The rice histone methylation regulates hub species of the root microbiota

Zhiyao Lv; Rui Dai; Haoran Xu; Yongxin Liu; Bo Bai; Ying Meng; Haiyan Li; Xiaofeng Cao; Yang Bai; Xianwei Song; Jingying Zhang

doi:10.1016/j.jgg.2021.06.005

Volume 48 Issue 9

Sep. 2021

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The rice histone methylation regulates hub species of the root microbiota

doi: 10.1016/j.jgg.2021.06.005

Zhiyao Lv^a,
Rui Dai^b,c,d,e,
Haoran Xu^b,c,d,e,
Yongxin Liu^b,c,d,
Bo Bai^b,c,f,
Ying Meng^g,
Haiyan Li^a,
Xiaofeng Cao^b,e,h,
Yang Bai^b,c,d,e,
Xianwei Song^b,i,
Jingying Zhang^b,c,d

a. College of Life Sciences, Engineering Research Center of the Chinese Ministry of Education for Bioreactor and Pharmaceutical Development, Jilin Agricultural University, Changchun, Jilin 130118, China;
b. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
c. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China;
d. CAS-JIC Centre of Excellence for Plant and Microbial Science, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
e. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;
f. Shandong Rice Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, China;
g. Institute of Farming and Cultivation, Heilongjiang Provincial Academy of Agricultural Sciences, Harbin 150086, China;
h. Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing 100101, China;
i. INASEED, Chinese Academy of Sciences, Beijing 100101, China

Funds:

31801945 to J.Z.), and the Youth Innovation Promotion Association CAS (2020101 to J.Z.

QYZDY-SSW-SMC022 to X.C.), the National Natural Science Foundation of China (31788103 to X.C.

2021092 to Y.L.).

XDB27030201 to X.C.), the Key Research Program of Frontier Sciences of the Chinese Academy of Sciences (QYZDB-SSW-SMC021 to Y.B.

This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA24020104 to Y.B.

Received Date: 2021-06-09
Accepted Date: 2021-06-20
Rev Recd Date: 2021-06-20
Publish Date: 2021-07-02

Abstract

Abstract

Plants have a close relationship with their root microbiota, which comprises a complex microbial network. Histone methylation is an important epigenetic modification influencing multiple plant traits; however, little is known about the role of plant histone methylation in the assembly and network structure of the root microbiota. In this study, we established that the rice (Oryza sativa) histone methylation regulates the structure and composition of the root microbiota, especially the hub species in the microbial network. DJ-jmj703 (defective in histone H3K4 demethylation) and ZH11-sdg714 (defective in H3K9 methylation) showed significant different root microbiota compared with the corresponding wild types at the phylum and family levels, with a consistent increase in the abundance of Betaproteobacteria and a decrease in the Firmicutes. In the root microbial network, 35 of 44 hub species in the top 10 modules in the tested field were regulated by at least one histone methylation-related gene. These observations establish that the rice histone methylation plays a pivotal role in regulating the assembly of the root microbiota, providing insights into the links between plant epigenetic regulation and root microbiota.
- Histone methylation,
- Root microbiota,
- Hub species,
- Co-occurrence network,
- Rice,
- Epigenetics

These authors contribute equally to this work.

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References(45)

References

Allis, C.D., Jenuwein, T., 2016. The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 17, 487-500.

Andrews, S., 2010. Fastqc: A quality control tool for high throughput sequence data. https://www.Bioinformatics.Babraham.Ac.Uk/projects/fastqc/.

Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: an open source software for exploring and manipulating networks. AAAI ICWSM.

Berni Canani, R., Di Costanzo, M., Leone, L., 2012. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin. Epigenet. 4, 4.

Berry, D., Widder, S., 2014. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol. 5, 219.

Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al-Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852-857.

Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., 2012. Revealing structure and assembly cues for arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95.

Cao, X., Aufsatz, W., Zilberman, D., Mette, M.F., Huang, M.S., Matzke, M., Jacobsen, S.E., 2003. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212-2217.

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., 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336.

Carrion, V.J., Perez-Jaramillo, J., Cordovez, V., Tracanna, V., de Hollander, M., Ruiz-Buck, D., Mendes, L.W., van Ijcken, W.F.J., Gomez-Exposito, R., Elsayed, S.S., 2019. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366, 606-612.

Carthew, R.W., Sontheimer, E.J., 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655.

Castrillo, G., Teixeira, P.J., Paredes, S.H., Law, T.F., de Lorenzo, L., Feltcher, M.E., Finkel, O.M., Breakfield, N.W., Mieczkowski, P., Jones, C.D., 2017. Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513-518.

Chan, S.W., Zilberman, D., Xie, Z., Johansen, L.K., Carrington, J.C., Jacobsen, S.E., 2004. RNA silencing genes control de novo DNA methylation. Science 303, 1336.

Cui, X., Jin, P., Cui, X., Gu, L., Lu, Z., Xue, Y., Wei, L., Qi, J., Song, X., Luo, M., 2013. Control of transposon activity by a histone H3K4 demethylase in rice. Proc. Natl. Acad. Sci. U. S. A. 110, 1953-1958.

de Vries, F.T., Griffiths, R.I., Bailey, M., Craig, H., Girlanda, M., Gweon, H.S., Hallin, S., Kaisermann, A., Keith, A.M., Kretzschmar, M., 2018. Soil bacterial networks are less stable under drought than fungal networks. Nat. Commun. 9, 3033.

Deng, X., Song, X.W., Wei, L.Y., Liu, C.Y., Cao, X.F., 2016. Epigenetic regulation and epigenomic landscape in rice. Natl. Sci. Rev. 3, 309-327.

