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Plant synthetic epigenomic engineering for crop improvement

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Abstract

Efforts have been directed to redesign crops with increased yield, stress adaptability, and nutritional value through synthetic biology—the application of engineering principles to biology. A recent expansion in our understanding of how epigenetic mechanisms regulate plant development and stress responses has unveiled a new set of resources that can be harnessed to develop improved crops, thus heralding the promise of “synthetic epigenetics.” In this review, we summarize the latest advances in epigenetic regulation and highlight how innovative sequencing techniques, epigenetic editing, and deep learning-driven predictive tools can rapidly extend these insights. We also proposed the future directions of synthetic epigenetics for the development of engineered smart crops that can actively monitor and respond to internal and external cues throughout their life cycles.

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References

  • Anderson, J.C., Clarke, E.J., Arkin, A.P., and Voigt, C.A. (2006). Environmentally controlled invasion of cancer cells by engineered bacteria. J Mol Biol 355, 619–627.

    Article  PubMed  CAS  Google Scholar 

  • Angermueller, C., Lee, H.J., Reik, W., and Stegle, O. (2017). DeepCpG: accurate prediction of single-cell DNA methylation states using deep learning. Genome Biol 18, 67.

    Article  PubMed  PubMed Central  Google Scholar 

  • Anzalone, A.V., Koblan, L.W., and Liu, D.R. (2020). Genome editing with CRISPR-Cas nucleases, base editors, transposases and prime editors. Nat Biotechnol 38, 824–844.

    Article  PubMed  CAS  Google Scholar 

  • Arribas-Hernández, L., Bressendorff, S., Hansen, M.H., Poulsen, C., Erdmann, S., and Brodersen, P. (2018). An m6A-YTH module controls developmental timing and morphogenesis in arabidopsis. Plant Cell 30, 952–967.

    Article  PubMed  PubMed Central  Google Scholar 

  • Belcher, M.S., Vuu, K.M., Zhou, A., Mansoori, N., Agosto Ramos, A., Thompson, M.G., Scheller, H.V., Loqué, D., and Shih, P.M. (2020). Design of orthogonal regulatory systems for modulating gene expression in plants. Nat Chem Biol 16, 857–865.

    Article  PubMed  CAS  Google Scholar 

  • Berhanu, S., Ueda, T., and Kuruma, Y. (2019). Artificial photosynthetic cell producing energy for protein synthesis. Nat Commun 10, 1325.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bozsoki, Z., Gysel, K., Hansen, S.B., Lironi, D., Krönauer, C., Feng, F., de Jong, N., Vinther, M., Kamble, M., Thygesen, M.B., et al. (2020). Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity. Science 369, 663–670.

    Article  PubMed  CAS  Google Scholar 

  • Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., and Greenleaf, W.J. (2013). Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10, 1213–1218.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cavalli, G., and Heard, E. (2019). Advances in epigenetics link genetics to the environment and disease. Nature 571, 489–499.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J.H., Chen, S.T., He, N.Y., Wang, Q.L., Zhao, Y., Gao, W., and Guo, F.Q. (2020b). Nuclear-encoded synthesis of the D1 subunit of photosystem II increases photosynthetic efficiency and crop yield. Nat Plants 6, 570–580.

    Article  PubMed  CAS  Google Scholar 

  • Chen, R., Deng, Y., Ding, Y., Guo, J., Qiu, J., Wang, B., Wang, C., Xie, Y., Zhang, Z., Chen, J., et al. (2022a). Rice functional genomics: decades’ efforts and roads ahead. Sci China Life Sci 65, 33–92.

    Article  PubMed  Google Scholar 

  • Chen, X., Chen, S., Song, S., Gao, Z., Hou, L., Zhang, X., Lv, H., and Jiang, R. (2022b). Cell type annotation of single-cell chromatin accessibility data via supervised Bayesian embedding. Nat Mach Intell 4, 116–126.

    Article  Google Scholar 

  • Chen, Y., Nie, F., Xie, S.Q., Zheng, Y.F., Dai, Q., Bray, T., Wang, Y.X., Xing, J.F., Huang, Z.J., Wang, D.P., et al. (2021). Efficient assembly of nanopore reads via highly accurate and intact error correction. Nat Commun 12, 60.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, Z., and Zhang, Y. (2020). Role of mammalian DNA methyltransferases in development. Annu Rev Biochem 89, 135–158.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, P., Bao, S., Li, C., Tong, J., Shen, L., and Yu, H. (2022). RNA N6-methyladenosine modification promotes auxin biosynthesis required for male meiosis in rice. Dev Cell 57, 246–259.e4.

