Skip to main content
Log in

A Malvaceae-specific miRNA targeting the newly duplicated GaZIP1L to regulate Zn2+ ion transporter capacity in cotton ovules

  • Cover Article
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) play critical roles in regulating gene expression in plants, yet their functions underlying cultivated diploid Gossypium arboreum cotton ovule development are largely unknown. Here, we acquired small RNA profiles from G. arboreum ovules and fibers collected at different growth stages, and identified 46 novel miRNAs that accounted for 23.7% of all miRNAs in G. arboreum reported in the latest plant sRNA database. Through analysis of 84 (including 38 conserved) differentially expressed G. arboreum miRNAs, we detected 215 putative protein-coding genes in 26 biological processes as their potential targets. A Malvaceae-specific novel miRNA named gar-miRN44 was found to likely regulate cotton ovule growth by targeting to a newly duplicated Zn2+ ion transporter gene GaZIP1L. During cotton ovule development, gar-miRN44 transcript level decreased sharply after 10 to 15 days post-anthesis (DPA), while that of the GaZIP1L increased significantly, with a concomitant increase of Zn2+ ion concentration in late ovule developmental stages. Molecular dynamics simulation and ion absorption analysis showed that GaZIP1L has stronger Zn2+ ion binding ability than the original GaZIP1, indicating that the newly evolved GaZIP1L may be more suitable for maintaining high Zn2+ ion transport capacity that is likely required for cotton ovule growth via enhanced cellulose synthase activities. Our systematic miRNA profiling in G. arboreum and characterization of gar-miRN44 not only contribute to the understanding of miRNA function in cotton, but also provide potential targets for plant breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Axtell, M.J., and Bowman, J.L. (2008). Evolution of plant microRNAs and their targets. Trends Plant Sci 13, 343–349.

    Article  CAS  PubMed  Google Scholar 

  • Ayubov, M.S., Mirzakhmedov, M.H., Sripathi, V.R., Buriev, Z.T., Ubaydullaeva, K.A., Usmonov, D.E., Norboboyeva, R.B., Emani, C., Kumpatla, S.P., and Abdurakhmonov, I.Y. (2019). Role of microRNAs and small RNAs in regulation of developmental processes and agronomic traits in Gossypium species. Genomics 111, 1018–1025.

    Article  CAS  PubMed  Google Scholar 

  • Baumberger, N., and Baulcombe, D.C. (2005). Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102, 11928–11933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao, J.F., Zhao, B., Huang, C.C., Chen, Z.W., Zhao, T., Liu, H.R., Hu, G.J., Shangguan, X.X., Shan, C.M., Wang, L.J., et al. (2020). The miR319-targeted GhTCP4 promotes the transition from cell elongation to wall thickening in cotton fiber. Mol Plant 13, 1063–1077.

    Article  CAS  PubMed  Google Scholar 

  • Chen, F.Y., Chen, X.Y., and Mao, Y.B. (2019). Heterogeneous signals in plant-biotic interactions and their applications. Sci China Life Sci 62, 1707–1709.

    Article  PubMed  Google Scholar 

  • Deng, Y., Wang, J., Tung, J., Liu, D., Zhou, Y., He, S., Du, Y., Baker, B., and Li, F. (2018). A role for small RNA in regulating innate immunity during plant growth. PLoS Pathog 14, e1006756.

    Article  PubMed  PubMed Central  Google Scholar 

  • Du, X., Huang, G., He, S., Yang, Z., Sun, G., Ma, X., Li, N., Zhang, X., Sun, J., Liu, M., et al. (2018). Resequencing of 243 diploid cotton accessions based on an updated A genome identifies the genetic basis of key agronomic traits. Nat Genet 50, 796–802.

    Article  CAS  PubMed  Google Scholar 

  • Eide, D., Broderius, M., Fett, J., and Guerinot, M.L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93, 5624–5628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farooq, M., Mansoor, S., Guo, H., Amin, I., Chee, P.W., Azim, M.K., and Paterson, A.H. (2017). Identification and characterization of miRNA transcriptome in Asiatic cotton (Gossypium arboreum) using high throughput sequencing. Front Plant Sci 8, 969.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong, Z., Xiong, L., Shi, H., Yang, S., Herrera-Estrella, L.R., Xu, G., Chao, D.Y., Li, J., Wang, P.Y., Qin, F., et al. (2020). Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci, doi: https://doi.org/10.1007/s11427-020-1683-x.

  • Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M.L., and Eide, D. (1998). Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA 95, 7220–7224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan, X., Pang, M., Nah, G., Shi, X., Ye, W., Stelly, D.M., and Chen, Z.J. (2014). miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat Commun 5, 3050.

