Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

Potential Application of CRISPR/Cas9 System to Engineer Abiotic Stress Tolerance in Plants

Author(s): Temoor Ahmed, Muhammad Noman, Muhammad Shahid*, Sher Muhammad, Muhammad Tahir ul Qamar, Md. Arshad Ali, Awais Maqsood, Rahila Hafeez, Solabomi Olaitan Ogunyemi and Bin Li*

Volume 28, Issue 8, 2021

Published on: 18 February, 2021

Page: [861 - 877] Pages: 17

DOI: 10.2174/0929866528666210218220138

Price: $65

Abstract

Abiotic stresses in plants such as salinity, drought, heavy metal toxicity, heat, and nutrients limitations significantly reduce agricultural production worldwide. The genome editing techniques such as transcriptional activator-like effector nucleases (TALENs) and zinc finger nucleases (ZFNs) have been used for genome manipulations in plants. However, clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) technique has recently emerged as a promising tool for genome editing in plants to acquire desirable traits. The CRISPR/Cas9 system has a great potential to develop crop varieties with improved tolerance against abiotic stresses. This review is centered on the biology and potential application of the CRISPR/Cas9 system to improve abiotic stress tolerance in plants. Furthermore, this review highlighted the recent advancements of CRISPR/Cas9-mediated genome editing for sustainable agriculture.

Keywords: CRISPR/Cas9, abiotic stresses, genome editing, crop improvement, transcription, sgRNA.

Graphical Abstract

[1]
Suweisa, S.; Carrb, J.A.; Maritana, A.; Rinaldoc, A.; D’Odoricob, P. Correction for Suweis et al., Resilience and reactivity of global food security. Proc. Natl. Acad. Sci. USA, 2015, 112(34), E4811.
[http://dx.doi.org/10.1073/pnas.1512971112] [PMID: 26170325]
[2]
Khan, M.S.; Ahmad, D.; Khan, M.A. Utilization of genes encoding osmoprotectants in transgenic plants for enhanced abiotic stress tolerance. Electron. J. Biotechnol., 2015, 18(4), 257-266.
[http://dx.doi.org/10.1016/j.ejbt.2015.04.002]
[3]
Zafar, S.A.; Zaidi, S.S-A.; Gaba, Y.; Singla-Pareek, S.L.; Dhankher, O.P.; Li, X.; Mansoor, S.; Pareek, A. Engineering abiotic stress tolerance via CRISPR/ Cas-mediated genome editing. J. Exp. Bot., 2020, 71(2), 470-479.
[http://dx.doi.org/10.1093/jxb/erz476] [PMID: 31644801]
[4]
Wani, S.H.; Kumar, V.; Shriram, V.; Sah, S.K. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J., 2016, 4(3), 162-176.
[http://dx.doi.org/10.1016/j.cj.2016.01.010]
[5]
Ahmad, S.; Wei, X.; Sheng, Z.; Hu, P.; Tang, S. CRISPR/Cas9 for development of disease resistance in plants: recent progress, limitations and future prospects. Brief. Funct. Genomics, 2020, 19(1), 26-39.
[http://dx.doi.org/10.1093/bfgp/elz041] [PMID: 31915817]
[6]
Debbarma, J.; Sarki, Y.N.; Saikia, B.; Boruah, H.P.D.; Singha, D.L.; Chikkaputtaiah, C. 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., 2019, 61(2), 153-172.
[http://dx.doi.org/10.1007/s12033-018-0144-x] [PMID: 30600447]
[7]
Cheeseman, J. Food security in the face of salinity, drought, climate change, and population growth. In: Halophytes for Food Security in Dry Lands; Khan, M.A.; Ozturk, O.; Ahmed, M.Z., Eds.; Academic Press, 2016; pp. 111-123.
[http://dx.doi.org/10.1016/B978-0-12-801854-5.00007-8]
[8]
Shinwari, Z.K.; Jan, S.A.; Nakashima, K.; Yamaguchi-Shinozaki, K. Genetic engineering approaches to understanding drought tolerance in plants. Plant Biotechnol. Rep., 2020, 14(2), 151-162.