    Article  PubMed  CAS  Google Scholar 

  • Crevillén, P., Yang, H., Cui, X., Greeff, C., Trick, M., Qiu, Q., Cao, X., and Dean, C. (2014). Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515, 587–590.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui, X., Liang, Z., Shen, L., Zhang, Q., Bao, S., Geng, Y., Zhang, B., Leo, V., Vardy, L.A., Lu, T., et al. (2017). 5-methylcytosine RNA methylation in Arabidopsis thaliana. Mol Plant 10, 1387–1399.

    Article  PubMed  CAS  Google Scholar 

  • David, R., Burgess, A., Parker, B., Li, J., Pulsford, K., Sibbritt, T., Preiss, T., and Searle, I.R. (2017). Transcriptome-wide mapping of RNA 5-methylcytosine in arabidopsis mRNAs and noncoding RNAs. Plant Cell 29, 445–460.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deery, D.M., and Jones, H.G. (2021). Field phenomics: will it enable crop improvement? Plant Phenomics 2021, 1–16.

    Article  Google Scholar 

  • Deng, Y., Zhai, K., Xie, Z., Yang, D., Zhu, X., Liu, J., Wang, X., Qin, P., Yang, Y., Zhang, G., et al. (2017). Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355, 962–965.

    Article  PubMed  CAS  Google Scholar 

  • Dong, W., Zhu, Y., Chang, H., Wang, C., Yang, J., Shi, J., Gao, J., Yang, W., Lan, L., Wang, Y., et al. (2020). An SHR-SCR module specifies legume cortical cell fate to enable nodulation. Nature 589, 586–590.

    Article  PubMed  Google Scholar 

  • Duan, H.C., Wei, L.H., Zhang, C., Wang, Y., Chen, L., Lu, Z., Chen, P.R., He, C., and Jia, G. (2017). ALKBH10B is an RNA N6-methyladenosine demethylase affecting arabidopsis floral transition. Plant Cell 29, 2995–3011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ermakova, M., Arrivault, S., Giuliani, R., Danila, F., Alonso-Cantabrana, H., Vlad, D., Ishihara, H., Feil, R., Guenther, M., Borghi, G.L., et al. (2020). Installation of C4 photosynthetic pathway enzymes in rice using a single construct. Plant Biotechnol J 19, 575–588.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallego-Bartolomé, J., Gardiner, J., Liu, W., Papikian, A., Ghoshal, B., Kuo, H.Y., Zhao, J.M.C., Segal, D.J., and Jacobsen, S.E. (2018). Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc Natl Acad Sci USA 115, E2125–E2134.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao, C. (2021). Genome engineering for crop improvement and future agriculture. Cell 184, 1621–1635.

    Article  PubMed  CAS  Google Scholar 

  • Guo, W., Liu, H., Wang, Y., Zhang, P., Li, D., Liu, T., Zhang, Q., Yang, L., Pu, L., Tian, J., et al. (2022). SMOC: a smart model for open chromatin region prediction in rice genomes. J Genet Genomics 49, 514–517.

    Article  PubMed  Google Scholar 

  • Guo, Z., Yang, W., Chang, Y., Ma, X., Tu, H., Xiong, F., Jiang, N., Feng, H., Huang, C., Yang, P., et al. (2018). Genome-wide association studies of image traits reveal genetic architecture of drought resistance in rice. Mol Plant 11, 789–805.

    Article  PubMed  CAS  Google Scholar 

  • Haynes, K.A., and Silver, P.A. (2011). Synthetic reversal of epigenetic silencing. J Biol Chem 286, 27176–27182.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoffman, G.E., Bendl, J., Girdhar, K., Schadt, E.E., and Roussos, P. (2019). Functional interpretation of genetic variants using deep learning predicts impact on chromatin accessibility and histone modification. Nucleic Acids Res 47, 10597–10611.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hou, Y., Sun, J., Wu, B., Gao, Y., Nie, H., Nie, Z., Quan, S., Wang, Y., Cao, X., and Li, S. (2021). CPSF30-L-mediated recognition of mRNA m6A modification controls alternative polyadenylation of nitrate signaling-related gene transcripts in Arabidopsis. Mol Plant 14, 688–699.