    Article  PubMed  Google Scholar 

  • Hu, Y., Chen, J., Fang, L., Zhang, Z., Ma, W., Niu, Y., Ju, L., Deng, J., Zhao, T., Lian, J., et al. (2019). Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet 51, 739–748.

    Article  CAS  PubMed  Google Scholar 

  • Huang, G., Wu, Z., Percy, R.G., Bai, M., Li, Y., Frelichowski, J.E., Hu, J., Wang, K., Yu, J.Z., and Zhu, Y. (2020). Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution. Nat Genet 52, 516–524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, G., and Zhu, Y.X. (2018). Plant polyploidy and evolution. J Integr Plant Biol jipb.12758.

  • Ji, S.J., Lu, Y.C., Feng, J.X., Wei, G., Li, J., Shi, Y.H., Fu, Q., Liu, D., Luo, J.C., and Zhu, Y.X. (2003). Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic Acids Res 31, 2534–2543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones-Rhoades, M.W., Bartel, D.P., and Bartel, B. (2006). MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57, 19–53.

    Article  CAS  PubMed  Google Scholar 

  • Kambe, T., Tsuji, T., Hashimoto, A., and Itsumura, N. (2015). The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol Rev 95, 749–784.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H.J., and Triplett, B.A. (2001). Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol 127, 1361–1366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurek, I., Kawagoe, Y., Jacob-Wilk, D., Doblin, M., and Delmer, D. (2002). Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proc Natl Acad Sci USA 99, 11109–11114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwak, P.B., Wang, Q.Q., Chen, X.S., Qiu, C.X., and Yang, Z.M. (2009). Enrichment of a set of microRNAs during the cotton fiber development. BMC Genomics 10, 457.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee, H., Yoo, S.J., Lee, J.H., Kim, W., Yoo, S.K., Fitzgerald, H., Carrington, J.C., and Ahn, J.H. (2010). Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38, 3081–3093.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, F., Fan, G., Wang, K., Sun, F., Yuan, Y., Song, G., Li, Q., Ma, Z., Lu, C., Zou, C., et al. (2014). Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet 46, 567–572.

    Article  CAS  PubMed  Google Scholar 

  • Li, F., Fan, G., Lu, C., Xiao, G., Zou, C., Kohel, R.J., Ma, Z., Shang, H., Ma, X., Wu, J., et al. (2015). Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33, 524–530.

    Article  PubMed  Google Scholar 

  • Li, S., Zhou, X., Zhao, Y., Li, H., Liu, Y., Zhu, L., Guo, J., Huang, Y., Yang, W., Fan, Y., et al. (2016). Constitutive expression of the ZmZIP7 in Arabidopsis alters metal homeostasis and increases Fe and Zn content. Plant Physiol Biochem 106, 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Lichten, L.A., and Cousins, R.J. (2009). Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr 29, 153–176.

    Article  PubMed  Google Scholar 

  • Liu, N., Tu, L., Tang, W., Gao, W., Lindsey, K., and Zhang, X. (2014). Small RNA and degradome profiling reveals a role for miRNAs and their targets in the developing fibers of Gossypium barbadense. Plant J 80, 331–344.

    Article  CAS  PubMed  Google Scholar 

  • Luan, Y.X., Wang, B.S., Zhao, Q., Ao, G.M., and Yu, J.J. (2010). Ectopic expression of foxtail millet zip-like gene, SiPf40, in transgenic rice plants causes a pleiotropic phenotype affecting tillering, vascular distribution and root development. Sci China Life Sci 53, 1450–1458.

    Article  CAS  PubMed  Google Scholar 

  • Merelo, P., Ram, H., Pia Caggiano, M., Ohno, C., Ott, F., Straub, D., Graeff, M., Cho, S.K., Yang, S.W., Wenkel, S., et al. (2016). Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity. Proc Natl Acad Sci USA 113, 11973–11978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyers, B.C., Axtell, M.J., Bartel, B., Bartel, D.P., Baulcombe, D., Bowman, J.L., Cao, X., Carrington, J.C., Chen, X., Green, P.J., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell 20, 3186–3190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milner, M.J., Seamon, J., Craft, E., and Kochian, L.V. (2013). Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64, 369–381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreau, S., Thomson, R.M., Kaiser, B.N., Trevaskis, B., Guerinot, M.L., Udvardi, M.K., Puppo, A., and Day, D.A. (2002). GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem 277, 4738–4746.

    Article  CAS  PubMed  Google Scholar 

  • Pang, M., Woodward, A.W., Agarwal, V., Guan, X., Ha, M., Ramachandran, V., Chen, X., Triplett, B.A., Stelly, D.M., and Chen, Z.J. (2009). Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol 10, R122.

