Abstract
Cinnamomum migao H. W. Li is an evergreen tree belonging to the Lauraceae family and is endemic to China. Previous studies have found that the rhizosphere microbiome associated with the C. migao wild population plays an essential role in the production of fruit chemical components. However, it remains unknown whether the rhizosphere microbiome affects the production of fruit chemical compounds in cultivated C. migao population. Herein, we studied a 10-year-old fruit-bearing population of C. migao and used techniques such as culturing, amplicon sequencing, and metagenomic sequencing to explore the changes in the rhizosphere microbial community structure over three periods. Meanwhile, the molecular ecological network of the rhizosphere microbiome was constructed based on random matrix theory. The unidentified species were found to belong to fungi and Capnodiales. Sphingomonas sp. mm-1 and Streptomyces scabiei in network hubs were recognized in over three fruiting periods. Further, four network hubs were significantly related to fruit chemical compounds production in C. migao. The higher the number of species annotated, the better the explanation for fruit chemical compounds production in C. migao. The rhizosphere microbiome was found to exert a synergistic effect by increasing fruit chemical component production in C. migao. This was evinced through KEGG analysis, which revealed the different metabolic activities affected by the rhizosphere microbiome. This study revealed the potential ways and putative keystone taxa of rhizosphere microbiome affecting fruit component production in C. migao, which opens up new opportunities for further manipulation and development of the rhizosphere microbiome to promote plant productivity.
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The data presented in this study are included in the article/Supplementary Materials; further inquiries may be directed to the corresponding authors.
Abbreviations
- MENs:
-
Molecular ecological networks
- RMT:
-
Random matrix theory
References
Abdelaziz ME, Abdelsattar M, Abdeldaym EA, Atia MAM, Mahmoud AWM, Saad MM, Hirt H (2019) Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Sci Hortic 256:108532–108532. https://doi.org/10.1016/j.scienta.2019.05.059
Acua JJ, Marileo LG, Araya MA, Rilling JI, Jorquera MA (2020) In situ cultivation approach to increase the culturable bacterial diversity in the rhizobiome of plants. J Soil Sci Plant Nutr 20:1411–1426. https://doi.org/10.1007/s42729-020-00222-0
Asaf S, Numan M, Khan AL, Al-Harrasi A (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40(2):138–152. https://doi.org/10.1080/07388551.2019.1709793
Breitwieser FP, Lu J, Salzberg SL (2017) A review of methods and databases for metagenomic classification and assembly. Brief Bioinform 20(4):1125–1136. https://doi.org/10.1093/bib/bbx120
Busby PE, Chinmay S, Wagner MR, Friesen ML, James K, Alison B, Mustafa M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15:e2001793. https://doi.org/10.1371/journal.pbio.2001793
Cadot S, Guan H, Bigalke M, Walser JC, Jander GEM, Heijden MVD, Schlaeppi K (2020) Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field. Microbiome 9(1):103. https://doi.org/10.1186/s40168-021-01049-2
Ceja-Navarro JA, Wang Y, Ning D, Arellano A, Firestone MK (2021) Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop. Microbiome 9(1):96. https://doi.org/10.1186/s40168-021-01042-9
Chater KF (2016) Recent advances in understanding Streptomyces. F1000Res 30(5):2795. https://doi.org/10.12688/f1000research.9534.1
Chen S, Zhou Y, Chen Y, Jia G (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chen J, Huang X, Liu J, Sun Q (2021a) Dominant microbial community in rhizosphere affecting active components of Cinnamomum migao at different ripening stages and their response to soil properties. J Plant Nutr Fertil 27(10):1779–1791. https://doi.org/10.11674/zwyf.2021095