    Article  PubMed  CAS  Google Scholar 

  • Hu, J., Cai, J., Park, S.J., Lee, K., Li, Y., Chen, Y., Yun, J.Y., Xu, T., and Kang, H. (2021). N6-methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis. Plant J 106, 1759–1775.

    Article  PubMed  CAS  Google Scholar 

  • Huang, H., Weng, H., Zhou, K., Wu, T., Zhao, B.S., Sun, M., Chen, Z., Deng, X., Xiao, G., Auer, F., et al. (2019a). Histone H3 trimethylation at lysine 36 guides m6A RNA modification co-transcriptionally. Nature 567, 414–419.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang, S., Zhang, A., Jin, J.B., Zhao, B., Wang, T.J., Wu, Y., Wang, S., Liu, Y., Wang, J., Guo, P., et al. (2019b). Arabidopsis histone H3K4 demethylase JMJ17 functions in dehydration stress response. New Phytol 223, 1372–1387.

    Article  PubMed  CAS  Google Scholar 

  • Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., Lindahl, T., Pan, T., Yang, Y.G., et al. (2011). N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 7, 885–887.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson, L.M., Du, J., Hale, C.J., Bischof, S., Feng, S., Chodavarapu, R.K., Zhong, X., Marson, G., Pellegrini, M., Segal, D.J., et al. (2014). SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507, 124–128.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones, D.T., and Woods, D.R. (1986). Acetone-butanol fermentation revisited. Microbiol Rev 50, 484–524.

    Google Scholar 

  • Kan, R.L., Chen, J., and Sallam, T. (2021). Crosstalk between epitranscriptomic and epigenetic mechanisms in gene regulation. Trends Genet 38, 182–193.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawakatsu, T., Huang, S.S.C., Jupe, F., Sasaki, E., Schmitz, R.J., Urich, M. A., Castanon, R., Nery, J.R., Barragan, C., He, Y., et al. (2016). Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166, 492–505.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim, H.K., Yu, G., Park, J., Min, S., Lee, S., Yoon, S., and Kim, H.H. (2020). Predicting the efficiency of prime editing guide RNAs in human cells. Nat Biotechnol 39, 198–206.

    Article  PubMed  Google Scholar 

  • Li, H., Feng, H., Guo, C., Yang, S., Huang, W., Xiong, X., Liu, J., Chen, G., Liu, Q., Xiong, L., et al. (2020). High-throughput phenotyping accelerates the dissection of the dynamic genetic architecture of plant growth and yield improvement in rapeseed. Plant Biotechnol J 18, 2345–2353.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li, Q., Li, X., Tang, H., Jiang, B., Dou, Y., Gorospe, M., and Wang, W. (2017). NSUN2-mediated m5C methylation and METTL3/METTL14-mediated m6A methylation cooperatively enhance p21 translation. J Cell Biochem 118, 2587–2598.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li, Z., Fu, X., Wang, Y., Liu, R., and He, Y. (2018a). Polycomb-mediated gene silencing by the BAH-EMF1 complex in plants. Nat Genet 50, 1254–1261.

    Article  PubMed  CAS  Google Scholar 

  • Li, X., Harris, C.J., Zhong, Z., Chen, W., Liu, R., Jia, B., Wang, Z., Li, S., Jacobsen, S.E., and Du, J. (2018b). Mechanistic insights into plant SUVH family H3K9 methyltransferases and their binding to context-biased non-CG DNA methylation. Proc Natl Acad Sci USA 115, E8793–E8802.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liang, Z., Riaz, A., Chachar, S., Ding, Y., Du, H., and Gu, X. (2020). Epigenetic modifications of mRNA and DNA in plants. Mol Plant 13, 14–30.

    Article  PubMed  CAS  Google Scholar 

  • Liang, Z., Shen, L., Cui, X., Bao, S., Geng, Y., Yu, G., Liang, F., Xie, S., Lu, T., Gu, X., et al. (2018). DNA N-adenine methylation in Arabidopsis thaliana. Dev Cell 45, 406–416.e3.

