. https://doi.org/10.1111/1574-6941.12438
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112(8):911–920. https://doi.org/10.1073/pnas.1414592112
Errasti AD, Carmarán CC, Novas MV (2010) Diversity and significance of fungal endophytes from living stems of naturalized trees from Argentina. Fungal Divers 41(1):29–40. https://doi.org/10.1007/s13225-009-0012-x
Fahimipour AK, Kardish MR, Lang JM, Green JL, Eisen JA, Stachowicz JJ (2017) Global-scale structure of the eelgrass microbiome. Appl Environ Microbiol 83(12):1–12. https://doi.org/10.1128/AEM.03391-16
Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42(1):23–46. https://doi.org/10.1146/annurev-ecolsys-102710-145039
Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Adv Microb Physiol 41:47–92
Geel MV, Jacquemyn H, Plue J, Saar L, Kasari L, Peeters G, van Acker K, Honnay O, Ceulemans T (2017) Abiotic rather than biotic filtering shapes the arbuscular mycorrhizal fungal communities of European seminatural grasslands. New Phytol 220:1262–1272. https://doi.org/10.1111/nph.14947
Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26(24):6960–6973. https://doi.org/10.1111/mec.14414
Hazard C, Gosling P, Mitchell DT, Doohan FM, Bending GD (2014) Diversity of fungi associated with hair roots of ericaceous plants is affected by land use. FEMS Microbiol Ecol 87(3):586–600. https://doi.org/10.1111/1574-6941.12247
Innerebner G, Knief C, Vorholt JA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl Environ Microbiol 77(10):3202–3210. https://doi.org/10.1128/AEM.00133-11
Julien M, Lindow SE (2000) Role of leaf surface sugars in colonization of plants by bacterial epiphytes. Appl Environ Microbiol 66(1):369–374. https://doi.org/10.1128/AEM.66.1.369-374.2000
Ko HJ, Oh SK, Jin JH, Son KH, Kim HP (2013) Inhibition of experimental systemic inflammation (septic inflammation) and chronic bronchitis by new phytoformula BL containing Broussonetia papyrifera and Lonicera japonica. Biomol Ther (Seoul) 21(1):66–71. https://doi.org/10.4062/biomolther.2012.081
Laforest-Lapointe I, Messier C, Kembel SW (2016) Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4(1):27. https://doi.org/10.1186/s40168-016-0174-1
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(15):5111–5120. https://doi.org/10.1128/AEM.00335-09
Li L, Tilman D, Lambers H, Zhang F-S (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203(1):63–69. https://doi.org/10.1111/nph.12778
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Malapi-Wight M, Salgado-Salazar C, Demers J, Veltri D, Croucha JA (2015) Draft genome sequence of Dactylonectria macrodidyma, a plant-pathogenic fungus in the Nectriaceae. Genome Announc 3(2). https://doi.org/10.1128/genomeA.00278-15
Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14(1):36–41. https://doi.org/10.1111/j.1461-0248.2010.01547.x
Morris MH, Smith ME, Rizzo DM, Rejmanek M, Bledsoe CS (2008) Contrasting ectomycorrhizal fungal communities on the roots of co-occurring oaks (Quercus spp.) in a California woodland. New Phytol 178(1):167–176. https://doi.org/10.1111/j.1469-8137.2007.02348.x
Naylor D, DeGraaf S, Purdom E, Coleman-Derr D (2017) Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J 11(12):2691–2704. https://doi.org/10.1038/ismej.2017.118
Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract pseudomonas putida to the rhizosphere. PLoS One 7(4):e35498. https://doi.org/10.1111/j.1574-6968.1988.tb02676.x-i1
Niu B, Paulson JN, Zheng XQ, Kolter R (2017) Simplified and representative bacterial community of maize roots. Proc Natl Acad Sci U S A 114(12):E2450–E2459. https://doi.org/10.1073/pnas.1616148114
Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252–263. https://doi.org/10.1038/nrmicro2990
