Abstract
Key message
Integrating CRISPR/Cas9 genome editing into modern breeding programs for crop improvement in cereals.
Abstract
Global climate trends in many agricultural regions have been rapidly changing over the past decades, and major advances in global food systems are required to ensure food security in the face of these emerging challenges. With increasing climate instability due to warmer temperatures and rising CO2 levels, the productivity of global agriculture will continue to be negatively impacted. To combat these growing concerns, creative approaches will be required, utilising all the tools available to produce more robust and tolerant crops with increased quality and yields under more extreme conditions. The integration of genome editing and transgenics into current breeding strategies is one promising solution to accelerate genetic gains through targeted genetic modifications, producing crops that can overcome the shifting climate realities. This review focuses on how revolutionary genome editing tools can be directly implemented into breeding programs for cereal crop improvement to rapidly counteract many of the issues affecting agriculture production in the years to come.


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References
Abe J, Morita S (1994) Growth direction of nodal roots in rice: its variation and contribution to root system formation. Plant Soil 165:333–337. https://doi.org/10.1007/BF00008078
Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274. https://doi.org/10.1007/s00299-006-0204-8
Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627. https://doi.org/10.1038/nrg3291
Araki H, Morita S, Tatsumi J, Iijima M (2002) Physiol-morphological analysis on axile root growth in upland rice. Plant Prod Sci 5:286–293. https://doi.org/10.1626/pps.5.286
Asseng S et al (2015) Rising temperatures reduce global wheat production. Nat Clim Change 5:143–147. https://doi.org/10.1038/Nclimate2470
Atlin GN, Cairns JE, Das B (2017) Rapid breeding and varietal replacement are critical to adaptation of cropping systems in the developing world to climate change. Glob Food Secur Agr 12:31–37. https://doi.org/10.1016/j.gfs.2017.01.008
Avila EM, Gisby MF, Day A (2016) Seamless editing of the chloroplast genome in plants. BMC Plant Biol 16:1–13
Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods. https://doi.org/10.1186/1746-4811-9-39
Bock R (2015) Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Ann Rev Plant Biol 66:211–241
Borrelli et al (2020) The enhancement of plant disease resistance using CRISPR/Cas9 technology. Front Plant Sci 9:1245. https://doi.org/10.3389/fpls.2018.01245
Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52. https://doi.org/10.1016/j.biotechadv.2014.12.006
Bouteillé M, Rolland G, Balsera C, Loudet O, Muller B (2012) Disentangling the intertwined genetic bases of root and shoot growth in arabidopsis. PLoS ONE 7:e32319. https://doi.org/10.1371/journal.pone.0032319
Casacuberta JM, Nogue F, du Jardin P (2017) GMO risk assessment in the EU: interplay between science, policy and politics towards a new regulatory framework for gm crops in the European union: scientific, ethical, social and legal issues and the challenges ahead. Wageningen Academic Publisher, Wageningen. pp 141–154 doi:https://doi.org/10.3920/978-90-8686-845-2_9
Challinor AJ, Koehler AK, Ramirez-Villegas J, Whitfield S, Das B (2016) Current warming will reduce yields unless maize breeding and seed systems adapt immediately. Nat Clim Change 6:954–958. https://doi.org/10.1038/Nclimate3061
Chang ZY et al (2017) Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene (vol 113, pg 14145, 2016). P Natl Acad Sci USA 114:E107–E107. https://doi.org/10.1073/pnas.1619974114
Char SN, Wei J, Mu Q, Li X, Zhang ZJ, Yu J, Yang B (2020) An Agrobacterium-delivered CRISPR/Cas9 system for targeted mutagenesis in sorghum. Plant Biotechnol J 18:319–321. https://doi.org/10.1111/pbi.13229
Chavez A et al (2016) Comparison of Cas9 activators in multiple species. Nat Methods 13:563–567. https://doi.org/10.1038/nmeth.3871
Chen RR, Xu QL, Liu Y, Zhang JJ, Ren DT, Wang GY, Liu YJ (2018) Generation of transgene-free maize male sterile lines using the CRISPR/Cas9 system. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01180