    Article  PubMed  CAS  Google Scholar 

  • Liang, Z., Zhang, Q., Ji, C., Hu, G., Zhang, P., Wang, Y., Yang, L., and Gu, X. (2021). Reorganization of the 3D chromatin architecture of rice genomes during heat stress. BMC Biol 19, 53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, C., Cheng, Y.J., Wang, J.W., and Weigel, D. (2017). Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat Plants 3, 742–748.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Q., Fang, L., Yu, G., Wang, D., Xiao, C.L., and Wang, K. (2019a). Detection of DNA base modifications by deep recurrent neural network on Oxford Nanopore sequencing data. Nat Commun 10, 2449.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Liu, X.M., Zhou, J., Mao, Y., Ji, Q., and Qian, S.B. (2019b). Programmable RNA N6-methyladenosine editing by CRISPR-Cas9 conjugates. Nat Chem Biol 15, 865–871.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, Z.H., Tang, S., Hu, W., Lv, R., Mei, H., Yang, R., Song, X., Cao, X., and Wang, D. (2022). Precise editing of methylated cytosine in Arabidopsis thaliana using a human APOBEC3Bctd-Cas9 fusion. Sci China Life Sci 65, 219–222.

    Article  PubMed  CAS  Google Scholar 

  • Long, Y., Liu, Z., Jia, J., Mo, W., Fang, L., Lu, D., Liu, B., Zhang, H., Chen, W., and Zhai, J. (2021). FlsnRNA-seq: protoplasting-free full-length single-nucleus RNA profiling in plants. Genome Biol 22, 1–4.

    Article  Google Scholar 

  • Luo, C., Li, X., Zhang, Q., and Yan, J. (2019). Single gametophyte sequencing reveals that crossover events differ between sexes in maize. Nat Commun 10, 785.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma, K., Han, J., Zhang, Z., Li, H., Zhao, Y., Zhu, Q., Xie, Y., Liu, Y.G., and Chen, L. (2021). OsEDM2L mediates m6A of EAT1 transcript for proper alternative splicing and polyadenylation regulating rice tapetal degradation. J Integr Plant Biol 63, 1982–1994.

    Article  PubMed  CAS  Google Scholar 

  • Marand, A.P., Chen, Z., Gallavotti, A., and Schmitz, R.J. (2021). A cis-regulatory atlas in maize at single-cell resolution. Cell 184, 3041–3055.

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Pérez, M., Aparicio, F., López-Gresa, M.P., Bellés, J.M., Sánchez-Navarro, J.A., and Pallás, V. (2017). Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc Natl Acad Sci USA 114, 10755–10760.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller, T.E., Beneyton, T., Schwander, T., Diehl, C., Girault, M., McLean, R., Chotel, T., Claus, P., Cortina, N.S., Baret, J.C., et al. (2020). Light-powered CO2 fixation in a chloroplast mimic with natural and synthetic parts. Science 368, 649–654.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nuñez, J.K., Chen, J., Pommier, G.C., Cogan, J.Z., Replogle, J.M., Adriaens, C., Ramadoss, G.N., Shi, Q., Hung, K.L., Samelson, A.J., et al. (2021). Genome-wide programmable transcriptional memory by CRISPR-based epigenome editing. Cell 184, 2503–2519.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ochoa-Fernandez, R., Abel, N.B., Wieland, F.G., Schlegel, J., Koch, L.A., Miller, J.B., Engesser, R., Giuriani, G., Brandl, S.M., Timmer, J., et al. (2020). Optogenetic control of gene expression in plants in the presence of ambient white light. Nat Methods 17, 717–725.

    Article  PubMed  CAS  Google Scholar 

  • Papanatsiou, M., Petersen, J., Henderson, L., Wang, Y., Christie, J.M., and Blatt, M.R. (2019). Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science 363, 1456–1459.

    Article  PubMed  CAS  Google Scholar 

  • Pan, C., Sretenovic, S., and Qi, Y. (2021). CRISPR/dCas-mediated transcriptional and epigenetic regulation in plants. Curr Opin Plant Biol 60, 101980.

    Article  PubMed  CAS  Google Scholar 

  • Papikian, A., Liu, W., Gallego-Bartolomé, J., and Jacobsen, S.E. (2019). Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat Commun 10, 729.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Park, M., Keung, A.J., and Khalil, A.S. (2016). The epigenome: the next substrate for engineering. Genome Biol 17, 183.

    Article  PubMed  PubMed Central  Google Scholar 

  • Park, M., Patel, N., Keung, A.J., and Khalil, A.S. (2019). Engineering epigenetic regulation using synthetic read-write modules. Cell 176, 227–238.

    Article  PubMed  CAS  Google Scholar 

  • Park, S.Y., Peterson, F.C., Mosquna, A., Yao, J., Volkman, B.F., and Cutler, S.R. (2015). Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520, 545–548.