Peay KG, von Sperber C, Cardarelli E, Toju H, Francis CA, Chadwick OA, Vitousek PM (2017) Convergence and contrast in the community structure of Bacteria, Fungi and Archaea along a tropical elevation-climate gradient. FEMS Microbiol Ecol 93(5). https://doi.org/10.1093/femsec/fix045
Peiffera JA, Sporb A, Korenb O, Jinb Z, Tringed SG, Dangle JL, Bucklera ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110(16):6548–6553. https://doi.org/10.1073/pnas.1302837110
Peng XJ, Shen S (2018) The paper mulberry: a novel model system for woody plant research. Chin Bull Bot 53(3):372–381
Peng XJ, Teng LH, Wang XM, Wang YC, Shen SH (2014) De novo assembly of expressed transcripts and global transcriptomic analysis from seedlings of the paper mulberry (Broussonetia kazinoki x Broussonetia papyifera). PLoS One 9(5):e97487. https://doi.org/10.1371/journal.pone.0097487
Peng XJ, Liu H, Chen PL, Tang F, Hu YM, Wang FF, Pi Z, Zhao ML, Chen NZ, Chen H, Zhang XK, Yan XQ, Liu M, Fu XJ, Zhao GF, Yao P, Wang LL, Dai H, Li XM, Xiong W, Xu WC, Zheng HK, Yu HY, Shen SH (2019) A chromosome-scale genome assembly of paper mulberry (Broussonetia papyrifera) provides new insights into its forage and papermaking usage. Mol Plant. https://doi.org/10.1016/j.molp.2019.01.021
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11(11):789–799. https://doi.org/10.1038/nrmicro3109
Pi Z, Zhao ML, Peng XJ, Shen SH (2017) Phosphoproteomic analysis of paper mulberry reveals phosphorylation functions in chilling tolerance. J Proteome Res 16(5):1944–1961. https://doi.org/10.1021/acs.jproteome.6b01016
Robinson RJ, Fraaije BA, Clark IM, Jackson RW, Hirsch PR, Mauchline TH (2016) Wheat seed embryo excision enables the creation of axenic seedlings and Koch’s postulates testing of putative bacterial endophytes. Sci Rep 6:25581. https://doi.org/10.1038/srep25581
Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci U S A 112(36):E5013–E5020. https://doi.org/10.1073/pnas.1505765112
Santos-Medellin 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(4):e00764–e00717. https://doi.org/10.1128/mBio.00764-17
Sawers RJ, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13(2):93–97. https://doi.org/10.1016/j.tplants.2007.11.006
Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbé J, Muchero W, Bonito G, Vilgalys R, Tuskan G, Podar M, Schadt CW (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8(10):e76382. https://doi.org/10.1371/journal.pone.0076382
Shen SH, Peng XJ (2017) The black tech in “paper mulberry poverty alleviation” fills the lack of crude protein feed material of Chinese animal husbandry. Sci Technol Dev 13(6):435–442. https://doi.org/10.11842/chips.2017.06.005
Silva UC, Medeiros JD, Leite LR, Morais DK, Cuadros-Orellana S, Oliveira CA, de Paula Lana UG, Gomes EA, Dos Santos VL (2017) Long-term rock phosphate fertilization impacts the microbial communities of maize rhizosphere. Front Microbiol 8:1266. https://doi.org/10.3389/fmicb.2017.01266
Souza R, Ambrosini A, Passaglia LM (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38(4):401–419. https://doi.org/10.1590/S1415-475738420150053
Stefanova P, Taseva M, Georgieva T, Gotcheva V, Angelov A (2014) A modified CTAB method for DNA extraction from soybean and meat products. Biotechnol Biotechnol Equip 27(3):3803–3810. https://doi.org/10.5504/bbeq.2013.0026
Swamy CT, Gayathri D, Devaraja TN, Bandekar M, D'Souza SE, Meena RM, Ramaiah N (2016) Plant growth promoting potential and phylogenetic characteristics of a lichenized nitrogen fixing bacterium, Enterobacter cloacae. J Basic Microbiol 56(12):1369–1379. https://doi.org/10.1002/jobm.201600197
Takahashi S, Katanuma H, Abe K, Kera Y (2017) Identification of alkaline phosphatase genes for utilizing a flame retardant, Tris(2-chloroethyl) phosphate, in Sphingobium sp. strain TCM1. Appl Microbiol Biotechnol 101(5):2153–2162. https://doi.org/10.1007/s00253-016-7991-9