Chen KL, Wang YP, Zhang R, Zhang HW, Gao CX (2019) CRISPR/cas genome editing and precision plant breeding in agriculture. Ann Rev Plant Biol 70:667–697. https://doi.org/10.1146/annurev-arplant-050718-100049
Christian M et al (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757-U476. https://doi.org/10.1534/genetics.110.120717
Cong L et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823. https://doi.org/10.1126/science.1231143
Cui M, Zhang W, Zhang Q, Xu Z, Zhu Z, Duan F, Wu R (2011) Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiol Biochem 49:1384–1391. https://doi.org/10.1016/j.plaphy.2011.09.012
Cui Y, Zhu M, Xu Z, Xu Q (2019) Assessment of the effect of ten heading time genes on reproductive transition and yield components in rice using a CRISPR/Cas9 system. Int J Plant Breed Res 132:1887–1896. https://doi.org/10.1007/s00122-019-03324-1
Custers R, Casacuberta JM, Eriksson D, Sagi L, Schiemann J (2019) Genetic alterations that do or do not occur naturally; consequences for genome edited organisms in the context of regulatory oversight. Front Bioeng Biotech. https://doi.org/10.3389/fbioe.2018.00213
Dai A (2011) Drought under global warming: a review. Wiley Interdisciplinary Reviews: Climate Change 2:45–65
Dawson IK, Russell J, Powell W, Steffenson B, Thomas WTB, Waugh R (2015) Barley: a translational model for adaptation to climate change. New Phytol 206:913–931. https://doi.org/10.1111/nph.13266
Day A, Goldschmidt-Clermont M (2011) The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol J 9:540–553. https://doi.org/10.1111/j.1467-7652.2011.00604.x
Debbarma J, Sarki YN, Saikia B, Boruah HPD, Singha DL, Chikkaputtaiah C (2019) Ethylene response factor (ERF) family proteins in abiotic stresses and CRISPR-Cas9 genome editing of ERFs for multiple abiotic stress tolerance in crop plants: a review. Mol Biotechnol 61:153–172. https://doi.org/10.1007/s12033-018-0144-x
Debernardi JM, Greenwood JR, Jean Finnegan E, Jernstedt J, Dubcovsky J (2020) APETALA 2-like genes AP2L2 and Q specify lemma identity and axillary floral meristem development in wheat. Plant J 101:171–187. https://doi.org/10.1111/tpj.14528
Dhankher OP, Foyer CH (2018) Climate resilient crops for improving global food security and safety. Plant Cell Environ 41:877–884. https://doi.org/10.1111/pce.13207
Enquist BJ, Niklas KJ (2002) Global allocation rules for patterns of biomass partitioning in seed plants. Science 295:1517–1520. https://doi.org/10.1126/science.1066360
Eriksson D (2019) The evolving EU regulatory framework for precision breeding. Theor Appl Genet 132:569–573. https://doi.org/10.1007/s00122-018-3200-9
Farhat S et al (2019) CRISPR-Cas9 directed genome engineering for enhancing salt stress tolerance in rice. Semin Cell Dev Biol 96:91–99. https://doi.org/10.1016/j.semcdb.2019.05.003
Feng XP, Peng C, Chen Y, Liu XD, Feng XJ, He Y (2017) Discrimination of CRISPR/Cas9-induced mutants of rice seeds using near-infrared hyperspectral imaging. Sci Rep. https://doi.org/10.1038/s41598-017-16254-z
Ferguson John N, Meyer Rhonda C, Edwards Kieron D, Humphry M, Brendel O, Bechtold U (2019) Accelerated flowering time reduces lifetime water use without penalizing reproductive performance in Arabidopsis. Plant, Cell Environ 42:1847–1867. https://doi.org/10.1111/pce.13527
Flohr BM, Hunt JR, Kirkegaard JA, Evans JR (2017) Water and temperature stress define the optimal flowering period for wheat in south-eastern Australia. Field Crops Research 209:108–119. https://doi.org/10.1016/j.fcr.2017.04.012
Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525. https://doi.org/10.1007/s10265-011-0412-3
Fukai S, Cooper M (1995) Development of drought-resistant cultivars using physiomorphological traits in rice. Field Crops Research 40:67–86. https://doi.org/10.1016/0378-4290(94)00096-U
Furbank RT, Jimenez-Berni JA, George-Jaeggli B, Potgieter AB, Deery DM (2019) Field crop phenomics: enabling breeding for radiation use efficiency and biomass in cereal crops. New Phytol 223:1714–1727. https://doi.org/10.1111/nph.15817