    Article  PubMed  Google Scholar 

  • Pratanwanich, P.N., Yao, F., Chen, Y., Koh, C.W.Q., Wan, Y.K., Hendra, C., Poon, P., Goh, Y.T., Yap, P.M.L., Chooi, J.Y., et al. (2021). Identification of differential RNA modifications from nanopore direct RNA sequencing with xPore. Nat Biotechnol 39, 1394–1402.

    Article  PubMed  CAS  Google Scholar 

  • Pu, L., and Sung, Z.R. (2015). PcG and trxG in plants—friends or foes. Trends Genet 31, 252–262.

    Article  PubMed  CAS  Google Scholar 

  • Qian, F., Zhao, Q.Y., Zhang, T.N., Li, Y.L., Su, Y.N., Li, L., Sui, J.H., Chen, S., and He, X.J. (2021). A histone H3K27me3 reader cooperates with a family of PHD finger-containing proteins to regulate flowering time in Arabidopsis. J Integr Plant Biol 63, 787–802.

    Article  PubMed  CAS  Google Scholar 

  • Qian, S., Lv, X., Scheid, R.N., Lu, L., Yang, Z., Chen, W., Liu, R., Boersma, M.D., Denu, J.M., Zhong, X., et al. (2018). Dual recognition of H3K4me3 and H3K27me3 by a plant histone reader SHL. Nat Commun 9, 2425.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin, H., Ou, L., Gao, J., Chen, L., Wang, J.W., Hao, P., and Li, X. (2022). DENA: training an authentic neural network model using Nanopore sequencing data of Arabidopsis transcripts for detection and quantification of N6-methyladenosine on RNA. Genome Biol 23, 25.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rakyan, V.K., Down, T.A., Balding, D.J., and Beck, S. (2011). Epigenomewide association studies for common human diseases. Nat Rev Genet 12, 529–541.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ribeiro, C., Hennen-Bierwagen, T.A., Myers, A.M., Cline, K., and Settles, A.M. (2020). Engineering 6-phosphogluconate dehydrogenase improves grain yield in heat-stressed maize. Proc Natl Acad Sci USA 117, 33177–33185.

    Article  PubMed Central  CAS  Google Scholar 

  • Růžička, K., Zhang, M., Campilho, A., Bodi, Z., Kashif, M., Saleh, M., Eeckhout, D., El-Showk, S., Li, H., Zhong, S., et al. (2017). Identification of factors required for m6A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI. New Phytol 215, 157–172.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen, H., Ontiveros, R.J., Owens, M.C., Liu, M.Y., Ghanty, U., Kohli, R. M., and Liu, K.F. (2021). TET-mediated 5-methylcytosine oxidation in tRNA promotes translation. J Biol Chem 296, 100087.

    Article  PubMed  CAS  Google Scholar 

  • Shen, L., Liang, Z., Gu, X., Chen, Y., Teo, Z.W.N., Hou, X., Cai, W.M., Dedon, P.C., Liu, L., and Yu, H. (2016). N6-methyladenosine RNA modification regulates shoot stem cell fate in Arabidopsis. Dev Cell 38, 186–200.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen, B.R., Wang, L.M., Lin, X.L., Yao, Z., Xu, H.W., Zhu, C.H., Teng, H. Y., Cui, L.L., Liu, E.E., Zhang, J.J., et al. (2019). Engineering a new chloroplastic photorespiratory bypass to increase photosynthetic efficiency and productivity in rice. Mol Plant 12, 199–214.

    Article  PubMed  CAS  Google Scholar 

  • Song, P., Yang, J., Wang, C., Lu, Q., Shi, L., Tayier, S., and Jia, G. (2021). Arabidopsis N6-methyladenosine reader CPSF30-L recognizes FUE signals to control polyadenylation site choice in liquid-like nuclear bodies. Mol Plant 14, 571–587.

    Article  PubMed  CAS  Google Scholar 

  • South, P.F., Cavanagh, A.P., Liu, H.W., and Ort, D.R. (2019). Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363, eaat9077.

    Article  PubMed  CAS  Google Scholar 

  • Sun, Y., Dong, L., Zhang, Y., Lin, D., Xu, W., Ke, C., Han, L., Deng, L., Li, G., Jackson, D., et al. (2020). 3D genome architecture coordinates trans and cis regulation of differentially expressed ear and tassel genes in maize. Genome Biol 21, 43.

    Article  Google Scholar 

  • Tang, S., Yang, C., Wang, D., Deng, X., Cao, X., and Song, X. (2022). Targeted DNA demethylation produces heritable epialleles in rice. Sci China Life Sci 65, 753–756.