[http://dx.doi.org/10.1007/s11816-020-00598-6]
[9]
Hasegawa, T.; Fujimori, S.; Havlík, P.; Valin, H.; Bodirsky, B.L.; Doelman, J.C.; Fellmann, T.; Kyle, P.; Koopman, J.F.; Lotze-Campen, H. Risk of increased food insecurity under stringent global climate change mitigation policy. Nat. Clim. Chang., 2018, 8(8), 699-703.
[http://dx.doi.org/10.1038/s41558-018-0230-x]
[10]
Driedonks, N.; Rieu, I.; Vriezen, W.H. Breeding for plant heat tolerance at vegetative and reproductive stages. Plant Reprod., 2016, 29(1-2), 67-79.
[http://dx.doi.org/10.1007/s00497-016-0275-9] [PMID: 26874710]
[11]
Zaidi, S.S-A.; Tashkandi, M.; Mansoor, S.; Mahfouz, M.M. Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Front. Plant Sci., 2016, 7, 1673.
[http://dx.doi.org/10.3389/fpls.2016.01673] [PMID: 27877187]
[12]
Ray, D.K.; Mueller, N.D.; West, P.C.; Foley, J.A. Yield trends are insufficient to double global crop production by 2050. PLoS One, 2013, 8(6), e66428.
[http://dx.doi.org/10.1371/journal.pone.0066428] [PMID: 23840465]
[13]
Napier, J.A.; Haslam, R.P.; Tsalavouta, M.; Sayanova, O. The challenges of delivering genetically modified crops with nutritional enhancement traits. Nat. Plants, 2019, 5(6), 563-567.
[http://dx.doi.org/10.1038/s41477-019-0430-z] [PMID: 31160704]
[14]
Shukla, M.; Al-Busaidi, K.T.; Trivedi, M.; Tiwari, R.K. Status of research, regulations and challenges for genetically modified crops in India. GM Crops Food, 2018, 9(4), 173-188.
[http://dx.doi.org/10.1080/21645698.2018.1529518] [PMID: 30346874]
[15]
Zaidi, S.S-A.; Mahfouz, M.M.; Mansoor, S. CRISPR-Cpf1: A New Tool for Plant Genome Editing. Trends Plant Sci., 2017, 22(7), 550-553.
[http://dx.doi.org/10.1016/j.tplants.2017.05.001] [PMID: 28532598]
[16]
Čermák, T.; Curtin, S.J.; Gil-Humanes, J.; Čegan, R.; Kono, T.J.Y.; Konečná, E.; Belanto, J.J.; Starker, C.G.; Mathre, J.W.; Greenstein, R.L.; Voytas, D.F. A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell, 2017, 29(6), 1196-1217.
[http://dx.doi.org/10.1105/tpc.16.00922] [PMID: 28522548]
[17]
Arora, L.; Narula, A. Gene editing and crop improvement using CRISPR-Cas9 system. Front. Plant Sci., 2017, 8, 1932.
[http://dx.doi.org/10.3389/fpls.2017.01932] [PMID: 29167680]
[18]
Stella, S.; Montoya, G. The genome editing revolution: A CRISPR-Cas TALE off-target story. BioEssays, 2016, 38(Suppl. 1), S4-S13.
[http://dx.doi.org/10.1002/bies.201670903] [PMID: 27417121]
[19]
Nongpiur, R.C.; Singla-Pareek, S.L.; Pareek, A. Genomics approaches for improving salinity stress tolerance in crop plants. Curr. Genomics, 2016, 17(4), 343-357.
[http://dx.doi.org/10.2174/1389202917666160331202517] [PMID: 27499683]
[20]
Ceasar, S.A.; Rajan, V.; Prykhozhij, S.V.; Berman, J.N.; Ignacimuthu, S. Insert, remove or replace: a highly advanced genome editing system using CRISPR/Cas9. Biochim. Biophys. Acta, 2016, 1863(9), 2333-2344.
[http://dx.doi.org/10.1016/j.bbamcr.2016.06.009] [PMID: 27350235]
[21]
Kamthan, A.; Chaudhuri, A.; Kamthan, M.; Datta, A. Genetically modified (GM) crops: milestones and new advances in crop improvement. Theor. Appl. Genet., 2016, 129(9), 1639-1655.