Chen J, Huang X, Tong B, Wang D, Liu J, Liao X, Sun Q (2021b) Effects of rhizosphere fungi on the chemical composition of fruits of the medicinal plant Cinnamomum migao endemic to southwestern China. BMC Microbiol 21:206. https://doi.org/10.1186/S12866-021-02216-Z
Compant S, Samad A, Faist H, Sessitsch A (2019) A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J Adv Res 19:29–37. https://doi.org/10.1016/j.jare.2019.03.004
de Vries FT, Griffiths IR, Knight GC, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368(6488):270–274. https://doi.org/10.1126/science.aaz5192
Dong C, Shao Q, Zhang Q, Yao T, Han Y (2021) Preferences for core microbiome composition and function by different definition methods: evidence for the core microbiome of Eucommia ulmoides bark. Sci Total Environ 790:148091
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/NMETH.2604
Enebe MC, Babalola OO (2020) Effects of inorganic and organic treatments on the microbial community of maize rhizosphere by a shotgun metagenomics approach. Ann Microbiol 70(1):70–78. https://doi.org/10.1186/s13213-020-01591-8
Feng L, Zhong J, Yang Y, Scheuermann RH, Zhou J (2006) Application of random matrix theory to biological networks. Phys Lett A 357:420–423. https://doi.org/10.1016/j.physleta.2006.04.085
Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590. https://doi.org/10.1038/nrmicro.2017.87
Finkel OM, Salas-González I, Castrillo G, Conway JM, Dangl JL (2020) A single bacterial genus maintains root growth in a complex microbiome. Nature 587:103–108. https://doi.org/10.1038/s41586-020-2778-7
Franzosa AE, McIver JL, Rahnavard G, Thompson RL, Schirmer M, Weingart G, Lipson SK, Knight R, Caporaso GJ, Segata N, Huttenhower C (2018) Species-level functional profiling of metagenomes and metatranscriptomes. Nat Methods 15:962–968. https://doi.org/10.1038/s41592-018-0176-y
Gibbons SM (2020) Keystone taxa indispensable for microbiome recovery. Nat Microbiol 5:1067–1068. https://doi.org/10.1038/s41564-020-0783-0
Gu Y, Dong K, Geisen S, Yang W, Friman VP (2020) The effect of microbial inoculant origin on the rhizosphere bacterial community composition and plant growth-promotion. Plant Soil 452:105–117. https://doi.org/10.1007/s11104-020-04545-w
Ishaq M, Wei L, Muhammad RS, Li G, Syed HUS, Yang Z, Xiao G, Yan S, Ma X, Jin H (2021) Guaiane-type sesquiterpenoids from Cinnamomum migao H. W. Li: and their anti-inflammatory activities. Phytochemistry 190:112850. https://doi.org/10.1016/j.phytochem.2021.112850
Javier R, Domingo Á, Víctor F, Concepción AA, Pozo MJ (2018) Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol 220(4):1322–1336. https://doi.org/10.1111/nph.15295
Korenblum E, Dong Y, Szymanski J, Panda S, Aharoni A (2020) Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling. PNAS 117(7):3874–3883. https://doi.org/10.1073/pnas.1912130117
Kumar A, Dubey A (2020) Rhizosphere microbiome: engineering bacterial competitiveness for enhancing crop production. J Adv Res 24:337–352. https://doi.org/10.1016/j.jare.2020.04.014
Lewis WH, Tahon G, Geesink P, Sousa DZ, Ettema T (2021) Innovations to culturing the uncultured microbial majority. Nat Rev Microbiol 19:225–240. https://doi.org/10.1038/s41579-020-00458-8
Li X, Li J, Henk VDW (2008) Flora of China, vol 7. Science Press, Beijing, p 1760. http://www.iplant.cn/info/Cinnamomum%20migao?t=foc
Li Z, Wu Y, Yang K, Chen Y, Huang S, Song L, Hu C, Ban Q, Wang Y, Du S, Huang D (2014) Analysis of essential oil from stem of Cinnamomum migao H. W. Li and its application in cigarette flavoring. Flav Frag Cos (05):25–28+32
Li F, Zhang S, Wang Y, Li Y, Han Y (2020) Rare fungus, Mortierella capitata, promotes crop growth by stimulating primary metabolisms related genes and reshaping rhizosphere bacterial community. Soil Biol Biochem 151:108017. https://doi.org/10.1016/j.soilbio.2020.108017