Ding, Y., Wang, X., Su, L., Zhai, J., Cao, S., Zhang, D., Liu, C., Bi, Y., Qian, Q., Cheng, Z., 2007. SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19, 9-22.

Duran, P., Thiergart, T., Garrido-Oter, R., Agler, M., Kemen, E., Schulze-Lefert, P., Hacquard, S., 2018. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175, 973-983 e914.

Edgar, R.C., 2010. Search and clustering orders of magnitude faster than blast. Bioinformatics 26, 2460-2461.

Edwards, J., Johnson, C., Santos-Medellin, C., Lurie, E., Podishetty, N.K., Bhatnagar, S., Eisen, J.A., Sundaresan, V., 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U. S. A. 112, E911-E920.

Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538-550.

Ginestet, C., ggplot2: elegant graphics for data analysis. J. R. Stat. Soc. a Stat. 174, 245-245.

Harbort, C.J., Hashimoto, M., Inoue, H., Niu, Y., Guan, R., Rombola, A.D., Kopriva, S., Voges, M., Sattely, E.S., Garrido-Oter, R., 2020. Root-secreted coumarins and the microbiota interact to improve iron nutrition in Arabidopsis. Cell Host Microbe 28, 825-837. e826.

Huang, A.C., Jiang, T., Liu, Y.X., Bai, Y.C., Reed, J., Qu, B., Goossens, A., Nutzmann, H.W., Bai, Y., Osbourn, A., 2019. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364, eaau6389.

Huang, X.Q., Zhou, X., Zhang, J.B., Cai, Z.C., 2019. Highly connected taxa located in the microbial network are prevalent in the rhizosphere soil of healthy plant. Biol. Fertil. Soils 55, 299-312.

Kaushal, R., Peng, L., Singh, S.K., Zhang, M., Zhang, X., Vilchez, J.I., Wang, Z., He, D., Yang, Y., Lv, S., 2021. Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation. Microbiome 9, 57.

Kumar, M., Yadav, A.N., Saxena, R., Rai, P.K., Paul, D., Tomar, R.S., 2021. Novel methanotrophic and methanogenic bacterial communities from diverse ecosystems and their impact on environment. Biocatal. Agric. Biotechnol. 33., 10.1016/j.bcab.2021.102005.

Lebeis, S.L., Paredes, S.H., Lundberg, D.S., Breakfield, N., Gehring, J., McDonald, M., Malfatti, S., Glavina del Rio, T., Jones, C.D., Tringe, S.G., 2015. Plant microbiome. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860-864.

Liu, C., Lu, F., Cui, X., Cao, X., 2010. Histone methylation in higher plants. Annu. Rev. Plant Biol. 61, 395-420.

Liu, Y., Qin, Y., Guo, X., Bai, Y., 2019. Methods and applications for microbiome data analysis. Yi Chuan 41, 845-862.

Liu, Y.X., Qin, Y., Chen, T., Lu, M., Qian, X., Guo, X., Bai, Y., 2021. A practical guide to amplicon and metagenomic analysis of microbiome data. Protein Cell 12, 315-330.

Lundberg, D.S., Lebeis, S.L., Paredes, S.H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., Rio, T.G.d., 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90.

Ono, A., Kinoshita, T., 2021. Epigenetics and plant reproduction: multiple steps for responsibly handling succession. Curr. Opin. Plant Biol. 61, 102032.

Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596.

Ramos-Cruz, D., Troyee, A.N., Becker, C., 2021. Epigenetics in plant organismic interactions. Curr. Opin. Plant Biol. 61, 102060.

Ridenhour, B.J., Brooker, S.L., Williams, J.E., Van Leuven, J.T., Miller, A.W., Dearing, M.D., Remien, C.H., 2017. Modeling time-series data from microbial communities. ISME J. 11, 2526-2537.

Rottjers, L., Faust, K., 2018. From hairballs to hypotheses-biological insights from microbial networks. FEMS Microbiol. Rev. 42, 761-780.

Salas-Gonzalez, I., Reyt, G., Flis, P., Custodio, V., Gopaulchan, D., Bakhoum, N., Dew, T.P., Suresh, K., Franke, R.B., Dangl, J.L., 2021. Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis. Science 371, 10.1126/science.abd0695.

Samantara, K., Shiv, A., de Sousa, L.L., Sandhu, K.S., Priyadarshini, P., Mohapatra, S.R., 2021. A comprehensive review on epigenetic mechanisms and application of epigenetic modifications for crop improvement. Environ. Exp. Bot. 188., 10.1016/j.envexpbot.2021.104479.

Shi, S., Nuccio, E.E., Shi, Z.J., He, Z., Zhou, J., Firestone, M.K., 2016. The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol. Lett. 19, 926-936.

Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., 2007. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267.

Wei, L., Gu, L., Song, X., Cui, X., Lu, Z., Zhou, M., Wang, L., Hu, F., Zhai, J., Meyers, B.C., 2014. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc. Natl. Acad. Sci. U. S. A. 111, 3877-3882.

Xie, Z., Johansen, L.K., Gustafson, A.M., Kasschau, K.D., Lellis, A.D., Zilberman, D., Jacobsen, S.E., Carrington, J.C., 2004. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104.

Zhang, H., Lang, Z., Zhu, J.K., 2018. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489-506.

Zhang, J., Liu, Y.X., Zhang, N., Hu, B., Jin, T., Xu, H., Qin, Y., Yan, P., Zhang, X., Guo, X., 2019. Nrt1.1b is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37, 676-684.

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