    Article  PubMed  PubMed Central  Google Scholar 

  • Paterson, A.H., Wendel, J.F., Gundlach, H., Guo, H., Jenkins, J., Jin, D., Llewellyn, D., Showmaker, K.C., Shu, S., Udall, J., et al. (2012). Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492, 423–427.

    Article  CAS  PubMed  Google Scholar 

  • Ruan, M.B., Zhao, Y.T., Meng, Z.H., Wang, X.J., and Yang, W.C. (2009). Conserved miRNA analysis in Gossypium hirsutum through small RNA sequencing. Genomics 94, 263–268.

    Article  CAS  PubMed  Google Scholar 

  • Qin, Y.M., and Zhu, Y.X. (2011). How cotton fibers elongate: a tale of linear cell-growth mode. Curr Opin Plant Biol 14, 106–111.

    Article  CAS  PubMed  Google Scholar 

  • Qiu, C.X., Xie, F.L., Zhu, Y.Y., Guo, K., Huang, S.Q., Nie, L., and Yang, Z. M. (2007). Computational identification of microRNAs and their targets in Gossypium hirsutum expressed sequence tags. Gene 395, 49–61.

    Article  CAS  PubMed  Google Scholar 

  • Shahid, S., Kim, G., Johnson, N.R., Wafula, E., Wang, F., Coruh, C., Bernal-Galeano, V., Phifer, T., dePamphilis, C.W., Westwood, J.H., et al. (2018). MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553, 82–85.

    Article  CAS  PubMed  Google Scholar 

  • Song, X., Li, Y., Cao, X., and Qi, Y. (2019). MicroRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol 70, 489–525.

    Article  CAS  PubMed  Google Scholar 

  • Souret, F.F., Kastenmayer, J.P., and Green, P.J. (2004). AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15, 173–183.

    Article  CAS  PubMed  Google Scholar 

  • Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E.F., and Hellens, R.P. (2007). Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3, 12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vidal, E.A., Araus, V., Lu, C., Parry, G., Green, P.J., Coruzzi, G.M., and Gutiérrez, R.A. (2010). Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107, 4477–4482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, K., Wang, D., Zheng, X., Qin, A., Zhou, J., Guo, B., Chen, Y., Wen, X., Ye, W., Zhou, Y., et al. (2019). Multi-strategic RNA-seq analysis reveals a high-resolution transcriptional landscape in cotton. Nat Commun 10, 4714.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, K., Wang, Z., Li, F., Ye, W., Wang, J., Song, G., Yue, Z., Cong, L., Shang, H., Zhu, S., et al. (2012). The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44, 1098–1103.

    Article  CAS  PubMed  Google Scholar 

  • Wang, M., Tu, L., Yuan, D., Zhu, D., Shen, C., Li, J., Liu, F., Pei, L., Wang, P., Zhao, G., et al. (2019). Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat Genet 51, 224–229.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Long, X., Chern, M., and Chen, X. (2020). Understanding the molecular mechanisms of trade-offs between plant growth and immunity. Sci China Life Sci, doi: https://doi.org/10.1007/s11427-020-1719-y.

  • Wang, W.Q., Wang, J., Wu, Y.Y., Li, D.W., Allan, A.C., and Yin, X.R. (2019). Genome-wide analysis of coding and non-coding RNA reveals a conserved miR164-NAC regulatory pathway for fruit ripening. New Phytol 225, 1618–1634.

    Article  PubMed  Google Scholar 

  • Wang, Y.M., Ding, Y., Yu, D.W., Xue, W., and Liu, J.Y. (2015). High-throughput sequencing-based genome-wide identification of microRNAs expressed in developing cotton seeds. Sci China Life Sci 58, 778–786.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Wang, L., Zou, Y., Chen, L., Cai, Z., Zhang, S., Zhao, F., Tian, Y., Jiang, Q., Ferguson, B.J., et al. (2014). Soybean miR172c targets the repressive AP2 transcription factor NNC1 to activate ENOD40 expression and regulate nodule initiation. Plant Cell 26, 4782–4801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Z.M., Xue, W., Dong, C.J., Jin, L.G., Bian, S.M., Wang, C., Wu, X. Y., and Liu, J.Y. (2012). A comparative miRNAome analysis reveals seven fiber initiation-related and 36 novel miRNAs in developing cotton ovules. Mol Plant 5, 889–900.

    Article  CAS  PubMed  Google Scholar 

  • Wu, J., Yang, R., Yang, Z., Yao, S., Zhao, S., Wang, Y., Li, P., Song, X., Jin, L., Zhou, T., et al. (2017). ROS accumulation and antiviral defence control by microRNA528 in rice. Nat Plants 3, 16203.

    Article  CAS  PubMed  Google Scholar 

  • Xia, Y., Huang, G., and Zhu, Y. (2019). Sustainable plant disease control: biotic information flow and behavior manipulation. Sci China Life Sci 62, 1710–1713.