Li Y, Wang Z, Li T, Zhao D, Liao Y (2021) Wheat rhizosphere fungal community is affected by tillage and plant growth. Agric Ecosyst Environ 317:107475. https://doi.org/10.1016/j.agee.2021.107475
Liang G, Wei H (1989) Study on the volatile oil and fatty oil of Cinnamomum migao fruit. J Guiyang Univ Tradl Chin Med 55–60
Liu G, Liu Y, Kang X (2017) Content determination of total flavonoids and sugar components in Cinnamomum migao. J Anhui Agric Sci 45(03):141–144. https://doi.org/10.13989/j.cnki.0517-6611.201
Liu L, Huang X, Zhang J, Cai Z, Jiang K, Chang Y (2020) Deciphering the relative importance of soil and plant traits on the development of rhizosphere microbial communities. Soil Biol Biochem 148:107909. https://doi.org/10.1016/j.soilbio.2020.107909
Lu T, Ke M, Lavoie M, Jin Y, Fan X, Zhang Z, Fu Z, Sun L, Gillings M, Peñuelas J (2018) Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome 6:231. https://doi.org/10.1186/s40168-018-0615-0
Luo J, Guo X, Tao Q, Li J, Li T (2020) Succession of the composition and co-occurrence networks of rhizosphere microbiota is linked to Cd/Zn hyperaccumulation. Soil Biol Biochem 153:108120. https://doi.org/10.1016/j.soilbio.2020.108120
Lynchu JM (1987) Microbial interactions in the rhizosphere. Soil Microorg 30:33–41. https://doi.org/10.18946/jssm.30.0_33
Mago T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome asemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Mhlongo IM, Piater AL, Madala EN, Labuschagne N, Dubery AI (2018) The chemistry of plant-microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front Plant Sci 9:112. https://doi.org/10.3389/fpls.2018.00112
Morella NM, Weng CH, Joubert PM, Metcalf C, Koskella B (2020) Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. PNAS 117:1148–1159. https://doi.org/10.1073/pnas.1908600116
Mu DS, Ouyang Y, Chen G, Du Z (2021) Strategies for culturing active/dormant marine microbes. Mar Life Sci Technol 3:121–131. https://doi.org/10.1007/s42995-020-00053-z
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. PNAS 104:19891–19896. https://doi.org/10.1073/pnas.0706375104
Quince C, Walker AW, Simpson JT, Loman NJ, Segata N (2017) Shotgun metagenomics, from sampling to analysis. Nat Biotechnol 35:833. https://doi.org/10.1038/nbt.3935
Ramiro L, Shinichi S, Guillem S, Francisco MCC, Isabel F, Hugo S, Pascal H, Hiroyuki O, de Colomban V, Gipsi LM, Jeroen R, Julie P, Olivier J, Patrick W, Stefanie KL, Eric K, Peer B, Silvia GA (2014) Metagenomic 16S rDNA illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol 16(9):2659–2671. https://doi.org/10.1111/1462-2920.12250
Saleem M, Hu J, Jousset A (2019) More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu Rev Ecol Evol Syst 50:145–168. https://doi.org/10.1146/annurev-ecolsys-110617-062605
Shade A, Stopnisek N (2019) Abundance-occupancy distributions to prioritize plant core microbiome membership. Curr Opin Microbiol 49:50–58. https://doi.org/10.1016/j.mib.2019.09.008
Shi H, Shi Q, Wang T, Qin J, Wang Y (2003) Cinnamomum migao, a endemic the miao nationality plant in Guizhou province, China. In: Special edition of national Miao medicine symposium in China, Guiyang, China
Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K, Li J, da Rocha NU, He Z, Pett-Ridge J, Brodie LE, Zhou J, Firestone M (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. Mbio 6(4):e00746-e815. https://doi.org/10.1128/mBio.00746-15
Shi S, Nuccio EE, Shi Z, He Z, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936. https://doi.org/10.1111/ele.12630
Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393. https://doi.org/10.1016/j.tim.2004.06.008