Gammage PA, Moraes CT, Minczuk M (2018) Mitochondrial Genome Engineering: The Revolution May Not Be CRISPR-Ized. Trends Genet 34:101–110
Gatica-Arias A (2020) The regulatory current status of plant breeding technologies in some Latin American and the Caribbean countries. Plant Cell Tiss Org 141:229–242. https://doi.org/10.1007/s11240-020-01799-1
Gerashchenkov GA et al (2020) Design of guide RNA for CRISPR/Cas plant genome editing. Mol Biol 54:24–42. https://doi.org/10.1134/S0026893320010069
Ghosh S et al (2018) Speed breeding in growth chambers and glasshouses for crop breeding and model plant research. Nat Protoc 13:2944–2963. https://doi.org/10.1038/s41596-018-0072-z
Gilding E et al (2013) Allelic variation at a single gene increases food value in a drought-tolerant staple cereal. Nat Commun 4:1483. https://doi.org/10.1038/ncomms2450
Gornall J, Betts R, Burke E, Clark R, Camp J, Willett K, Wiltshire A (2010) Implications of climate change for agricultural productivity in the early twenty-first century. Philos T R Soc B 365:2973–2989. https://doi.org/10.1098/rstb.2010.0158
Hammer GL et al (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the U.S. Corn belt? Crop Sci 49:299–312. https://doi.org/10.2135/cropsci2008.03.0152
Hattori T, Totsuka M, Hobo T, Kagaya Y, Yamamoto-Toyoda A (2002) Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol 43:136–140. https://doi.org/10.1093/pcp/pcf014
Hawkesford MJ, Griffiths S (2019) Exploiting genetic variation in nitrogen use efficiency for cereal crop improvement. Curr Opin Plant Biol 49:35–42. https://doi.org/10.1016/j.pbi.2019.05.003
Hickey LT et al (2019) Breeding crops to feed 10 billion. Nat Biotechnol 37:744–754. https://doi.org/10.1038/s41587-019-0152-9
Hills C, Li CD (2016) Genetic architecture of flowering phenology in cereals and opportunities for crop improvement. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01906
Hoang TML, Tran TN, Nguyen TKT, Williams B, Wurm P, Bellairs S, Mundree S (2016) Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy. https://doi.org/10.3390/agronomy6040054
Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci 96:15348–15353. https://doi.org/10.1073/pnas.96.26.15348
Horvath P, Barrangou R (2010) CRISPR/cas, the immune system of bacteria and archaea. Science 327:167–170. https://doi.org/10.1126/science.1179555
Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Ann Rev Plant Biol 65:715–741. https://doi.org/10.1146/annurev-arplant-050213-040000
Huang L et al (2018) Characterization of transcription factor gene OsDRAP1 conferring drought tolerance in rice. Front Plant Sci 9:94–94. https://doi.org/10.3389/fpls.2018.00094
Hyles J, Bloomfield MT, Hunt JR, Trethowan RM, Trevaskis B (2020) Phenology and related traits for wheat adaptation. Heredity. https://doi.org/10.1038/s41437-020-0320-1
Jahne F, Hahn V, Wurschum T, Leiser WL (2020) Speed breeding short-day crops by LED-controlled light schemes. Theor Appl Genet 133:2335–2342. https://doi.org/10.1007/s00122-020-03601-4
Jain M (2015) Function genomics of abiotic stress tolerance in plants: a CRISPR approach. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00375
Jasin M, Rothstein R (2013) Repair of strand breaks by homologous recombination. Csh Perspect Biol. https://doi.org/10.1101/cshperspect.a012740
Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182-1187. https://doi.org/10.1093/nar/gkt1016
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA Endonuclease in Adaptive Bacterial Immunity. Science 337:816–821. https://doi.org/10.1126/science.1225829
Joshi, R K, Bharat S S and Mishra R (2020) Engineering drought tolerance in plants through CRISPR/Cas genome editing. 3 Biotech, 10:400 doi:https://doi.org/10.1007/s13205-020-02390-3
Kang BC et al (2018) Precision genome engineering through adenine base editing in plants. Nat Plants 4:427–431. https://doi.org/10.1038/s41477-018-0178-x
Kannan B, Jung JH, Moxley GW, Lee S, Altpeter F (2018) TALEN-mediated targeted mutagenesis of more than 100 COMT copies/alleles in highly polyploid sugarcane improves saccharification efficiency without compromising biomass yield. Plant Biotech J 16:856–866. https://doi.org/10.1111/pbi.12833
