Similar articles

Abstract: plant breeding is well recognized as one of the most important means to meet food security challenges caused by the ever-increasing world population. During the past three decades, plant breeding has been empowered by both new knowledge on trait development and regulation (e.g., functional genomics) and new technologies (e.g., biotechnologies and phenomics). gene editing, particularly by clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas) and its variants, has become a powerful technology in plant research and may become a game-changer in plant breeding. Traits are conferred by coding and non-coding genes. From this perspective, we propose different editing strategies for these two types of genes. The activity of an encoded enzyme and its quantity are regulated at transcriptional and post-transcriptional, as well as translational and post-translational, levels. Different strategies are proposed to intervene to generate gene functional variations and consequently phenotype changes. For non-coding genes, trait modification could be achieved by regulating transcription of their own or target genes via gene editing. Also included is a scheme of protoplast editing to make gene editing more applicable in plant breeding. In summary, this review provides breeders with a host of options to translate gene biology into practical breeding strategies, i.e., to use gene editing as a mechanism to commercialize gene biology in plant breeding.

基因编辑:将基因生物学用于植物育种的工具

[1]Al-Zeer MA, Dutkiewicz M, von Hacht A, et al., 2019. Alternatively spliced variants of the 5'-UTR of the ARPC2 mRNA regulate translation by an internal ribosome entry site (IRES) harboring a guanine-quadruplex motif. RNA Biol, 16(11):1622-1632.

[2]Apitz J, Nishimura K, Schmied J, et al., 2016. Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol, 170(4):2040-2051.

[3]Beale SI, 1999. Enzymes of chlorophyll biosynthesis. Photosynth Res, 60(1):43-73.

[4]Butelli E, Licciardello C, Zhang Y, et al., 2012. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell, 24(3):1242-1255.

[5]Cermak T, Doyle EL, Christian M, et al., 2011. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res, 39(12):e82.

[6]Čermák T, Baltes NJ, Čegan R, et al., 2015. High-frequency, precise modification of the tomato genome. Genome Biol, 16:232.

[7]Chavez A, Scheiman J, Vora S, et al., 2015. Highly efficient Cas9-mediated transcriptional programming. Nat Methods, 12(4):326-328.

[8]Chen KL, Wang YP, Zhang R, et al., 2019. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol, 70:667-697.

[9]Czarnecki O, Hedtke B, Melzer M, et al., 2011. An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell, 23(12):4476-4491.

[10]Deng X, Cao XF, 2017. Roles of pre-mRNA splicing and polyadenylation in plant development. Curr Opin Plant Biol, 35:45-53.

[11]Deribe YL, Pawson T, Dikic I, 2010. Post-translational modifications in signal integration. Nat Struct Mol Biol, 17(6):666-672.

[12]Duan GY, Walther D, 2015. The roles of post-translational modifications in the context of protein interaction networks. PLoS Comput Biol, 11(2):e1004049.

[13]Endo A, Masafumi M, Kaya H, et al., 2016. Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci Rep, 6:38169.

[14]Eş I, Gavahian M, Marti-Quijal FJ, et al., 2019. The application of the CRISPR-Cas9 genome editing machinery in food and agricultural science: current status, future perspectives, and associated challenges. Biotechnol Adv, 37(3):410-421.

[15]Espley RV, Brendolise C, Chagné D, et al., 2009. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell, 21(1):168-183.

[16]Filichkin S, Priest HD, Megraw M, et al., 2015. Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress. Curr Opin Plant Biol, 24:125-135.

[17]Fossi M, Amundson K, Kuppu S, et al., 2019. Regeneration of Solanum tuberosum plants from protoplasts induces widespread genome instability. Plant Physiol, 180:78-86.

[18]Goslings D, Meskauskiene R, Kim C, et al., 2004. Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J, 40(6):957-967.

[19]Hickey LT, Hafeez AN, Robinson H, et al., 2019. Breeding crops to feed 10 billion. Nat Biotechnol, 37(2):744-754.

