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Single-cell transcriptome atlas of the leaf and root of rice seedlings

Yu Wang Qing Huan Ke Li Wenfeng Qian

Yu Wang, Qing Huan, Ke Li, Wenfeng Qian. Single-cell transcriptome atlas of the leaf and root of rice seedlings[J]. 遗传学报, 2021, 48(10): 881-898. doi: 10.1016/j.jgg.2021.06.001
引用本文: Yu Wang, Qing Huan, Ke Li, Wenfeng Qian. Single-cell transcriptome atlas of the leaf and root of rice seedlings[J]. 遗传学报, 2021, 48(10): 881-898. doi: 10.1016/j.jgg.2021.06.001
Yu Wang, Qing Huan, Ke Li, Wenfeng Qian. Single-cell transcriptome atlas of the leaf and root of rice seedlings[J]. Journal of Genetics and Genomics, 2021, 48(10): 881-898. doi: 10.1016/j.jgg.2021.06.001
Citation: Yu Wang, Qing Huan, Ke Li, Wenfeng Qian. Single-cell transcriptome atlas of the leaf and root of rice seedlings[J]. Journal of Genetics and Genomics, 2021, 48(10): 881-898. doi: 10.1016/j.jgg.2021.06.001

Single-cell transcriptome atlas of the leaf and root of rice seedlings

doi: 10.1016/j.jgg.2021.06.001
基金项目: 

We thank Dr. Xiao Chu, Dr. Ying Chen, Yan-Ming Chen, Yuliang Zhang, Min Dai, and Dr. Xiaofeng Gu for supports in data analyses, Ting Li and Yanbo Tian for supports in flow cytometry and fluorescence microscopy, Dr. Caihuan Tian for supports in protoplast isolation, and Dr. Taolan Zhao and Dr. Yuling Jiao for reading the manuscript. This work was supported by grants from the National Natural Science Foundation of China (31900229 to Q.H. and 31922014 to W.Q.).

详细信息
    通讯作者:

    Qing Huan,E-mail:qhuan@genetics.ac.cn

    Wenfeng Qian,E-mail:wfqian@genetics.ac.cn

Single-cell transcriptome atlas of the leaf and root of rice seedlings

Funds: 

We thank Dr. Xiao Chu, Dr. Ying Chen, Yan-Ming Chen, Yuliang Zhang, Min Dai, and Dr. Xiaofeng Gu for supports in data analyses, Ting Li and Yanbo Tian for supports in flow cytometry and fluorescence microscopy, Dr. Caihuan Tian for supports in protoplast isolation, and Dr. Taolan Zhao and Dr. Yuling Jiao for reading the manuscript. This work was supported by grants from the National Natural Science Foundation of China (31900229 to Q.H. and 31922014 to W.Q.).

