CRISPR/Cas9-mediated disruption of TaNP1 genes results in complete male sterility in bread wheat

Journal of Genetics and Genomics - Tập 47 - Trang 263-272 - 2020
Jian Li1, Zheng Wang1, Guangming He2, Ligeng Ma3, Xing Wang Deng1,2
1Peking University Institute of Advanced Agricultural Sciences, Weifang, Shandong, 261325, China
2State Key Laboratory of Protein and Plant Gene Research, Peking-Tsinghua Center for Life Sciences, School of Advanced Agriculture Sciences and School of Life Sciences, Peking University, Beijing, 100871, China
3College of Life Sciences, Capital Normal University, Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, Beijing 100048, China

Tài liệu tham khảo

Adugna, 2004, A comparison of cytoplasmic and chemically-induced male sterility systems for hybrid seed production in wheat (Triticum aestivum L.), Euphytica, 135, 297, 10.1023/B:EUPH.0000013320.28114.c6 Arndell, 2019, gRNA validation for wheat genome editing with the CRISPR-Cas9 system, BMC Biotechnol., 19, 71, 10.1186/s12896-019-0565-z Bhowmik, 2018, Targeted mutagenesis in wheat microspores using CRISPR/Cas9, Sci. Rep., 8, 6502, 10.1038/s41598-018-24690-8 Burton, 2004, The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes, Plant Physiol., 134, 224, 10.1104/pp.103.032904 Chang, 2016, Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene, Proc. Natl. Acad. Sci. U. S. A., 113, 14145, 10.1073/pnas.1613792113 Chen, 2013, Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system, Cell, 155, 1479, 10.1016/j.cell.2013.12.001 Chen, 2019, The genomics of Oryza species provides insights into rice domestication and heterosis, Annu. Rev. Plant Biol., 70, 639, 10.1146/annurev-arplant-050718-100320 Chen, 2005, Problems of the hybrid with Chongqing thermo-photo-sensitive male sterility wheat C49S in the plain of Jiang Han, Mailei Zuowu Xuebao, 25, 147 Chen, 2017, IRREGULAR POLLEN EXINE1 is a novel factor in anther cuticle and pollen exine formation, Plant Physiol., 173, 307, 10.1104/pp.16.00629 Christensen, 1996, Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants, Transgenic Res., 5, 213, 10.1007/BF01969712 Cigan, 2017, Targeted mutagenesis of a conserved anther-expressed P450 gene confers male sterility in monocots, Plant Biotechnol., 15, 379, 10.1111/pbi.12633 Dang, 2015, Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency, Genome Biol., 16, 280, 10.1186/s13059-015-0846-3 De Vries, 1971, Flowering biology of wheat, particularly in view of hybrid seed production - a review, Euphytica, 20, 152, 10.1007/BF00056076 Duvick, 2001, Biotechnology in the 1930s: the development of hybrid maize, Nat. Rev. Genet., 2, 69, 10.1038/35047587 Driscoll, 1975, Cytogenetic analysis of two chromosomal male-sterility mutants in hexaploid wheat, Aust. J. Biol. Sci., 28, 413, 10.1071/BI9750413 Driscoll, 1977, Registration of Cornerstone male-sterile wheat germplasm, Crop Sci., 17, 190, 10.2135/cropsci1977.0011183X001700010059x Feng, 2013, Efficient genome editing in plants using a CRISPR/Cas system, Cell Res., 23, 1229, 10.1038/cr.2013.114 Feng, 2016, Efficient targeted genome modification in maize using CRISPR/Cas9 system, J. Genet. Genomics, 43, 37, 10.1016/j.jgg.2015.10.002 Fossati, 1970, A male sterile mutant in Triticum aestivum, Wheat Inform. Serv., 30, 8 Franckowiak, 1976, A proposal for hybrid wheat utilizing Aegilops squarrosa L. cytoplasm, Crop Sci., 16, 725, 10.2135/cropsci1976.0011183X001600050033x Geyer, 2018, Exploring the genetics of fertility restoration controlled by Rf1 in common wheat (Triticum aestivum L.) using high-density linkage maps, Mol. Genet. Genomics, 293, 451, 10.1007/s00438-017-1396-z Hoagland, 1953, Some histological and morphological effects of maleic hydrazide on spring wheat, Agron. J., 45, 468, 10.2134/agronj1953.00021962004500100003x Howells, 2018, Efficient generation of stable, heritable gene edits in wheat using CRISPR/Cas9, BMC Plant Biol., 18, 215, 10.1186/s12870-018-1433-z Kihara, 1951, Substitution of nucleus and its effects on genome manifestations, Cytologia, 16, 177, 10.1508/cytologia.16.177 Klindworth, 2002, Chromosomal location of genetic male sterility genes in four mutants of hexaploid wheat, Crop Sci., 42, 1447, 10.2135/cropsci2002.1447 Lawrenson, 2015, Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease, Genome Biol., 16, 258, 10.1186/s13059-015-0826-7 Li, 2018, Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion, Genome Biol., 19, 59, 10.1186/s13059-018-1443-z Li, 2019, CRISPR/Cas9-Based genome editing and its applications for functional genomic analyses in plants, Small Methods, 3, 1800473, 10.1002/smtd.201800473 