[http://dx.doi.org/10.1007/s00122-016-2747-6] [PMID: 27381849]
[22]
Zsögön, A.; Cermak, T.; Voytas, D.; Peres, L.E.P. Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: Case study in tomato. Plant Sci., 2017, 256, 120-130.
[http://dx.doi.org/10.1016/j.plantsci.2016.12.012] [PMID: 28167025]
[23]
Gao, J.; Wang, G.; Ma, S.; Xie, X.; Wu, X.; Zhang, X.; Wu, Y.; Zhao, P.; Xia, Q. CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol. Biol., 2015, 87(1-2), 99-110.
[http://dx.doi.org/10.1007/s11103-014-0263-0] [PMID: 25344637]
[24]
Belhaj, K.; Chaparro-Garcia, A.; Kamoun, S.; Patron, N.J.; Nekrasov, V. Editing plant genomes with CRISPR/Cas9. Curr. Opin. Biotechnol., 2015, 32, 76-84.
[http://dx.doi.org/10.1016/j.copbio.2014.11.007] [PMID: 25437637]
[25]
Haeussler, M.; Concordet, J.P. Genome editing with CRISPR-Cas9: can it get any better? J. Genet. Genomics, 2016, 43(5), 239-250.
[http://dx.doi.org/10.1016/j.jgg.2016.04.008] [PMID: 27210042]
[26]
Tripathi, L.; Ntui, V.O.; Tripathi, J.N. CRISPR/Cas9-based genome editing of banana for disease resistance. Curr. Opin. Plant Biol., 2020, 56, 118-126.
[http://dx.doi.org/10.1016/j.pbi.2020.05.003] [PMID: 32604025]
[27]
Makarova, K.S.; Haft, D.H.; Barrangou, R.; Brouns, S.J.; Charpentier, E.; Horvath, P.; Moineau, S.; Mojica, F.J.; Wolf, Y.I.; Yakunin, A.F.; van der Oost, J.; Koonin, E.V. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol., 2011, 9(6), 467-477.
[http://dx.doi.org/10.1038/nrmicro2577] [PMID: 21552286]
[28]
Rani, R.; Yadav, P.; Barbadikar, K.M.; Baliyan, N.; Malhotra, E.V.; Singh, B.K.; Kumar, A.; Singh, D. CRISPR/Cas9: a promising way to exploit genetic variation in plants. Biotechnol. Lett., 2016, 38(12), 1991-2006.
[http://dx.doi.org/10.1007/s10529-016-2195-z] [PMID: 27571968]
[29]
Schaeffer, S.M.; Nakata, P.A. CRISPR/Cas9-mediated genome editing and gene replacement in plants: transitioning from lab to field. Plant Sci., 2015, 240, 130-142.
[http://dx.doi.org/10.1016/j.plantsci.2015.09.011] [PMID: 26475194]
[30]
Hussain, M.I.; Lyra, D-A.; Farooq, M.; Nikoloudakis, N.; Khalid, N. Salt and drought stresses in safflower: a review. Agron. Sustain. Dev., 2016, 36(1), 4.
[http://dx.doi.org/10.1007/s13593-015-0344-8]
[31]
Jiang, W.; Yang, B.; Weeks, D.P. Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS One, 2014, 9(6), e99225.
[http://dx.doi.org/10.1371/journal.pone.0099225] [PMID: 24918588]
[32]
Kumar, V.; AlMomin, S.; Rahman, M.H.; Shajan, A. Use of CRISPR in climate smart/resilient agriculture. In: CRISPR/Cas Genome Editing; Bhattacharya, A.; Parkhi, V.; Char, B., Eds.; Springer International Publishing: Switzerland, 2020; pp. 131-164.
[http://dx.doi.org/10.1007/978-3-030-42022-2_7]
[33]
Alagoz, Y.; Gurkok, T.; Zhang, B.; Unver, T. Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci. Rep., 2016, 6(1), 30910.
[http://dx.doi.org/10.1038/srep30910] [PMID: 27483984]
[34]
Mercx, S.; Smargiasso, N.; Chaumont, F.; De Pauw, E.; Boutry, M.; Navarre, C. Inactivation of the β(1,2)-xylosyltransferase and the α(1,3)-fucosyltransferase genes in Nicotiana tabacum BY-2 cells by a multiplex CRISPR/Cas9 strategy results in glycoproteins without plant-specific glycans. Front. Plant Sci., 2017, 8, 403.