    Article  PubMed  CAS  Google Scholar 

  • Tang, Y., Gao, C.C., Gao, Y., Yang, Y., Shi, B., Yu, J.L., Lyu, C., Sun, B.F., Wang, H.L., Xu, Y., et al. (2020). OsNSUN2-mediated 5-methylcytosine mRNA modification enhances rice adaptation to high temperature. Dev Cell 53, 272–286.

    Article  PubMed  CAS  Google Scholar 

  • Vamvaka, E., Farré, G., Molinos-Albert, L.M., Evans, A., Canela-Xandri, A., Twyman, R.M., Carrillo, J., Ordóñez, R.A., Shattock, R.J., O’Keefe, B.R., et al. (2018). Unexpected synergistic HIV neutralization by a triple microbicide produced in rice endosperm. Proc Natl Acad Sci USA 115, E7854.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vo Ngoc, L., Huang, C.Y., Cassidy, C.J., Medrano, C., and Kadonaga, J.T. (2020). Identification of the human DPR core promoter element using machine learning. Nature 585, 459–463.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, C., Wang, X., Zhang, L., Yue, Q., Liu, Q., Xu, Y.M., Gunatilaka, A. A.L., Wei, X., Xu, Y., and Molnár, I. (2020). Intrinsic and extrinsic programming of product chain length and release mode in fungal collaborating iterative polyketide synthases. J Am Chem Soc 142, 17093–17104.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, C., Yang, J., Song, P., Zhang, W., Lu, Q., Yu, Q., and Jia, G. (2022). FIONA1 is an RNA N6-methyladenosine methyltransferase affecting Arabidopsis photomorphogenesis and flowering. Genome Biol 23, 40.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, J., Nan, N., Li, N., Liu, Y., Wang, T.J., Hwang, I., Liu, B., and Xu, Z. Y. (2020a). A DNA methylation reader-chaperone regulatortranscription factor complex activates OsHKT1;5 expression during salinity stress. Plant Cell 32, 3535–3558.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, J., Yu, C., Zhang, S., Ye, J., Dai, H., Wang, H., Huang, J., Cao, X., Ma, J., Ma, H., et al. (2020b). Cell-type-dependent histone demethylase specificity promotes meiotic chromosome condensation in Arabidopsis. Nat Plants 6, 823–837.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y., Zhang, P., Guo, W., Liu, H., Li, X., Zhang, Q., Du, Z., Hu, G., Han, X., Pu, L., et al. (2021). A deep learning approach to automate whole-genome prediction of diverse epigenomic modifications in plants. New Phytol 232, 880–897.

    Article  PubMed  CAS  Google Scholar 

  • Weber, W., Schoenmakers, R., Keller, B., Gitzinger, M., Grau, T., Daoud-El Baba, M., Sander, P., and Fussenegger, M. (2008). A synthetic mammalian gene circuit reveals antituberculosis compounds. Proc Natl Acad Sci USA 105, 9994–9998.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wei, L.H., Song, P., Wang, Y., Lu, Z., Tang, Q., Yu, Q., Xiao, Y., Zhang, X., Duan, H.C., and Jia, G. (2018). The m6A reader ECT2 controls trichome morphology by affecting mRNA stability in Arabidopsis. Plant Cell 30, 968–985.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, D., Wu, D., Feng, H., Duan, L., Dai, G., Liu, X., Wang, K., Yang, P., Chen, G., Gay, A.P., et al. (2021a). A deep learning-integrated micro-CT image analysis pipeline for quantifying rice lodging resistance-related traits. Plant Commun 2, 100165.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, K., Wang, S., Song, W., Zhang, J., Wang, Y., Liu, Q., Yu, J., Ye, Y., Li, S., Chen, J., et al. (2020). Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367, eaaz2046.

    Article  PubMed  CAS  Google Scholar 

  • Wu, X., Feng, H., Wu, D., Yan, S., Zhang, P., Wang, W., Zhang, J., Ye, J., Dai, G., Fan, Y., et al. (2021b). Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance. Genome Biol 22, 185.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiang, N., Guo, C., Liu, J., Xu, H., Dixon, R., Yang, J., and Wang, Y.P. (2020). Using synthetic biology to overcome barriers to stable expression of nitrogenase in eukaryotic organelles. Proc Natl Acad Sci USA 117, 16537–16545.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiao, C.L., Zhu, S., He, M., Chen, D., Zhang, Q., Chen, Y., Yu, G., Liu, J., Xie, S.Q., Luo, F., et al. (2018). N6-Methyladenine DNA modification in the human genome. Mol Cell 71, 306–318.e7.