Karvelis T, Gasiunas G, Young JS, Bigelyte G, Silanskas A, Cigan M, Siksnys V (2015) Rapid characterization of CRISPR-Cas9 protospacer adjacent motif sequence elements. Genome Biol. https://doi.org/10.1186/s13059-015-0818-7
Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51:677–686
Kazama T et al (2019) Curing cytoplasmic male sterility via TALEN-mediated mitochondrial genome editing. Nat Plants 5:722–730. https://doi.org/10.1038/s41477-019-0459-z
Kim YJ, Zhang DB (2018) Molecular control of male fertility for crop hybrid breeding trends. Plant Sci 23:53–65. https://doi.org/10.1016/j.tplants.2017.10.001
Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: Zinc finger fusions to Fok I cleavage domain. P Natl Acad Sci USA 93:1156–1160. https://doi.org/10.1073/pnas.93.3.1156
Kitomi Y, Kanno N, Kawai S, Mizubayashi T, Fukuoka S, Uga Y (2015) QTLs underlying natural variation of root growth angle among rice cultivars with the same functional allele of DEEPER ROOTING 1. Rice, (N Y) 8:16–16 doi:https://doi.org/10.1186/s12284-015-0049-2
Kleinstiver BP, Prew MS, Topkar VV, Tsai SQ, Joung JK (2015) Engineered Cas9 variants with novel PAM specificities expand the targeting range of CRISPR/Cas nucleases. Mol Ther 23:S26–S26. https://doi.org/10.1016/S1525-0016(16)33663-2
Kleinstiver BP et al (2016) Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat Biotechnol 34:869. https://doi.org/10.1038/nbt.3620
Kleter GA, Kuiper HA, Kok EJ (2019) Gene-edited crops: towards a harmonized safety assessment trends. Biotechnol 37:443–447. https://doi.org/10.1016/j.tibtech.2018.11.014
Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748. https://doi.org/10.1093/jxb/err210
Ledford H (2016) CRISPR patent probe begins. Nature 531:149–149. https://doi.org/10.1038/531149a
Li C, Yue J, Wu X, Xu C, Yu J (2014) An ABA-responsive DRE-binding protein gene from Setaria italica, SiARDP, the target gene of SiAREB, plays a critical role under drought stress. J Exp Bot 65:5415–5427. https://doi.org/10.1093/jxb/eru302
Li X et al (2017) High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. Journal of Genetics and Genomics 44:175–178. https://doi.org/10.1016/j.jgg.2017.02.001
Li C, Lin H, Chen A, Lau M, Jernstedt J, Dubcovsky J (2019) Wheat VRN1, FUL2 and FUL3 play critical and redundant roles in spikelet development and spike determinacy Development (Cambridge, England) 146 doi:https://doi.org/10.1242/dev.175398
Liang Z et al (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun. https://doi.org/10.1038/ncomms14261
Liu C, Moschou PN (2018) Phenotypic novelty by CRISPR in plants. Dev Biol 435:170–175. https://doi.org/10.1016/j.ydbio.2018.01.015
Liu S et al (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLOS Genet 9:e1003790. https://doi.org/10.1371/journal.pgen.1003790
Lobell DB, Sibley A, Ortiz-Monasterio JI (2012) Extreme heat effects on wheat senescence in India. Nat Clim Change 2:186–189. https://doi.org/10.1038/Nclimate1356
Lobell DB, Hammer GL, McLean G, Messina C, Roberts MJ, Schlenker W (2013) The critical role of extreme heat for maize production in the United States. Nat Clim Change 3:497–501
Lou Q et al (2017) Root Transcriptomic Analysis Revealing the Importance of Energy Metabolism to the Development of Deep Roots in Rice (Oryza sativa L.). Front Plant Sci. https://doi.org/10.3389/fpls.2017.01314
Lowder LG et al (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169:971–985. https://doi.org/10.1104/pp.15.00636
Lu YM, Zhu JK (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10:523–525. https://doi.org/10.1016/j.molp.2016.11.013
Lu G et al (2015) OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. Plant J 83:913–925. https://doi.org/10.1111/tpj.12939
Lucas S, Durmaz E, Akpinar BA, Budak H (2011) The drought response displayed by a DRE-binding protein from Triticum dicoccoides. Plant Physiol Bioch 49:346–351. https://doi.org/10.1016/j.plaphy.2011.01.016
Ma XL, Zhu QL, Chen YL, Liu YG (2016) CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Mol Plant 9:961–974. https://doi.org/10.1016/j.molp.2016.04.009
Ma XS et al (2019) A novel rice grain size gene OsSNB was identified by genome-wide association study in natural population. Plos Genet. https://doi.org/10.1371/journal.pgen.1008191