Van Elsas JDV, Trevors JT, Starodub ME (1988) Bacterial conjugation between pseudomonads in the rhizosphere of wheat. FEMS Microbiol Lett 4(5):299–306. https://doi.org/10.1111/j.1574-6968.1988.tb02676.x-i1
Wagner MR, Lundberg DS, Del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151. https://doi.org/10.1038/ncomms12151
Wang Y, Sheng HF, He Y, Wu JY, Jiang YX, Tam NF, Zhou HW (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl Environ Microbiol 78(23):8264–8271. https://doi.org/10.1128/AEM.01821-12
Wang JS, Liu JS, Peng XJ, Ni ZY, Wang GJ, Shen SH (2014) Applied hybrid paper mulberry in ecological virescence of the coastal saline. Tianjin Agric Sci 20:95–101
Wani ZA, Kumar A, Sultan P, Bindu K, Riyaz-Ul-Hassan S, Ashraf N (2017) Mortierella alpina CS10E4, an oleaginous fungal endophyte of Crocus sativus L. enhances apocarotenoid biosynthesis and stress tolerance in the host plant. Sci Rep 7(1):8598. https://doi.org/10.1038/s41598-017-08974-z
Xiao X, Chen W, Zong L, Yang J, Jiao S, Lin Y, Wang E, Wei G (2017) Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments. Mol Ecol 26(6):1641–1651. https://doi.org/10.1111/mec.14027
Yan J, Wang PS, Du HZ, Zhang QE (2011) First report of black spot caused by Colletotrichum gloeosporioides on paper mulberry in China. Plant Dis 95(7):880–880. https://doi.org/10.1094/PDIS-03-11-0186
Yeoh YK, Paungfoo-Lonhienne C, Dennis PG, Robinson N, Ragan MA, Schmidt S, Hugenholtz P (2016) The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application. Environ Microbiol 18(5):1338–1351. https://doi.org/10.1111/1462-2920.12925
Yoneyama K, Mori N, Sato T, Yoda A, Xie XN, Okamoto M, Iwanaga M, Ohnishi T, Nishiwaki H, Asami T, Yokota T, Akiyama K, Yoneyama K, Nomura T (2018) Conversion of carlactone to carlactonoic acid is a conserved function of MAX1 homologs in strigolactone biosynthesis. New Phytol 218(4):1522–1533. https://doi.org/10.1111/nph.15055
You YH, Park JM, Seo YG, Lee W, Kang MS, Kim JG (2017) Distribution, characterization, and diversity of the endophytic fungal communities on Korean seacoasts showing contrasting geographic conditions. Mycobiology 45(3):150–159. https://doi.org/10.5941/MYCO.2017.45.3.150
Yu P, Wang C, Baldauf JA, Tai H, Gutjahr C, Hochholdinger F, Li C (2017) Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field-grown maize roots. New Phytol 217(3):1240–1253. https://doi.org/10.1111/nph.14893
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S, van der Lelie D, Gilbert JA (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6(2):e02527–e02514. https://doi.org/10.1128/mBio.02527-14
Zhai XQ, Zeng H, Liu YP, Liu F (2012) Change of nutrients and shape of Broussonetia papyrifera leaves from different clones. J Northeast Forest Univ 40(11):38–52
Zhang Y, Ni J, Tang F, Pei K, Luo Y, Jiang L, Sun L, Liang Y (2016) Root-associated fungi of Vaccinium carlesii in subtropical forests of China: intra- and inter-annual variability and impacts of human disturbances. Sci Rep 6:22399. https://doi.org/10.1038/srep22399
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This work was supported by the National Natural Science Foundation of China (31770360, 31870247), the Poverty Relief Project of the Chinese Academy of Sciences (KFJ-FP-24), and the Huimin Technology Demonstration Project of the National Modern Agricultural Science and Technology Achievements City (Z151100001015008).
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Chen, P., Zhao, M., Tang, F. et al. The effect of environment on the microbiome associated with the roots of a native woody plant under different climate types in China. Appl Microbiol Biotechnol 103, 3899–3913 (2019). https://doi.org/10.1007/s00253-019-09747-6
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DOI: https://doi.org/10.1007/s00253-019-09747-6