[http://dx.doi.org/10.3389/fpls.2017.00403] [PMID: 28396675]
[35]
Niu, Q.; Wu, S.; Li, Y.; Yang, X.; Liu, P.; Xu, Y.; Lang, Z. Expanding the scope of CRISPR/Cas9-mediated genome editing in plants using an xCas9 and Cas9-NG hybrid. J. Integr. Plant Biol., 2020, 62(4), 398-402.
[http://dx.doi.org/10.1111/jipb.12886] [PMID: 31702097]
[36]
Liu, X.; Xie, C.; Si, H.; Yang, J. CRISPR/Cas9-mediated genome editing in plants. Methods, 2017, 121-122, 94-102.
[http://dx.doi.org/10.1016/j.ymeth.2017.03.009] [PMID: 28315486]
[37]
Sun, Y.; Zhang, X.; Wu, C.; He, Y.; Ma, Y.; Hou, H.; Guo, X.; Du, W.; Zhao, Y.; Xia, L. Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant, 2016, 9(4), 628-631.
[http://dx.doi.org/10.1016/j.molp.2016.01.001] [PMID: 26768120]
[38]
Eid, A.; Alshareef, S.; Mahfouz, M.M. CRISPR base editors: genome editing without double-stranded breaks. Biochemical Journal, 2018, 475(11), 1955-1964.
[39]
Kantor, A.; McClements, M.E.; MacLaren, R.E. CRISPR-Cas9 DNA base-editing and prime-editing. Int. J. Mol. Sci., 2020, 21(17), 6240.
[http://dx.doi.org/10.3390/ijms21176240] [PMID: 32872311]
[40]
Qin, L.; Li, J.; Wang, Q.; Xu, Z.; Sun, L.; Alariqi, M.; Manghwar, H.; Wang, G.; Li, B.; Ding, X.; Rui, H.; Huang, H.; Lu, T.; Lindsey, K.; Daniell, H.; Zhang, X.; Jin, S. High-efficient and precise base editing of C•G to T•A in the allotetraploid cotton (Gossypium hirsutum) genome using a modified CRISPR/Cas9 system. Plant Biotechnol. J., 2020, 18(1), 45-56.
[http://dx.doi.org/10.1111/pbi.13168] [PMID: 31116473]
[41]
Molla, K.A.; Yang, Y. CRISPR/Cas-mediated base editing: technical considerations and practical applications. Trends Biotechnol., 2019, 37(10), 1121-1142.
[http://dx.doi.org/10.1016/j.tibtech.2019.03.008] [PMID: 30995964]
[42]
Anzalone, A.V.; Randolph, P.B.; Davis, J.R.; Sousa, A.A.; Koblan, L.W.; Levy, J.M.; Chen, P.J.; Wilson, C.; Newby, G.A.; Raguram, A.; Liu, D.R. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature, 2019, 576(7785), 149-157.
[http://dx.doi.org/10.1038/s41586-019-1711-4] [PMID: 31634902]
[43]
Marzec, M.; Brąszewska-Zalewska, A.; Hensel, G. Prime editing: a new way for genome editing. Trends Cell Biol., 2020, 30(4), 257-259.
[http://dx.doi.org/10.1016/j.tcb.2020.01.004] [PMID: 32001098]
[44]
Feng, Z.; Zhang, B.; Ding, W.; Liu, X.; Yang, D-L.; Wei, P.; Cao, F.; Zhu, S.; Zhang, F.; Mao, Y.; Zhu, J.K. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res., 2013, 23(10), 1229-1232.
[http://dx.doi.org/10.1038/cr.2013.114] [PMID: 23958582]
[45]
Mao, Y.; Zhang, H.; Xu, N.; Zhang, B.; Gou, F.; Zhu, J-K. Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol. Plant, 2013, 6(6), 2008-2011.
[http://dx.doi.org/10.1093/mp/sst121] [PMID: 23963532]
[46]
Li, J-F.; Norville, J.E.; Aach, J.; McCormack, M.; Zhang, D.; Bush, J.; Church, G.M.; Sheen, J. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol., 2013, 31(8), 688-691.