[20]Hu JH, Miller SM, Geurts MH, et al., 2018. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature, 556(7699):57-63.

[21]Hua K, Tao XP, Zhu JK, 2018. Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnol J, 17(2):499-504.

[22]Hua K, Zhang JS, Botella JR, et al., 2019. Perspectives on the application of genome-editing technologies in crop breeding. Mol Plant, 12(8):1047-1059.

[23]Huber SC, Hardin SC, 2004. Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels. Curr Opin Plant Biol, 7(3):318-322.

[24]Hunt AG, 2014. The Arabidopsis polyadenylation factor subunit CPSF30 as conceptual link between mRNA polyadenylation and cellular signaling. Curr Opin Plant Biol, 21: 128-132.

[25]Jia HG, Zhang YZ, Orbović V, et al., 2017. Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J, 15(7):817-823.

[26]Jiang M, Liu YH, Li RQ, et al., 2019. A suppressor mutation partially reverts the xantha trait via lowered methylation in the promoter of genomes uncoupled 4 in Rice. Front Plant Sci, 10:1003.

[27]Jiao YQ, Wang YH, Xue DW, et al., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet, 42(6):541-544.

[28]Jorrín-Novo JV, Maldonado AM, Echevarria-Zomeno S, et al., 2009. Plant proteomics update (2007–2008):second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfill MIAPE standards, increase plant proteome coverage and expand biological knowledge. J Proteomics, 72(3):285-314.

[29]Kausch AP, Nelson-Vasilchik K, Hague J, et al., 2019. Edit at will: genotype independent plant transformation in the era of advanced genomics and genome editing. Plant Sci, 281: 186-205.

[30]Kauss D, Bischof S, Steiner S, et al., 2012. FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg⁺⁺-branch of this pathway. FEBS Lett, 586(3):211-216.

[31]Kim S, Kim D, Cho SW, et al., 2014. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res, 24(6):1012-1019.

[32]Kleinstiver BP, Tsai SQ, Prew MS, et al., 2016. Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat Biotechnol, 34(8):869-874.

[33]Leppek K, Das R, Barna M, 2018. Functional 5' UTR mRNA structures in eukaryotic translation regulation and how to find them. Nat Rev Mol Cell, 19(3):158-174.

[34]Li AX, Jia SG, Yobi A, et al., 2018. Editing of an alpha-kafirin gene family increases, digestibility and protein quality in sorghum. Plant Physiol, 177(4):1425-1438.

[35]Li JF, Norville JE, Aach J, et al., 2013. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol, 31(8):688-691.

[36]Li T, Liu B, Spalding MH, et al., 2012. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol, 30(5):390-392.

[37]Li T, Liu B, Chen CY, et al., 2016. TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genomic, 43(5):297-305.

[38]Li WT, Zhu ZW, Chern M, et al., 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell, 170(1):114-126.

[39]Li YB, Fan CC, Xing YZ, et al., 2011. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet, 43(12):1266-1269.

[40]Liang XQ, Potter J, Kumar S, et al., 2015. Rapid and highly efficient mammalian cell engineering via Cas9 protein transfection. J Biotechnol, 208:44-53.

[41]Lin CS, Hsu CT, Yang LH, et al., 2018. Application of protoplast technology to CRISPR/Cas9 mutagenesis: from single-cell mutation detection to mutant plant regeneration. Plant Biotechnol J, 16(7):1295-1310.

[42]Lin S, Zhao YY, Zhu YF, et al., 2016. An effective and inducible system of TAL effector-mediated transcriptional repression in Arabidopsis. Mol Plant, 9(11):1546-1549.

[43]Liu SM, Jiang J, Liu Y, et al., 2019. Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. Rice Sci, 26(2):88-97.

[44]Lloyd A, Plaisier CL, Carroll D, et al., 2005. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci USA, 102(6):2232-2237.

[45]Mahfouz MM, Li LX, Shamimuzzaman M, et al., 2011. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci USA, 108(6):2623-2628.

[46]Mao YF, Botella JR, Liu YG, et al., 2019. Gene editing in plants: progress and challenges. Natl Sci Rev, 6(3):421-437.