  • These authors contributed equally to this work
  • 摘要: As a multicellular organism, rice flourishes relying on gene expression diversity among cells of various functions. However, cellular-resolution transcriptome features are yet to be fully recognized, let alone cell-specific transcriptional responses to environmental stimuli. In this study, we apply single-cell RNA sequencing to both shoot and root of rice seedlings growing in Kimura B nutrient solution or exposed to various abiotic stresses and characterize transcriptomes for a total of 237,431 individual cells. We identify 15 and 9 cell types in the leaf and root, respectively, and observe that common transcriptome features are often shared between leaves and roots in the same tissue layer, except for endodermis or epidermis. Abiotic stress stimuli alter gene expression largely in a cell type-specific manner, but for a given cell type, different stresses often trigger transcriptional regulation of roughly the same set of genes. Besides, we detect proportional changes in cell populations in response to abiotic stress and investigate the underlying molecular mechanisms through single-cell reconstruction of the developmental trajectory. Collectively, our study represents a benchmark-setting data resource of single-cell transcriptome atlas for rice seedlings and an illustration of exploiting such resources to drive discoveries in plant biology.
    These authors contributed equally to this work
  • Abdellaoui, R., Boughalleb, F., Chebil, Z., Mahmoudi, M., Belgacem, A.O., 2017. Physiological, anatomical and antioxidant responses to salinity in the Mediterranean pastoral grass plant Stipa lagascae. Crop Pasture Sci. 68, 872-884.
    Anders, S., Pyl, P.T., Huber, W., 2015. HTSeq–a Python framework to work with highthroughput sequencing data. Bioinformatics 31, 166-169.
    Birnbaum, K., Jung, J.W., Wang, J.Y., Lambert, G.M., Hirst, J.A., Galbraith, D.W., Benfey, P.N., 2005. Cell type-specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat. Methods 2, 615-619.
    Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., Benfey, P.N., 2003. A gene expression map of the Arabidopsis root. Science 302, 1956-1960.
    Blondel, V.D., Guillaume, J.-L., Lambiotte, R., Lefebvre, E., 2008. Fast unfolding of communities in large networks. J. Stat. Mech. Theor. Exp. 2008, P10008.
    Buenrostro, J.D., Wu, B., Litzenburger, U.M., Ruff, D., Gonzales, M.L., Snyder, M.P., Chang, H.Y., Greenleaf, W.J., 2015. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523, 486-490.
    Butler, A., Hoffman, P., Smibert, P., Papalexi, E., Satija, R., 2018. Integrating singlecell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411-420.
    Chen, Y., Li, K., Chu, X., Carey, L.B., Qian, W., 2019. Synchronized replication of genes encoding the same protein complex in fast-proliferating cells. Genome Res. 29, 1929-1938.
    Chonan, N., 1978. A comparative anatomy of mesophyll among the leaves of gramineous crops. Jpn. Agric. Res. Q. 12, 128-131.
    Denyer, T., Ma, X., Klesen, S., Scacchi, E., Nieselt, K., Timmermans, M.C.P., 2019. Spatiotemporal developmental trajectories in the Arabidopsis root revealed using high-throughput single-cell RNA sequencing. Dev. Cell 48, 840-852. e845.
    Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J., Benfey, P.N., 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942-945.
    Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21.
    Efroni, I., Ip, P.L., Nawy, T., Mello, A., Birnbaum, K.D., 2015. Quantification of cell identity from single-cell gene expression profiles. Genome Biol. 16, 9.
    Evrard, A., Bargmann, B.O., Birnbaum, K.D., Tester, M., Baumann, U., Johnson, A.A., 2012. Fluorescence-activated cell sorting for analysis of cell type-specific responses to salinity stress in Arabidopsis and rice. Methods Mol. Biol. 913, 265-276.
    Frank, M.H., Scanlon, M.J., 2015. Cell-specific transcriptomic analyses of threedimensional shoot development in the moss Physcomitrella patens. Plant J. 83, 743-751.
    Giacomello, S., Salmen, F., Terebieniec, B.K., Vickovic, S., Navarro, J.F., Alexeyenko, A., Reimegard, J., McKee, L.S., Mannapperuma, C., Bulone, V., et al., 2017. Spatially resolved transcriptome profiling in model plant species. Native Plants 3, 17061.