    Article  PubMed  CAS  Google Scholar 

  • Xu, T., Wu, X., Wong, C.E., Fan, S., Zhang, Y., Zhang, S., Liang, Z., Yu, H., and Shen, L. (2022). FIONA1-mediated m6A modification regulates the floral transition in Arabidopsis. Adv Sci 9, 2103628.

    Article  CAS  Google Scholar 

  • Yang, X., Yang, Y., Sun, B.F., Chen, Y.S., Xu, J.W., Lai, W.Y., Li, A., Wang, X., Bhattarai, D.P., Xiao, W., et al. (2017). 5-methylcytosine promotes mRNA export—NSUN2 as the methyltransferase and ALYREF as an m5C reader. Cell Res 27, 606–625.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang, L., Perrera, V., Saplaoura, E., Apelt, F., Bahin, M., Kramdi, A., Olas, J., Mueller-Roeber, B., Sokolowska, E., Zhang, W., et al. (2019). m5C methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr Biol 29, 2465–2476.e5.

    Article  PubMed  CAS  Google Scholar 

  • Yang, W., Feng, H., Zhang, X., Zhang, J., Doonan, J.H., Batchelor, W.D., Xiong, L., and Yan, J. (2020). Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives. Mol Plant 13, 187–214.

    Article  PubMed  CAS  Google Scholar 

  • Ye, G., Zhang, H., Chen, B., Nie, S., Liu, H., Gao, W., Wang, H., Gao, Y., and Gu, L. (2019). De novo genome assembly of the stress tolerant forest species Casuarina equisetifolia provides insight into secondary growth. Plant J 97, 779–794.

    Article  PubMed  CAS  Google Scholar 

  • Yu, Q., Liu, S., Yu, L., Xiao, Y., Zhang, S., Wang, X., Xu, Y., Yu, H., Li, Y., Yang, J., et al. (2021). RNA demethylation increases the yield and biomass of rice and potato plants in field trials. Nat Biotechnol 39, 1581–1588.

    Article  PubMed  CAS  Google Scholar 

  • Yu, X., Leiboff, S., Li, X., Guo, T., Ronning, N., Zhang, X., Muehlbauer, G. J., Timmermans, M.C.P., Schnable, P.S., Scanlon, M.J., et al. (2020). Genomic prediction of maize microphenotypes provides insights for optimizing selection and mining diversity. Plant Biotechnol J 18, 2456–2465.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan, D.H., Xing, J.F., Luan, M.W., Ji, K.K., Guo, J., Xie, S.Q., and Zhang, Y.M. (2020). DNA N6-methyladenine modification in wild and cultivated soybeans reveals different patterns in nucleus and cytoplasm. Front Genet 11, 736.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Q., Liang, Z., Cui, X., Ji, C., Li, Y., Zhang, P., Liu, J., Riaz, A., Yao, P., Liu, M., et al. (2018b). N6-Methyladenine DNA methylation in Japonica and Indica rice genomes and its association with gene expression, plant development, and stress responses. Mol Plant 11, 1492–1508.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, P., Wang, Y., Chachar, S., Tian, J., and Gu, X. (2020b). eRice: a refined epigenomic platform for japonica and indica rice. Plant Biotechnol J 18, 1642–1644.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, P., Wang, Y., and Gu, X. (2020a). RNA 5-Methylcytosine controls plant development and environmental adaptation. Trends Plant Sci 25, 954–958.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, P., Zhu, C., Geng, Y., Wang, Y., Yang, Y., Liu, Q., Guo, W., Chachar, S., Riaz, A., Yan, S., et al. (2021a). Rice and Arabidopsis homologs of yeast CHROMOSOME TRANSMISSION FIDELITY PROTEIN 4 commonly interact with Polycomb complexes but exert divergent regulatory functions. Plant Cell 33, 1417–1429.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, T.Q., Chen, Y., Liu, Y., Lin, W.H., and Wang, J.W. (2021b). Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root. Nat Commun 12, 2053.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang, T.Q., Xu, Z.G., Shang, G.D., and Wang, J.W. (2019b). A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol Plant 12, 648–660.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, L., Yu, H., Ma, B., Liu, G., Wang, J., Wang, J., Gao, R., Li, J., Liu, J., Xu, J., et al. (2017). A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun 8, 14789.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang, F., Zhang, Y.C., Liao, J.Y., Yu, Y., Zhou, Y.F., Feng, Y.Z., Yang, Y. W., Lei, M.Q., Bai, M., Wu, H., et al. (2019a). The subunit of RNA N6-methyladenosine methyltransferase OsFIP regulates early degeneration of microspores in rice. PLoS Genet 15, e1008120.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang, K., Zhuang, X., Dong, Z., Xu, K., Chen, X., Liu, F., and He, Z. (2021c). The dynamics of N6-methyladenine RNA modification in interactions between rice and plant viruses. Genome Biol 22, 189.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao, X., Li, J., Lian, B., Gu, H., Li, Y., and Qi, Y. (2018). Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nat Commun 9, 5056.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, L., Wang, S., Cao, Z., Ouyang, W., Zhang, Q., Xie, L., Zheng, R., Guo, M., Ma, M., Hu, Z., et al. (2019). Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation. Nat Commun 10, 3640.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, L., Xie, L., Zhang, Q., Ouyang, W., Deng, L., Guan, P., Ma, M., Li, Y., Zhang, Y., Xiao, Q., et al. (2020). Integrative analysis of reference epigenomes in 20 rice varieties. Nat Commun 11, 2658.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng, G., Dahl, J.A., Niu, Y., Fedorcsak, P., Huang, C.M., Li, C.J., Vågbø, C.B., Shi, Y., Wang, W.L., Song, S.H., et al. (2013). ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell 49, 18–29.