[47]Meskauskiene R, Nater M, Goslings D, et al., 2001. FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA, 98(22):12826-12831.

[48]Minkenberg B, Xie KB, Yang YN, 2017. Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinase genes. Plant J, 89(3):636-648.

[49]Molla KA, Yang YN, 2019. CRISPR/Cas-mediated base editing: technical considerations and practical applications. Trends Biotechnol, 37(10):1121-1142.

[50]Morsy M, Gouthu S, Orchard S, et al., 2008. Charting plant interactomes: possibilities and challenges. Trends Plant Sci, 13(4):183-191.

[51]Nekrasov V, Staskawicz B, Weigel D, et al., 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol, 31(8):691-693.

[52]Nishimasu H, Shi X, Ishiguro S, et al., 2018. Engineered CRISPR-Cas9 nuclease with expanded targeting space. Science, 361(6408):1259-1262.

[53]Oikawa T, Maeda H, Oguchi T, et al., 2015. The birth of a black rice gene and its local spread by introgression. Plant Cell, 27(9):2401-2414.

[54]Pandiarajan R, Grover A, 2018. In vivo promoter engineering in plants: are we ready? Plant Sci, 277:132-138.

[55]Piatek A, Ali Z, Baazim H, et al., 2015. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J, 13(4):578-589.

[56]Pierre-Jerome E, Drapek C, Benfey PN, 2018. Regulation of division and differentiation of plant stem cells. Annu Rev Cell Dev Biol, 34(1):289-310.

[57]Qin ZR, Wu JJ, Geng SF, et al., 2017. Regulation of FT splicing by an endogenous cue in temperate grasses. Nat Commun, 8:14320.

[58]Reddy ASN, Marquez Y, Kalyna M, et al., 2013. Complexity of the alternative splicing landscape in plants. Plant Cell, 25(10):3657-3683.

[59]Ren B, Liu L, Li SF, et al., 2019. Cas9-NG greatly expands the targeting scope of the genome-editing toolkit by recognizing NG and other atypical PAMs in rice. Mol Plant, 12(7):1015-1026.

[60]Richter AS, Hochheuser C, Fufezan C, et al., 2016. Phosphorylation of GENOMES UNCOUPLED 4 alters stimulation of Mg chelatase activity in angiosperms. Plant Physiol, 172(3):1578-1595.

[61]Rodriguez-Leal D, Lemmon ZH, Man J, et al., 2017. Engineering quantitative trait variation for crop improvement by genome editing. Cell, 171(2):470-480.E8.

[62]Shan QW, Wang YP, Li J, et al., 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol, 31(8):686-688.

[63]Shan QW, Wang YP, Li J, et al., 2014. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc, 9(10):2395-2410.

[64]Shan QW, Zhang Y, Chen KL, et al., 2015. Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J, 13(6):791-800.

[65]Shi JR, Gao HR, Wang HY, et al., 2017. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J, 15(2):207-216.

[66]Shimatani Z, Kashojiya S, Takayama M, et al., 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol, 35(5):441-443.

[67]Soyk S, Müller NA, Park SJ, et al., 2017. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet, 49(1):162-168.

[68]Sun YW, Jiao GA, Liu ZP, et al., 2017. Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci, 8:298.

[69]Takahashi K, Yamanaka S, 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126(4):663-676.

[70]Takenaka M, Zehrmann A, Verbitskiy D, et al., 2013. RNA editing in plants and its evolution. Annu Rev Genet, 47: 335-352.

[71]Tang L, Mao BG, Li YK, et al., 2017. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep, 7:14438.

[72]Tang X, Lowder LG, Zhang T, et al., 2017. A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants, 3(3):17018.

[73]von Arnim AG, Jia QD, Vaughn JN, 2014. Regulation of plant translation by upstream open reading frames. Plant Sci, 214:1-12.

[74]Wang B, Smith SM, Li JY, 2018. Genetic regulation of shoot architecture. Annu Rev Plant Biol, 69(1):437-468.