[http://dx.doi.org/10.1038/nbt.2654] [PMID: 23929339]
[47]
Jiang, W.; Zhou, H.; Bi, H.; Fromm, M.; Yang, B.; Weeks, D.P. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res., 2013, 41(20), e188.
[http://dx.doi.org/10.1093/nar/gkt780] [PMID: 23999092]
[48]
Fauser, F.; Schiml, S.; Puchta, H. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J., 2014, 79(2), 348-359.
[http://dx.doi.org/10.1111/tpj.12554] [PMID: 24836556]
[49]
Feng, Z.; Mao, Y.; Xu, N.; Zhang, B.; Wei, P.; Yang, D-L.; Wang, Z.; Zhang, Z.; Zheng, R.; Yang, L.; Zeng, L.; Liu, X.; Zhu, J.K. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl. Acad. Sci. USA, 2014, 111(12), 4632-4637.
[http://dx.doi.org/10.1073/pnas.1400822111] [PMID: 24550464]
[50]
Schiml, S.; Fauser, F.; Puchta, H. The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J., 2014, 80(6), 1139-1150.
[http://dx.doi.org/10.1111/tpj.12704] [PMID: 25327456]
[51]
Hyun, Y.; Kim, J.; Cho, S.W.; Choi, Y.; Kim, J-S.; Coupland, G. Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta, 2015, 241(1), 271-284.
[http://dx.doi.org/10.1007/s00425-014-2180-5] [PMID: 25269397]
[52]
Wang, Z-P.; Xing, H-L.; Dong, L.; Zhang, H-Y.; Han, C-Y.; Wang, X-C.; Chen, Q-J. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol., 2015, 16(1), 144.
[http://dx.doi.org/10.1186/s13059-015-0715-0] [PMID: 26193878]
[53]
Yan, L.; Wei, S.; Wu, Y.; Hu, R.; Li, H.; Yang, W.; Xie, Q. High-efficiency genome editing in Arabidopsis using YAO promoter-driven CRISPR/Cas9 system. Mol. Plant, 2015, 8(12), 1820-1823.
[http://dx.doi.org/10.1016/j.molp.2015.10.004] [PMID: 26524930]
[54]
Peterson, B.A.; Haak, D.C.; Nishimura, M.T.; Teixeira, P.J.; James, S.R.; Dangl, J.L.; Nimchuk, Z.L. Genome-wide assessment of efficiency and specificity in CRISPR/Cas9 mediated multiple site targeting in Arabidopsis. PLoS One, 2016, 11(9), e0162169.
[http://dx.doi.org/10.1371/journal.pone.0162169] [PMID: 27622539]
[55]
Gao, X.; Chen, J.; Dai, X.; Zhang, D.; Zhao, Y. An effective strategy for reliably isolating heritable and Cas9-free Arabidopsis mutants generated by CRISPR/Cas9-mediated genome editing. Plant Physiol., 2016, 171(3), 1794-1800.
[http://dx.doi.org/10.1104/pp.16.00663] [PMID: 27208253]
[56]
Mao, Y.; Zhang, Z.; Feng, Z.; Wei, P.; Zhang, H.; Botella, J.R.; Zhu, J.K. Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol. J., 2016, 14(2), 519-532.
[http://dx.doi.org/10.1111/pbi.12468] [PMID: 26360626]
[57]
Hahn, F.; Mantegazza, O.; Greiner, A.; Hegemann, P.; Eisenhut, M.; Weber, A.P. An efficient visual screen for CRISPR/Cas9 activity in Arabidopsis thaliana. Front. Plant Sci., 2017, 8, 39.
[http://dx.doi.org/10.3389/fpls.2017.00039] [PMID: 28174584]
[58]
Ryder, P.; McHale, M.; Fort, A.; Spillane, C. Generation of stable nulliplex autopolyploid lines of Arabidopsis thaliana using CRISPR/Cas9 genome editing. Plant Cell Rep., 2017, 36(6), 1005-1008.