Maher MF, Nasti RA, Vollbrecht M, Starker CG, Clark MD, Voytas DF (2020) Plant gene editing through de novo induction of meristems. Nat Biotechnol 38:84–89. https://doi.org/10.1038/s41587-019-0337-2
Marcotte WR, Russell SH, Quatrano RS (1989) Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1:969–976. https://doi.org/10.2307/3868997
Massel K et al (2016) Whole genome sequencing reveals potential new targets for improving nitrogen uptake and utilization in sorghum bicolor. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01544
Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao Z-C (2007) Global Climate Projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom, New York, NY, USA
Meyer RS, Purugganan MD (2013) Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet 14:840–852. https://doi.org/10.1038/nrg3605
Moradpour M, Abdulah SNA (2020) CRISPR/dCas9 platforms in plants: strategies and applications beyond genome editing. Plant Biotechnol J 18:32–44. https://doi.org/10.1111/pbi.13232
Morran S et al (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249. https://doi.org/10.1111/j.1467-7652.2010.00547.x
Muller M et al (2016) Streptococcus thermophilus CRISPR-Cas9 systems enable specific editing of the human genome. Mol Ther 24:636–644. https://doi.org/10.1038/mt.2015.218
Muraya MM, Chu JT, Zhao YS, Junker A, Klukas C, Reif JC, Altmann T (2017) Genetic variation of growth dynamics in maize (Zea mays L.) revealed through automated non-invasive phenotyping. Plant J 89:366–380. https://doi.org/10.1111/tpj.13390
Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in arabidopsis and grasses. Plant Physiol 149:88–95. https://doi.org/10.1104/pp.108.129791
Narusaka Y et al (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148. https://doi.org/10.1046/j.1365-313x.2003.01708.x
Ngangkham U et al (2018) Effect of multiple allelic combinations of genes on regulating grain size in rice. PLoS ONE 13(1):e0190684. https://doi.org/10.1371/journal.pone.0190684
Normile D (2019) Chinese scientist who produced genetically altered babies sentenced to 3 years in jail. Science. https://doi.org/10.1126/science.aba7347
Normile D, Cohen J (2019) Government report blasts creator of CRISPR twins. Science 363:328–328. https://doi.org/10.1126/science.363.6425.328
Okada A et al (2019) CRISPR/Cas9-mediated knockout of Ms1 enables the rapid generation of male-sterile hexaploid wheat lines for use in hybrid seed production. Plant Biotechnol J 17:1905–1913. https://doi.org/10.1111/pbi.13106
Osakabe Y, Watanabe T, Sugano SS, Ueta R, Ishihara R, Shinozaki K, Osakabe K (2016) Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci Rep. https://doi.org/10.1038/srep26685
Pacher M, Puchta H (2017) From classical mutagenesis to nuclease-based breeding - directing natural DNA repair for a natural end-product. Plant J 90:819–833. https://doi.org/10.1111/tpj.13469
Peng SB et al (2004) Rice yields decline with higher night temperature from global warming. P Natl Acad Sci USA 101:9971–9975. https://doi.org/10.1073/pnas.0403720101
Phukan UJ, Jeena GS, Tripathi V, Shukla RK (2017) Regulation of Apetala2/Ethylene response factors in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00150
Piatek A et al (2015) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13:578–589. https://doi.org/10.1111/pbi.12284
Prado JR et al (2014) Genetically engineered crops: from idea to product. Annu Rev Plant Biol 65:769–790. https://doi.org/10.1146/annurev-arplant-050213-040039
Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in arabidopsis. Plant Cell 12:479–492
Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281–2308. https://doi.org/10.1038/nprot.2013.143
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE. https://doi.org/10.1371/journal.pone.0066428
Reynolds MP et al (2016) An integrated approach to maintaining cereal productivity under climate change. Global Food Security 8:9–18. https://doi.org/10.1016/j.gfs.2016.02.002
Rhee SY, Mutwil M (2014) Towards revealing the functions of all genes in plants. Trends Plant Sci 19:212–221. https://doi.org/10.1016/j.tplants.2013.10.006
Ricroch AE, Ammann K, Kuntz M (2016) Editing EU legislation to fit plant genome editing. Embo Rep 17:1365–1369. https://doi.org/10.15252/embr.201643099