    Article  CAS  PubMed  Google Scholar 

  • Xie, F., Wang, Q., Sun, R., and Zhang, B. (2015). Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton. J Exp Bot 66, 789–804.

    Article  CAS  PubMed  Google Scholar 

  • Xie, Y., Liu, Y., Wang, H., Ma, X., Wang, B., Wu, G., and Wang, H. (2017). Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis. Nat Commun 8, 348.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu, L., Hu, Y., Cao, Y., Li, J., Ma, L., Li, Y., and Qi, Y. (2018). An expression atlas of miRNAs in Arabidopsis thaliana. Sci China Life Sci 61, 178–189.

    Article  CAS  PubMed  Google Scholar 

  • Xue, Y., Chen, R., Qu, L., and Cao, X. (2020). Noncoding RNA: from dark matter to bright star. Sci China Life Sci 63, 463–468.

    Article  PubMed  Google Scholar 

  • Yan, J., Zhao, C., Zhou, J., Yang, Y., Wang, P., Zhu, X., Tang, G., Bressan, R.A., and Zhu, J.K. (2016). The miR165/166 mediated regulatory module plays critical roles in ABA homeostasis and response in Arabidopsis thaliana. PLoS Genet 12, e1006416.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, R., Li, P., Mei, H., Wang, D., Sun, J., Yang, C., Hao, L., Cao, S., Chu, C., Hu, S., et al. (2019). Fine-tuning of miR528 accumulation modulates flowering time in rice. Mol Plant 12, 1103–1113.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., Qanmber, G., Wang, Z., Yang, Z., and Li, F. (2020). Gossypium genomics: trends, scope, and utilization for cotton improvement. Trends Plant Sci 25, 488–500.

    Article  CAS  PubMed  Google Scholar 

  • Yu, N., Cai, W.J., Wang, S., Shan, C.M., Wang, L.J., and Chen, X.Y. (2010). Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22, 2322–2335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, Y., Jia, T., and Chen, X. (2017). The ‘how’ and ‘where’ of plant microRNAs. New Phytol 216, 1002–1017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, B., Wang, Q., Wang, K., Pan, X., Liu, F., Guo, T., Cobb, G.P., and Anderson, T.A. (2007). Identification of cotton microRNAs and their targets. Gene 397, 26–37.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, T., Liu, J., Fellner, M., Zhang, C., Sui, D., and Hu, J. (2017). Crystal structures of a ZIP zinc transporter reveal a binuclear metal center in the transport pathway. Sci Adv 3, e1700344.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, T., Zhao, Y.L., Zhao, J.H., Wang, S., Jin, Y., Chen, Z.Q., Fang, Y.Y., Hua, C.L., Ding, S.W., and Guo, H.S. (2016). Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat Plants 2, 16153.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, T., Hu, Y., Jiang, W., Fang, L., Guan, X., Chen, J., Zhang, J., Saski, C.A., Scheffler, B.E., Stelly, D.M., et al. (2015). Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33, 531–537.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Zhao, H., Gao, S., Wang, W.C., Katiyar-Agarwal, S., Huang, H. D., Raikhel, N., and Jin, H. (2011). Arabidopsis Argonaute 2 regulates innate immunity via miRNA393*-mediated silencing of a Golgilocalized SNARE gene, MEMB12. Mol Cell 42, 356–366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Jiao, Y., Jiao, H., Zhao, H., and Zhu, Y.X. (2017). Two-step functional innovation of the stem-cell factors WUS/WOX5 during plant evolution. Mol Biol Evol msw263.

  • Zhou, Y., Honda, M., Zhu, H., Zhang, Z., Guo, X., Li, T., Li, Z., Peng, X., Nakajima, K., Duan, L., et al. (2015). Spatiotemporal sequestration of miR165/166 by Arabidopsis Argonaute10 promotes shoot apical meristem maintenance. Cell Rep 10, 1819–1827.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31690090 and 31690091 to Y.Z.) and the National Postdoctoral Program for Innovative Talent (to G.H.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuxian Zhu.

Additional information

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Electronic supplementary material

11427_2020_1868_MOESM1_ESM.docx

A Malvaceae-specific miRNA targeting the newly duplicated GaZIP1L to regulate Zn2+ ion transporter capacity in cotton ovules, approximately 3.19 MB.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wen, X., Huang, G., Li, C. et al. A Malvaceae-specific miRNA targeting the newly duplicated GaZIP1L to regulate Zn2+ ion transporter capacity in cotton ovules. Sci. China Life Sci. 64, 339–351 (2021). https://doi.org/10.1007/s11427-020-1868-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-020-1868-9

Navigation