    Article  PubMed  CAS  Google Scholar 

  • Zheng, S., Hu, H., Ren, H., Yang, Z., Qiu, Q., Qi, W., Liu, X., Chen, X., Cui, X., Li, S., et al. (2019). The Arabidopsis H3K27me3 demethylase JUMONJI 13 is a temperature and photoperiod dependent flowering repressor. Nat Commun 10, 1303.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, Y., Wang, Y., Krause, K., Yang, T., Dongus, J.A., Zhang, Y., and Turck, F. (2018a). Telobox motifs recruit CLF/SWN-PRC2 for H3K27me3 deposition via TRB factors in Arabidopsis. Nat Genet 50, 638–644.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, C., Wang, C., Liu, H., Zhou, Q., Liu, Q., Guo, Y., Peng, T., Song, J., Zhang, J., Chen, L., et al. (2018b). Identification and analysis of adenine N6-methylation sites in the rice genome. Nat Plants 4, 554–563.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, H., Li, C., and Gao, C. (2020). Applications of CRISPR-Cas in agriculture and plant biotechnology. Nat Rev Mol Cell Biol 21, 661–677.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, Q., Yu, S., Zeng, D., Liu, H., Wang, H., Yang, Z., Xie, X., Shen, R., Tan, J., Li, H., et al. (2017). Development of “purple endosperm rice” by engineering anthocyanin biosynthesis in the endosperm with a high-efficiency transgene stacking system. Mol Plant 10, 918–929.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, Q., Zeng, D., Yu, S., Cui, C., Li, J., Li, H., Chen, J., Zhang, R., Zhao, X., Chen, L., et al. (2018a). From Golden Rice to aSTARice: bioengineering astaxanthin biosynthesis in rice endosperm. Mol Plant 11, 1440–1448.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, S., Beaulaurier, J., Deikus, G., Wu, T.P., Strahl, M., Hao, Z., Luo, G., Gregory, J.A., Chess, A., He, C., et al. (2018b). Mapping and characterizing N6-methyladenine in eukaryotic genomes using single-molecule real-time sequencing. Genome Res 28, 1067–1078.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2021YFF1000301), the National Natural Science Foundation of China (32130080, 31871606, 32101786), the Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ZDRW202004), the Fundamental Research Funds for Central Non-Profit of Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (Y2020YJ09), Hainan Yazhou Bay Seed Laboratory (B21HJ0223), and Beijing Natural Science Foundation (6222055).

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  1. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Liwen Yang, Pingxian Zhang, Yifan Wang, Guihua Hu, Weijun Guo, Xiaofeng Gu & Li Pu

  2. College of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Pingxian Zhang

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  1. Liwen Yang
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Correspondence to Xiaofeng Gu or Li Pu.

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Yang, L., Zhang, P., Wang, Y. et al. Plant synthetic epigenomic engineering for crop improvement. Sci. China Life Sci. 65, 2191–2204 (2022). https://doi.org/10.1007/s11427-021-2131-6

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