    Gui, J., Shen, J., Li, L., 2011. Functional characterization of evolutionarily divergent 4-coumarate:coenzyme A ligases in rice. Plant Physiol. 157, 574-586.
    Hafemeister, C., Satija, R., 2019. Normalization and variance stabilization of singlecell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 296.
    Haghverdi, L., Lun, A.T.L., Morgan, M.D., Marioni, J.C., 2018. Batch effects in singlecell RNA-sequencing data are corrected by matching mutual nearest neighbors. Nat. Biotechnol. 36, 421-427.
    Hainer, S.J., Boskovic, A., McCannell, K.N., Rando, O.J., Fazzio, T.G., 2019. Profiling of pluripotency factors in single cells and early embryos. Cell 177, 1319-1329 e1311.
    Han, Y., Chu, X., Yu, H., Ma, Y.-K., Wang, X.-J., Qian, W., Jiao, Y., 2017. Single-cell transcriptome analysis reveals widespread monoallelic gene expression in individual rice mesophyll cells. Sci. Bull. 62, 1304-1314.
    Huan, Q., Zhang, Y., Wu, S., Qian, W., 2018. HeteroMeth: a database of cell-to-cell heterogeneity in DNA methylation. Genom. Proteom. Bioinform. 16, 234-243.
    Jabnoune, M., Secco, D., Lecampion, C., Robaglia, C., Shu, Q., Poirier, Y., 2015. An efficient procedure for protoplast isolation from mesophyll cells and nuclear fractionation in rice. Bio-protocol 5. https://doi.org/10.21769/BioProtoc.1412.
    Jean-Baptiste, K., McFaline-Figueroa, J.L., Alexandre, C.M., Dorrity, M.W., Saunders, L., Bubb, K.L., Trapnell, C., Fields, S., Queitsch, C., Cuperus, J.T., 2019. Dynamics of gene expression in single root cells of Arabidopsis thaliana. Plant Cell 31, 993-1011.
    Jiao, Y., Meyerowitz, E.M., 2010. Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol. Syst. Biol. 6, 419.
    Jiao, Y., Tausta, S.L., Gandotra, N., Sun, N., Liu, T., Clay, N.K., Ceserani, T., Chen, M., Ma, L., Holford, M., et al., 2009. A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat. Genet. 41, 258-263.
    Kawahara, Y., de la Bastide, M., Hamilton, J.P., Kanamori, H., McCombie, W.R., Ouyang, S., Schwartz, D.C., Tanaka, T., Wu, J., Zhou, S., et al., 2013. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6, 4.
    Kawata, S.-i., Suzuki, S., Yamazaki, k., 1979. The detachment of the “primary root caps” in rice plants. Jpn. J. Crop Sci. 48, 303-310.
    Lai, B., Gao, W., Cui, K., Xie, W., Tang, Q., Jin, W., Hu, G., Ni, B., Zhao, K., 2018. Principles of nucleosome organization revealed by single-cell micrococcal nuclease sequencing. Nature 562, 281-285.
    Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M., et al., 2012. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40, D1202-D1210.
    Lex, A., Gehlenborg, N., Strobelt, H., Vuillemot, R., Pfister, H., 2014. UpSet: visualization of intersecting sets. IEEE Trans. Visual. Comput. Graph. 20, 1983-1992.
    Lieckfeldt, E., Simon-Rosin, U., Kose, F., Zoeller, D., Schliep, M., Fisahn, J., 2008. Gene expression profiling of single epidermal, basal and trichome cells of Arabidopsis thaliana. J. Plant Physiol. 165, 1530-1544.
    Liu, Q., Liang, Z., Feng, D., Jiang, S., Wang, Y., Du, Z., Li, R., Hu, G., Zhang, P., Ma, Y., et al., 2021. Transcriptional landscape of rice roots at the single-cell resolution. Mol. Plant 14, 384-394.
    Liu, H.L., Xu, Y.Y., Xu, Z.H., Chong, K., 2007. A rice YABBY gene, OsYABBY4, preferentially expresses in developing vascular tissue. Dev. Gene. Evol. 217, 629-637.
    Liu, Z., Zhou, Y., Guo, J., Li, J., Tian, Z., Zhu, Z., Wang, J., Wu, R., Zhang, B., Hu, Y., et al., 2020. Global dynamic molecular profiling of stomatal lineage cell development by single-cell RNA sequencing. Mol. Plant 13, 1178-1193.
    Long, Y., Liu, Z., Jia, J., Mo, W., Fang, L., Lu, D., Liu, B., Zhang, H., Chen, W., Zhai, J., 2021. FlsnRNA-seq: protoplasting-free full-length single-nucleus RNA profiling in plants. Genome Biol. 22, 66.
    McInnes, L., Healy, J., Melville, J., 2018. UMAP: uniform manifold approximation and projection for dimension reduction. arXiv, 180203426.
    Mustroph, A., Zanetti, M.E., Jang, C.J., Holtan, H.E., Repetti, P.P., Galbraith, D.W., Girke, T., Bailey-Serres, J., 2009. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 106, 18843-18848.
    Negi, J., Matsuda, O., Nagasawa, T., Oba, Y., Takahashi, H., Kawai-Yamada, M., Uchimiya, H., Hashimoto, M., Iba, K., 2008. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452, 483-486.