Stopnisek N, Shade A (2021) Persistent microbiome members in the common bean rhizosphere: an integrated analysis of space, time, and plant genotype. ISME J 15:2708–2722. https://doi.org/10.1038/s41396-021-00955-5
Tong B, Liu J, Chen J, Wu M, Guan R (2019) Correlation between fungal diversity in rhizosphere soil and medicinal active components in fruits of Cinnamomum migao. Mycosystema 38(07):1058–1070. https://doi.org/10.13346/j.mycosystema.190062
Wang Y, Zhang L, Feng Y, Zhang Di, Guo S, Pang X, Geng Z, Xi C, Du S (2019) Comparative evaluation of the chemical composition and bioactivities of essential oils from four spice plants (Lauraceae) against stored product insects. Ind Crop Prod 140:111640. https://doi.org/10.1016/j.indcrop.2019.111640
Webb OC, Ackerly DD, McPeek AM, Donoghue JM (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Xun W, Liu Y, Li W, Ren Y, Zhang R (2021) Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome 9(1):35. https://doi.org/10.1186/s40168-020-00985-9
Yang L, Lou J, Wang H, Wu L, Xu J (2018) Use of an improved high-throughput absolute abundance quantification method to characterize soil bacterial community and dynamics. Sci Total Environ 633:360–371. https://doi.org/10.1016/j.scitotenv.2018.03.201
Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P, Huang Q, Bai Y, Vivanco MJ, Kowalchuk AG, Berendsen LR, Shen Q (2018) Root exudates drive the soil borne legacy of aboveground pathogen infection. Microbiome 6:156. https://doi.org/10.1186/s40168-018-0537-x
Yuan MM, Guo X, Wu L, Zhang Y, Zhou J (2021) Climate warming enhances microbial network complexity and stability. Nat Clim Change 11:343–348. https://doi.org/10.1038/s41558-021-00989-9
Yue Y, Shao T, Long X, He T, Rengel Z (2020) Microbiome structure and function in rhizosphere of Jerusalem artichoke grown in saline land. SciTotal Environ 724:138259. https://doi.org/10.1016/j.scitotenv.2020.138259
Zhalnina K, Louie KB, Hao Z, Mansoori N, Rocha U, Shi S, Cho H, Karaoz U, Loqué D, Bowen BP (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
Zhang J, Liu YX, Guo X, Qin Y, Garrido-Oter R, Schulze-Lefert P, Bai Y (2021) High-throughput cultivation and identification of bacteria from the plant root microbiota. Nat Protoc 16:988–1012. https://doi.org/10.1038/s41596-020-00444-7
Zhong W, Yian G, VillePetri F, Kowalchuk GA, Xu YC, Qirong S, Alexandre J (2019) Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv 5(9):eaaw0759. https://doi.org/10.1126/sciadv.aaw0759
Zhou T, Yang Z, Jiang W, Qiang AI, Guo P (2010) Variation and regularity of volatile oil constituents in fruits of national medicine Cinnamomum migao. China J Chin Mater Med 35(07):852–856. https://doi.org/10.4268/cjcmm20100710
Zhou Y, Coventry DR, Gupta V, Fuentes D, Denton MD (2020) The preceding root system drives the composition and function of the rhizosphere microbiome. Genome Biol 21(1):89. https://doi.org/10.1186/s13059-020-01999-0
Zimmerman N, Izard J, Klatt C, Zhou J, Aronson E (2014) The unseen world: environmental microbial sequencing and identification methods for ecologists. Front Ecol Environ 12(4):224–231. https://doi.org/10.1890/130055
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We thank Rosalie K for his help with language revision.
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This work was supported by the National Natural Science Foundation of Unite, China (U1812403-2), The Guizhou Science and Technology Program (Qiankehe [2019]2774).
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Chen, Jz., Liu, Jm. & Liao, Xf. Effects of rhizosphere microbiome on the fruit of Cinnamomum migao H. W. Li: culture, amplicon sequencing, and metagenomic sequencing. Hortic. Environ. Biotechnol. 64, 785–800 (2023). https://doi.org/10.1007/s13580-023-00516-z
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DOI: https://doi.org/10.1007/s13580-023-00516-z