Roca Paixão JF et al (2019) Improved drought stress tolerance in Arabidopsis by CRISPR/dCas9 fusion with a Histone AcetylTransferase. Sci Rep 9:8080. https://doi.org/10.1038/s41598-019-44571-y
Rodgers-Melnick E et al (2015) Recombination in diverse maize is stable, predictable, and associated with genetic load. P Natl Acad Sci USA 112:3823–3828. https://doi.org/10.1073/pnas.1413864112
Rodriguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:470–480. https://doi.org/10.1016/j.cell.2017.08.030
Sakuma S et al (2017) Extreme suppression of lateral floret development by a single amino acid change in the VRS1 transcription factor. Plant Physiol 175:1720–1731. https://doi.org/10.1104/pp.17.01149
Sánchez-León S, Gil-Humanes J, Ozuna CV, Giménez MJ, Sousa C, Voytas DF, Barro F (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16:902910. https://doi.org/10.1111/pbi.12837
Santosh Kumar VV, Verma RK, Yadav SK, Yadav P, Watts A, Rao MV, Chinnusamy V (2020) CRISPR-Cas9 mediated genome editing of drought and salt tolerance (OsDST) gene in indica mega rice cultivar MTU1010. Physiology and Molecular Biology of Plants 26:1099–1110. https://doi.org/10.1007/s12298-020-00819-w
Scheben A, Edwards D (2018) Towards a more predictable plant breeding pipeline with CRISPR/Cas-induced allelic series to optimize quantitative and qualitative traits. Curr Opin Plant Biol 45:218–225. https://doi.org/10.1016/j.pbi.2018.04.013
Scheben A, Wolter F, Batley J, Puchta H, Edwards D (2017) Towards CRISPR/Cas crops - bringing together genomics and genome editing. New Phytol 216:682–698. https://doi.org/10.1111/nph.14702
Schiemann J, Robienski J, Schleissing S, Spok A, Sprink T, Wilhelm RA (2020) Editorial: plant genome editing - policies and governance. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00284
Sharwood RE (2017) Engineering chloroplasts to improve Rubisco catalysis: prospects for translating improvements into food and fiber crops. New Phytol 213:494–510. https://doi.org/10.1111/nph.14351
Shen Q, Zhang P, Ho TH (1996) Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8:1107–1119. https://doi.org/10.1105/tpc.8.7.1107
Shen YO, Pan GT, Lubberstedt T (2015) Haploid strategies for functional validation of plant genes. Trends Biotechnol 33:611–620. https://doi.org/10.1016/j.tibtech.2015.07.005
Shen CX, Que ZQ, Xia YM, Tang N, Li D, He RH, Cao ML (2017) Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biol 60:539–547. https://doi.org/10.1007/s12374-016-0400-1
Shen L et al (2018) QTL editing confers opposing yield performance in different rice varieties. J Integr Plant Biol 60:89–93. https://doi.org/10.1111/jipb.12501
Shi WM, Muramoto Y, Ueda A, Takabe T (2001) Cloning of peroxisomal ascorbate peroxidase gene from barley and enhanced thermotolerance by overexpressing in Arabidopsis thaliana. Gene 273:23–27
Shi JR et al (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216. https://doi.org/10.1111/pbi.12603
Shim SH et al (2020) Loss of function of rice plastidic glycolate/glycerate translocator 1 impairs photorespiration and plant growth. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01726
Shimatani Z et al (2017) Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol 35:441. https://doi.org/10.1038/nbt.3833
Singh V, Nguyen CT, van Oosterom EJ, Chapman SC, Jordan DR, Hammer GL (2015) Sorghum genotypes differ in high temperature responses for seed set. Field Crops Research 171:32–40. https://doi.org/10.1016/j.fcr.2014.11.003
Singh A, Ganapathysubramanian B, Singh AK, Sarkar S (2016) Machine learning for high-throughput stress phenotyping in plants. Trends Plant Sci 21:110–124. https://doi.org/10.1016/j.tplants.2015.10.015
Singh M, Kumar M, Albertsen MC, Young JK, Cigan AM (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 97:371–383. https://doi.org/10.1007/s11103-018-0749-2
Singh B, Salaria N, Thakur K, Kukreja S, Gautam S, Goutam U (2019) Functional genomic approaches to improve crop plant heat stress tolerance. F1000Res, 8: 1721 doi:https://doi.org/10.12688/f1000research.19840.1