[http://dx.doi.org/10.1007/s00299-017-2125-0] [PMID: 28289885]
[59]
Tsutsui, H.; Higashiyama, T. pKAMA-ITACHI vectors for highly efficient CRISPR/Cas9-mediated gene knockout in Arabidopsis thaliana. Plant Cell Physiol., 2017, 58(1), 46-56.
[PMID: 27856772]
[60]
Dong, O.X.; Yu, S.; Jain, R.; Zhang, N.; Duong, P.Q.; Butler, C.; Li, Y.; Lipzen, A.; Martin, J.A.; Barry, K.W.; Schmutz, J.; Tian, L.; Ronald, P.C. Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nat. Commun., 2020, 11(1), 1178.
[http://dx.doi.org/10.1038/s41467-020-14981-y] [PMID: 32132530]
[61]
Shan, Q.; Wang, Y.; Li, J.; Zhang, Y.; Chen, K.; Liang, Z.; Zhang, K.; Liu, J.; Xi, J.J.; Qiu, J-L.; Gao, C. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol., 2013, 31(8), 686-688.
[http://dx.doi.org/10.1038/nbt.2650] [PMID: 23929338]
[62]
Zhou, H.; Liu, B.; Weeks, D.P.; Spalding, M.H.; Yang, B. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res., 2014, 42(17), 10903-10914.
[http://dx.doi.org/10.1093/nar/gku806] [PMID: 25200087]
[63]
Endo, M.; Mikami, M.; Toki, S. Multigene knockout utilizing off-target mutations of the CRISPR/Cas9 system in rice. Plant Cell Physiol., 2015, 56(1), 41-47.
[http://dx.doi.org/10.1093/pcp/pcu154] [PMID: 25392068]
[64]
Xu, R-F.; Li, H.; Qin, R-Y.; Li, J.; Qiu, C-H.; Yang, Y-C.; Ma, H.; Li, L.; Wei, P-C.; Yang, J-B. Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci. Rep., 2015, 5, 11491.
[http://dx.doi.org/10.1038/srep11491] [PMID: 26089199]
[65]
Li, M.; Li, X.; Zhou, Z.; Wu, P.; Fang, M.; Pan, X.; Lin, Q.; Luo, W.; Wu, G.; Li, H. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front. Plant Sci., 2016, 7, 377.
[http://dx.doi.org/10.3389/fpls.2016.00377] [PMID: 27066031]
[66]
Wang, M.; Lu, Y.; Botella, J.R.; Mao, Y.; Hua, K.; Zhu, J.K. Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Mol. Plant, 2017, 10(7), 1007-1010.
[http://dx.doi.org/10.1016/j.molp.2017.03.002] [PMID: 28315751]
[67]
Li, J.; Sun, Y.; Du, J.; Zhao, Y.; Xia, L. Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol. Plant, 2017, 10(3), 526-529.
[http://dx.doi.org/10.1016/j.molp.2016.12.001] [PMID: 27940306]
[68]
Lu, Y.; Zhu, J-K. Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant, 2017, 10(3), 523-525.
[http://dx.doi.org/10.1016/j.molp.2016.11.013] [PMID: 27932049]
[69]
Hu, X.; Meng, X.; Liu, Q.; Li, J.; Wang, K. Increasing the efficiency of CRISPR-Cas9-VQR precise genome editing in rice. Plant Biotechnol. J., 2018, 16(1), 292-297.
[http://dx.doi.org/10.1111/pbi.12771] [PMID: 28605576]
[70]
Endo, M.; Mikami, M.; Endo, A.; Kaya, H.; Itoh, T.; Nishimasu, H.; Nureki, O.; Toki, S. Genome editing in plants by engineered CRISPR-Cas9 recognizing NG PAM. Nat. Plants, 2019, 5(1), 14-17.
[http://dx.doi.org/10.1038/s41477-018-0321-8] [PMID: 30531939]
[71]
Upadhyay, S.K.; Kumar, J.; Alok, A.; Tuli, R. RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda), 2013, 3(12), 2233-2238.
[http://dx.doi.org/10.1534/g3.113.008847] [PMID: 24122057]
[72]
Wang, Y.; Cheng, X.; Shan, Q.; Zhang, Y.; Liu, J.; Gao, C.; Qiu, J-L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol., 2014, 32(9), 947-951.