[75]Wang FJ, Wang CL, Liu PQ, et al., 2016. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE, 11(4):e0154027.

[76]Wang J, Zhou L, Shi H, et al., 2018. A single transcription factor promotes both yield and immunity in rice. Science, 361(6406):1026-1028.

[77]Wang MG, Mao YF, Lu YM, et al., 2017. Multiplex gene editing in rice using the CRISPR-Cpf1 system. Mol Plant, 10(7):1011-1013.

[78]Wang SK, Wu K, Yuan QB, et al., 2012. Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet, 44(8):950-954.

[79]Wang SK, Li S, Liu Q, et al., 2015. The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet, 47(8):949-954.

[80]Wang YP, Cheng X, Shan QW, et al., 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 32(9):947-951.

[81]Woo JW, Kim J, Kwon SI, et al., 2015. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol, 33(11):1162-1164.

[82]Wu L, Zhou HY, Zhang QQ, et al., 2010. DNA methylation mediated by a microRNA pathway. Mol Cell, 38(3):465-475.

[83]Xie KB, Minkenberg B, Yang YN, 2015. Boosting CRISPR/ Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA, 112(11):3570-3575.

[84]Xu CJ, Liu Y, Li YB, et al., 2015. Differential expression of GS5 regulates grain size in rice. J Exp Bot, 66(9):2611-2623.

[85]Xu RF, Yang YC, Qing RY, et al., 2016. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genomics, 43(8):529-532.

[86]Xue CX, Zhang HW, Lin QP, et al., 2018. Manipulating mRNA splicing by base editing in plants. Sci China Life Sci, 61(11):1293-1300.

[87]Yang RX, Li PC, Mei HL, et al., 2019. Fine-tuning of miR528 accumulation modulates flowering time in rice. Mol Plant, 12(8):1103-1113.

[88]Ytterberg AJ, Jensen ON, 2010. Modification-specific proteomics in plant biology. J Proteomics, 73(11):2249-2266.

[89]Zaidi SSA, Mukhtar MS, Mansoor S, 2018. Genome editing: targeting susceptibility genes for plant disease resistance. Trends Biotechnol, 36(9):898-906.

[90]Zetsche B, Gootenberg JS, Abudayyeh OO, et al., 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163(3):759-771.

[91]Zhang H, Zhang JS, Lang ZB, et al., 2017. Genome editing-principles and applications for functional genomics research and crop improvement. Plant Sci, 36(4):291-309.

[92]Zhang HW, Si XM, Ji X, et al., 2018. Genome editing of upstream open reading frames enables translational control in plants. Nat Biotechnol, 36(9):894-898.

[93]Zhang JS, Zhang H, Botella JR, et al., 2018. Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol, 60(5):369-375.

[94]Zhang L, Yu H, Ma B, et al., 2017. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun, 8:14789.

[95]Zhang M, Zhang FL, Fang Y, et al., 2015. The non-canonical tetratricopeptide repeat (TPR) domain of fluorescent (FLU) mediates complex formation with glutamyl-tRNA reductase. J Biol Chem, 290(28):17559-17565.

[96]Zhang YX, Malzahn AA, Sretenovic S, et al., 2019. The emerging and uncultivated potential of CRSIPR technology in plant science. Nat Plants, 5(8):778-794.

[97]Zhou JP, Deng KJ, Cheng Y, et al., 2017. CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci, 8:1598.

[98]Zhou X, Deng L, Wang Q, et al., 2018. Breeding of waxy rice by genome editing. Mol Plant Breed, 16(17):5608-5615 (in Chinese).

[99]https://doi.org/10.13271/j.mpb.016.005608

[100]Zimny T, Sowa S, Tyczewska A, et al., 2019. Certain new plant breeding techniques and their marketability in the context of EU GMO legislation—recent developments. New Biotechnol, 51:49-56.

[101]Zong Y, Song QN, Li C, et al., 2018. Efficient C-to-T base editing in plants using a fusion of nCas9 and human APOBEC3A. Nat Biotechnol, 36(10):950-953.