South PF, Walker BJ, Cavanagh AP, Rolland V, Badger M, Ort DR (2017) Bile acid sodium symporter BASS6 can transport glycolate and is involved in photorespiratory metabolism in Arabidopsis thaliana. Plant Cell 29:808. https://doi.org/10.1105/tpc.16.00775
South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science. https://doi.org/10.1126/science.aat9077
Stephen L, p, Marshall-Colon A, Zhu X-G, (2015) Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161:56–66. https://doi.org/10.1016/j.cell.2015.03.019
Stratonovitch P, Semenov MA (2015) Heat tolerance around flowering in wheat identified as a key trait for increased yield potential in Europe under climate change. J Exp Bot 66:3599–3609. https://doi.org/10.1093/jxb/erv070
Tebaldi C, Arblaster JM, Knutti R (2011) Mapping model agreement on future climate projections. Geophys Res Lett 38:L23701
Theißen G, Melzer R, Rümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143:3259–3271. https://doi.org/10.1242/dev.134080
Thygesen P (2019) Clarifying the regulation of genome editing in Australia: situation for genetically modified organisms. Transgenic Res 28:151–159. https://doi.org/10.1007/s11248-019-00151-4
Tian F et al (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43:159-U113. https://doi.org/10.1038/ng.746
Trethowan RM (2014) Defining a genetic ideotype for crop improvement. In: Fleury D, Whitford R (eds) Crop breeding: methods and protocols. Springer New York, New York, NY, pp 1–20. doi:https://doi.org/10.1007/978-1-4939-0446-4_1
Tsuda M, Watanabe KN, Ohsawa R (2019) Regulatory status of genome-edited organisms under the Japanese cartagena act. Front Bioeng Biotech. https://doi.org/10.3389/fbioe.2019.00387
Uga Y et al (2013a) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45:1097–1102. https://doi.org/10.1038/ng.2725
Uga Y, Yamamoto E, Kanno N, Kawai S, Mizubayashi T, Fukuoka S (2013b) A major QTL controlling deep rooting on rice chromosome 4. Sci Rep 3:3040–3040. https://doi.org/10.1038/srep03040
Valluru R et al (2019) Deleterious mutation burden and its association with complex traits in Sorghum (Sorghum bicolor). Genetics 211:1075–1087. https://doi.org/10.1534/genetics.118.301742
Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86. https://doi.org/10.1186/s12870-016-0771-y
Voss-Fels KP et al (2018) VERNALIZATION1 modulates root system architecture in wheat and barley. Mol Plant 11:226–229. https://doi.org/10.1016/j.molp.2017.10.005
Voss-Fels KP HE, Dreisigacker S, Sukurmaran S, Watson A, Frisch M, Hayes BJ, Hickey LT (2018) "SpeedGS" to accelerate genetic gain in spring wheat. In: Applications of genetic and genomic research in cereals, 1st edn. Woodhead Publishing, Cambridge. doi:https://doi.org/10.1016/B978-0-08-102163-7.00014-4
Voss-Fels KP, Cooper M, Hayes B (2019) Accelerating crop genetic gains with genomic selection. Theor Appl Genet 132:669–686. https://doi.org/10.1007/s00122-018-3270-8
Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602. https://doi.org/10.1007/s11103-008-9340-6
Wang Y, Sun F, Cao H, Peng H, Ni Z, Sun Q, Yao Y (2012) TamiR159 directed wheat TaGAMYB cleavage and its involvement in anther development and heat response. PLoS ONE 7:e48445. https://doi.org/10.1371/journal.pone.0048445
Wang DX, Skibbe D, Walbot V (2013) Maize Male sterile 8 (Ms8), a putative beta-1,3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development. Plant Reprod 26:329–338. https://doi.org/10.1007/s00497-013-0230-y
Wang YP, Cheng X, Shan QW, Zhang Y, Liu JX, Gao CX, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951. https://doi.org/10.1038/nbt.2969
Wang MG, Lu YM, Botella JR, Mao YF, Hua K, Zhu JK (2017) Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Mol Plant 10:1007–1010. https://doi.org/10.1016/j.molp.2017.03.002
Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176. https://doi.org/10.1016/j.cj.2016.01.010
Watson A et al (2018) Speed breeding is a powerful tool to accelerate crop research and breeding. Nat Plants 4:23–29. https://doi.org/10.1038/s41477-017-0083-8
Weider C, Stamp P, Christov N, Husken A, Foueillassar X, Camp KH, Munsch M (2009) Stability of cytoplasmic male sterility in maize under different environmental conditions. Crop Sci 49:77–84. https://doi.org/10.2135/cropsci2007.12.0694