[http://dx.doi.org/10.1038/nbt.2969] [PMID: 25038773]
[73]
Shan, Q.; Wang, Y.; Li, J.; Gao, C. Genome editing in rice and wheat using the CRISPR/Cas system. Nat. Protoc., 2014, 9(10), 2395-2410.
[http://dx.doi.org/10.1038/nprot.2014.157] [PMID: 25232936]
[74]
Zhang, Y.; Liang, Z.; Zong, Y.; Wang, Y.; Liu, J.; Chen, K.; Qiu, J-L.; Gao, C. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat. Commun., 2016, 7, 12617.
[http://dx.doi.org/10.1038/ncomms12617] [PMID: 27558837]
[75]
Wang, W.; Akhunova, A.; Chao, S.; Akhunov, E. Optimizing multiplex CRISPR/Cas9-based genome editing for wheat. bioRxiv, 2016, 051342.
[76]
Gil-Humanes, J.; Wang, Y.; Liang, Z.; Shan, Q.; Ozuna, C.V.; Sánchez-León, S.; Baltes, N.J.; Starker, C.; Barro, F.; Gao, C.; Voytas, D.F. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J., 2017, 89(6), 1251-1262.
[http://dx.doi.org/10.1111/tpj.13446] [PMID: 27943461]
[77]
Li, C.; Unver, T.; Zhang, B. A high-efficiency CRISPR/Cas9 system for targeted mutagenesis in Cotton (Gossypium hirsutum L.). Sci. Rep., 2017, 7, 43902.
[http://dx.doi.org/10.1038/srep43902] [PMID: 28256588]
[78]
Chen, X.; Lu, X.; Shu, N.; Wang, S.; Wang, J.; Wang, D.; Guo, L.; Ye, W. Targeted mutagenesis in cotton (Gossypium hirsutum L.) using the CRISPR/Cas9 system. Sci. Rep., 2017, 7, 44304.
[http://dx.doi.org/10.1038/srep44304] [PMID: 28287154]
[79]
Wang, P.; Zhang, J.; Sun, L.; Ma, Y.; Xu, J.; Liang, S.; Deng, J.; Tan, J.; Zhang, Q.; Tu, L.; Daniell, H.; Jin, S.; Zhang, X. High efficient multisites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system. Plant Biotechnol. J., 2018, 16(1), 137-150.
[http://dx.doi.org/10.1111/pbi.12755] [PMID: 28499063]
[80]
Liang, Z.; Zhang, K.; Chen, K.; Gao, C. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J. Genet. Genomics, 2014, 41(2), 63-68.
[http://dx.doi.org/10.1016/j.jgg.2013.12.001] [PMID: 24576457]
[81]
Svitashev, S.; Young, J.K.; Schwartz, C.; Gao, H.; Falco, S.C.; Cigan, A.M. Targeted mutagenesis, precise gene editing and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol., 2015, 169(2), 931-945.
[http://dx.doi.org/10.1104/pp.15.00793] [PMID: 26269544]
[82]
Char, S.N.; Neelakandan, A.K.; Nahampun, H.; Frame, B.; Main, M.; Spalding, M.H.; Becraft, P.W.; Meyers, B.C.; Walbot, V.; Wang, K.; Yang, B. An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol. J., 2017, 15(2), 257-268.
[http://dx.doi.org/10.1111/pbi.12611] [PMID: 27510362]
[83]
Sun, X.; Hu, Z.; Chen, R.; Jiang, Q.; Song, G.; Zhang, H.; Xi, Y. Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci. Rep., 2015, 5, 10342.
[http://dx.doi.org/10.1038/srep10342] [PMID: 26022141]
[84]
Du, H.; Zeng, X.; Zhao, M.; Cui, X.; Wang, Q.; Yang, H.; Cheng, H.; Yu, D. Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J. Biotechnol., 2016, 217, 90-97.
[http://dx.doi.org/10.1016/j.jbiotec.2015.11.005] [PMID: 26603121]
[85]
Brooks, C.; Nekrasov, V.; Lippman, Z.B.; Van Eck, J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol., 2014, 166(3), 1292-1297.
[http://dx.doi.org/10.1104/pp.114.247577] [PMID: 25225186]
[86]
Ito, Y.; Nishizawa-Yokoi, A.; Endo, M.; Mikami, M.; Toki, S. CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem. Biophys. Res. Commun., 2015, 467(1), 76-82.