    Rebouillat, J., Dievart, A., Verdeil, J.L., Escoute, J., Giese, G., Breitler, J.C., Gantet, P., Espeout, S., Guiderdoni, E., Périn, C., 2009. Molecular genetics of rice root development. Rice 2, 15-34.
    Rhee, S.Y., Birnbaum, K.D., Ehrhardt, D.W., 2019. Towards building a plant cell atlas. Trends Plant Sci. 24, 303-310.
    Rich-Griffin, C., Stechemesser, A., Finch, J., Lucas, E., Ott, S., Schafer, P., 2020. Single-cell transcriptomics: a high-resolution avenue for plant functional genomics. Trends Plant Sci. 25, 186-197.
    Ryu, K.H., Huang, L., Kang, H.M., Schiefelbein, J., 2019. Single-cell RNA sequencing resolves molecular relationships among individual plant cells. Plant Physiol. 179, 1444-1456.
    Shulse, C.N., Cole, B.J., Ciobanu, D., Lin, J., Yoshinaga, Y., Gouran, M., Turco, G.M., Zhu, Y., O’Malley, R.C., Brady, S.M., et al., 2019. High-throughput single-cell transcriptome profiling of plant cell types. Cell Rep. 27, 2241-2247. e2244.
    Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck 3rd, W.M., Hao, Y., Stoeckius, M., Smibert, P., Satija, R., 2019. Comprehensive integration of single-cell data. Cell 177, 1888-1902. e1821.
    Takehisa, H., Sato, Y., Igarashi, M., Abiko, T., Antonio, B.A., Kamatsuki, K., Minami, H., Namiki, N., Inukai, Y., Nakazono, M., et al., 2012. Genome-wide transcriptome dissection of the rice root system: implications for developmental and physiological functions. Plant J. 69, 126-140.
    Tian, C., Du, Q., Xu, M., Du, F., Jiao, Y., 2020. Single-nucleus RNA-seq resolves spatiotemporal developmental trajectories in the tomato shoot apex. bioRxiv, 2020.2009.2020.305029.
    Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z., Xu, W., Su, Z., 2017. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122-W129.
    Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N.J., Livak, K.J., Mikkelsen, T.S., Rinn, J.L., 2014. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381-386.
    Tsutsumi, K., Taniguchi, Y., Kawasaki, M., Taniguchi, M., Miyake, H., 2006. Expression of photosynthesis-related genes during the leaf development of a C3 plant rice as visualized by in situ hybridization. Plant Prod. Sci. 9, 232-241.
    Turco, G.M., Rodriguez-Medina, J., Siebert, S., Han, D., Valderrama-Gomez, M.A., Vahldick, H., Shulse, C.N., Cole, B.J., Juliano, C.E., Dickel, D.E., et al., 2019. Molecular mechanisms driving switch behavior in xylem cell differentiation. Cell Rep. 28, 342-351. e344.
    Umeda, M., Umeda-Hara, C., Yamaguchi, M., Hashimoto, J., Uchimiya, H., 1999. Differential expression of genes for cyclin-dependent protein kinases in rice plants. Plant Physiol. 119, 31-40.
    Vahisalu, T., Kollist, H., Wang, Y.F., Nishimura, N., Chan, W.Y., Valerio, G., Lamminmaki, A., Brosche, M., Moldau, H., Desikan, R., et al., 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452, 487-491.
    Wang, Y., Song, F., Zhu, J., Zhang, S., Yang, Y., Chen, T., Tang, B., Dong, L., Ding, N., Zhang, Q., et al., 2017. GSA: Genome Sequence Archive. Genom. Proteom. Bioinform. 15, 14-18.
    Wendrich, J.R., Yang, B., Vandamme, N., Verstaen, K., Smet, W., Van de Velde, C., Minne, M., Wybouw, B., Mor, E., Arents, H.E., et al., 2020. Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions. Science 370, eaay4970.
    Zeng, M., Hu, B., Li, J., Zhang, G., Ruan, Y., Huang, H., Wang, H., Xu, L., 2016. Stem cell lineage in body layer specialization and vascular patterning of rice root and leaf. Sci. Bull. 61, 847-858.
    Zhang, T.Q., Chen, Y., Liu, Y., Lin, W.H., Wang, J.W., 2021a. Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root. Nat. Commun. 12, 2053.
    Zhang, T.Q., Chen, Y., Wang, J.W., 2021b. A single-cell analysis of the Arabidopsis vegetative shoot apex. Dev. Cell 56, 1056-1074. e1058.
    Zhang, T.Q., Xu, Z.G., Shang, G.D., Wang, J.W., 2019. A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol. Plant 12, 648-660.
    Zheng, G.X., Terry, J.M., Belgrader, P., Ryvkin, P., Bent, Z.W., Wilson, R., Ziraldo, S.B., Wheeler, T.D., McDermott, G.P., Zhu, J., et al., 2017. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8, 14049.
    Zhou, L.J., Xiao, L.T., Xue, H.W., 2017. Dynamic cytology and transcriptional regulation of rice lamina joint development. Plant Physiol. 174, 1728-1746.
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  • 收稿日期:  2021-06-08
  • 录用日期:  2021-06-09
  • 刊出日期:  2021-06-18

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