Liu, 1997, A preliminary study on the effects of Aegilops crassa 6x cytoplasm on the characters of common wheat, J. Genet. Genomics, 24, 241 Liu, 2002, Studies on fertility genetic characters in D2-type CMS lines of common wheat, J. Genet. Genomics, 29, 638 Liu, 2017, Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning, Plant J., 91, 263, 10.1111/tpj.13561 Longin, 2012, Hybrid breeding in autogamous cereals, Theor. Appl. Genet., 125, 1087, 10.1007/s00122-012-1967-7 Murai, 1993, Photoperiod-sensitive cytoplasmic male sterility in wheat with Aegilops crassa cytoplasm, Euphytica, 67, 41, 10.1007/BF00022723 Nekrasov, 2013, Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease, Nat. Biotechnol., 31, 691, 10.1038/nbt.2655 Pallotta, 2019, Wheat ms5 male-sterility is induced by recessive homoeologous A and D genome non-specific lipid transfer protein, Plant J., 99, 673, 10.1111/tpj.14350 Perez-Prat, 2002, Hybrid seed production and the challenge of propagating male-sterile plants, Trends Plant Sci., 7, 199, 10.1016/S1360-1385(02)02252-5 Petersen, 2006, Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum), Mol. Phylogenet. Evol., 39, 70, 10.1016/j.ympev.2006.01.023 Pickett, 1993, Hybrid wheat: results and problems, Adv. Plant Breeding Suppl., 15, 1 Pugsleay, 1959, Genic male sterility in wheat, Aust. Plant Breed Genet. Newsletter, 14, 10 Sasakuma, 1978, EMS-induced male-sterile mutants in euplasmic and alloplasmic common wheat, Crop Sci., 18, 850, 10.2135/cropsci1978.0011183X001800050043x Shan, 2013, Targeted genome modification of crop plants using a CRISPR-Cas system, Nat. Biotechnol., 31, 686, 10.1038/nbt.2650 Shan, 2014, Genome editing in rice and wheat using the CRISPR/Cas system, Nat. Protoc., 9, 2395, 10.1038/nprot.2014.157 Singh, 2010, Perspective of hybrid wheat research: a review, Indian J. Agr. Sci., 80, 1013 Singh, 2018, Concurrent modifications in the three homeologs of Ms45 gene with CRISPR-Cas9 lead to rapid generation of male sterile bread wheat (Triticum aestivum L.), Plant Mol. Biol., 97, 371, 10.1007/s11103-018-0749-2 Singh, 2017, MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility, PLoS One, 12 Tsunewaki, 1993, Genome-plasmon interaction in wheat, Jpn. J. Genet., 68, 1, 10.1266/jjg.68.1 Tucker, 2017, Molecular identification of the wheat male fertility gene Ms1 and its prospects for hybrid breeding, Nat. Commun., 8, 869, 10.1038/s41467-017-00945-2 Vandesompele, 2002, Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol., 3, 10.1186/gb-2002-3-7-research0034 Vats, 2019, Genome editing in plants: exploration of technological advancements and challenges, Cells, 8, 1386, 10.3390/cells8111386 Voytas, 2014, Precision genome engineering and agriculture: opportunities and regulatory challenges, PLoS Biol., 12, e1001877, 10.1371/journal.pbio.1001877 Wang, 2014, Simultaneous editing of three homoeoalleles in hexaploid bread confers heritable resistance to powdery mildew, Nat. Biotechnol., 32, 947, 10.1038/nbt.2969 Wang, 2017, Poaceae-specific MS1 encodes a phospholipid-binding protein for male fertility in bread wheat, Proc. Natl. Acad. Sci. U. S. A., 114, 12614, 10.1073/pnas.1715570114 Whitford, 2013, Hybrid breeding in wheat: technologies to improve hybrid wheat seed production, J. Exp. Bot., 64, 5411, 10.1093/jxb/ert333 Wilson, 1962, Male sterility interaction of the Triticum aestivum nucleus and Triticum timopheevii cytoplasm, Wheat Inf. Serv., 14, 29 Wu, 2016, Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops, Plant Biotechnol. J., 14, 1046, 10.1111/pbi.12477 Xie, 2015, Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system, Proc. Natl. Acad. Sci. U. S. A., 112, 3570, 10.1073/pnas.1420294112 Yao, 2006, Low copy number gene transfer and stable expression in a commercial wheat cultivar via particle bombardment, J. Exp. Bot., 57, 3737, 10.1093/jxb/erl145 Zhang, 2018, Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor, Plant Biotechnol. J., 16, 459, 10.1111/pbi.12786 Zhang, 2005 Zhang, 2018, Targeted mutagenesis using the Agrobacterium tumefaciens-mediated CRISPR-Cas9 system in common wheat, BMC Plant Biol., 18, 302, 10.1186/s12870-018-1496-x Zhang, 2017, Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat, Plant J., 91, 714, 10.1111/tpj.13599 Zhang, 2019, Development of an Agrobacterium-delivered CRISPR/Cas9 system for wheat genome editing, Plant Biotechnol., 17, 1623, 10.1111/pbi.13088 Zhao, 2013, Research and application of hybrid wheat in China, Eng. Sci., 11, 19 Zhou, 2008, A new male sterile mutant LZ in wheat (Triticum aestivum L.), Euphytica, 159, 403, 10.1007/s10681-007-9551-y