Whitford R, Fleury D, Reif JC, Garcia M, Okada T, Korzun V, Langridge P (2013) Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. J Exp Bot 64:5411–5428. https://doi.org/10.1093/jxb/ert333
Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338. https://doi.org/10.1038/nature10886
Wittkopp PJ, Kalay G (2011) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69. https://doi.org/10.1038/nrg3095
Wu YZ et al (2016) Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J 14:1046–1054. https://doi.org/10.1111/pbi.12477
Xie KB, Minkenberg B, Yang YN (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. P Natl Acad Sci USA 112:3570–3575. https://doi.org/10.1073/pnas.1420294112
Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci U S A 99:7530–7535. https://doi.org/10.1073/pnas.112209199
Yuan LP (1990) Progress of two-line system hybrid rice breeding. Scientia Agricultura Sinica 23:1–6
Yuan LP (2014) Development of hybrid rice to ensure food security. Rice Sci 21:1–2. https://doi.org/10.1016/S1672-6308(13)60167-5
Yue JJ, Hong CY, Wei PC, Tsai YC, Lin CS (2020) How to start your monocot CRISPR/Cas project: plasmid design, efficiency detection, and offspring analysis. Rice. https://doi.org/10.1186/s12284-019-0354-2
Zeng YF, Wen JY, Zhao WB, Wang Q, Huang WC (2020) Rational improvement of rice yield and cold tolerance by editing the three genes OsPIN5b, GS3, and OsMYB30 with the CRISPR-Cas9 system. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01663
Zhang QF, Shen BZ, Dai XK, Mei MH, Maroof MAS, Li ZB (1994) Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male-sterility in rice. P Natl Acad Sci USA 91:8675–8679. https://doi.org/10.1073/pnas.91.18.8675
Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119. https://doi.org/10.1016/j.fcr.2005.08.018
Zhang SW et al (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889–1901. https://doi.org/10.1104/pp.109.146803
Zhang H et al (2013) Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. P Natl Acad Sci USA 110:76–81. https://doi.org/10.1073/pnas.1213041110
Zhang LY et al (2017) Isolation and characterization of heat-responsive gene TaGASR1 from wheat (Triticum aestivum L.). J Plant Biol 60:57–65
Zhang YW, Bai Y, Wu GH, Zou SH, Chen YF, Gao CX, Tang DZ (2017) Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J 91:714–724. https://doi.org/10.1111/tpj.13599
Zhang AN et al (2019) Enhanced rice salinity tolerance via CRISPR/Cas9-targeted mutagenesis of the OsRR22 gene. Mol Breed. https://doi.org/10.1007/s11032-019-0954-y
Zhang Y, Massel K, Godwin ID, Gao CX (2019b) Applications and potential of genome editing in crop improvement (vol 19, 210, 2018) Genome Biol 20 doi: https://doi.org/10.1186/s13059-019-1622-6
Zhang DB et al (2020) Genome editing with the CRISPR-Cas system: an art, ethics and global regulatory perspective. Plant Biotechnol J 18:1651–1669. https://doi.org/10.1111/pbi.13383
Zhao L, Hu Y, Chong R, Wang T (2010) ARAG1, an ABA-responsive DREB gene, plays a role in seed germination and drought tolerance of rice. Ann Botany 105:401–409
Zhou H et al (2012) Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22:649–660. https://doi.org/10.1038/cr.2012.28
Zhou H et al (2014) RNase Z(S1) processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5:4884. https://doi.org/10.1038/ncomms5884
Zhou H et al (2016) Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep. https://doi.org/10.1038/srep37395
Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Ann Rev Plant Biol 61:235–261. https://doi.org/10.1146/annurev-arplant-042809-112206
Zong Y et al (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438. https://doi.org/10.1038/nbt.3811
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This was funded through a grant from the Australian Research Council (ARC) Discovery Project (ID: DP190102185) entitled “Cereal blueprints for a water-limited world”.
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Massel, K., Lam, Y., Wong, A.C.S. et al. Hotter, drier, CRISPR: the latest edit on climate change. Theor Appl Genet 134, 1691–1709 (2021). https://doi.org/10.1007/s00122-020-03764-0
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DOI: https://doi.org/10.1007/s00122-020-03764-0