[http://dx.doi.org/10.1016/j.bbrc.2015.09.117] [PMID: 26408904]
[87]
Čermák, T.; Baltes, N.J.; Čegan, R.; Zhang, Y.; Voytas, D.F. High-frequency, precise modification of the tomato genome. Genome Biol., 2015, 16(1), 232.
[http://dx.doi.org/10.1186/s13059-015-0796-9] [PMID: 26541286]
[88]
Pan, C.; Ye, L.; Qin, L.; Liu, X.; He, Y.; Wang, J.; Chen, L.; Lu, G. CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci. Rep., 2016, 6, 24765.
[http://dx.doi.org/10.1038/srep24765] [PMID: 27097775]
[89]
Jacobs, T.B.; Zhang, N.; Patel, D.; Martin, G.B. Generation of a collection of mutant tomato lines using pooled CRISPR libraries. Plant Physiol., 2017, 174(4), 2023-2037.
[http://dx.doi.org/10.1104/pp.17.00489] [PMID: 28646085]
[90]
Ueta, R.; Abe, C.; Watanabe, T.; Sugano, S.S.; Ishihara, R.; Ezura, H.; Osakabe, Y.; Osakabe, K. Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Sci. Rep., 2017, 7(1), 507.
[http://dx.doi.org/10.1038/s41598-017-00501-4] [PMID: 28360425]
[91]
Veillet, F.; Perrot, L.; Chauvin, L.; Kermarrec, M-P.; Guyon-Debast, A.; Chauvin, J-E.; Nogué, F.; Mazier, M. Transgene-free genome editing in tomato and potato plants using Agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int. J. Mol. Sci., 2019, 20(2), 402.
[http://dx.doi.org/10.3390/ijms20020402] [PMID: 30669298]
[92]
Ren, C.; Liu, Y.; Wang, X.; Guo, Y.; Fan, P.; Li, S.; Liang, Z. Targeted genome editing in Nicotiana tabacum using inducible CRISPR/Cas9 system. bioRxiv, 2020.
[93]
Jansing, J.; Sack, M.; Augustine, S.M.; Fischer, R.; Bortesi, L. CRISPR/Cas9-mediated knockout of six glycosyltransferase genes in Nicotiana benthamiana for the production of recombinant proteins lacking β-1,2-xylose and core α-1,3-fucose. Plant Biotechnol. J., 2019, 17(2), 350-361.
[http://dx.doi.org/10.1111/pbi.12981] [PMID: 29969180]
[94]
Matsuo, K.; Atsumi, G. CRISPR/Cas9-mediated knockout of the RDR6 gene in Nicotiana benthamiana for efficient transient expression of recombinant proteins. Planta, 2019, 250(2), 463-473.
[http://dx.doi.org/10.1007/s00425-019-03180-9] [PMID: 31065786]
[95]
Smith, J.; Bibikova, M.; Whitby, F.G.; Reddy, A.R.; Chandrasegaran, S.; Carroll, D. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Res., 2000, 28(17), 3361-3369.
[http://dx.doi.org/10.1093/nar/28.17.3361] [PMID: 10954606]
[96]
Petolino, J.F. Genome editing in plants via designed zinc finger nucleases. In Vitro Cell. Dev. Biol. Plant, 2015, 51(1), 1-8.
[http://dx.doi.org/10.1007/s11627-015-9663-3] [PMID: 25774080]
[97]
Ramirez, C.L.; Foley, J.E.; Wright, D.A.; Müller-Lerch, F.; Rahman, S.H.; Cornu, T.I.; Winfrey, R.J.; Sander, J.D.; Fu, F.; Townsend, J.A.; Cathomen, T.; Voytas, D.F.; Joung, J.K. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods, 2008, 5(5), 374-375.
[http://dx.doi.org/10.1038/nmeth0508-374] [PMID: 18446154]
[98]
Kang, S.; Jeon, S.; Kim, S.; Chang, Y.K.; Kim, Y-C. Development of a pVEC peptide-based ribonucleoprotein (RNP) delivery system for genome editing using CRISPR/Cas9 in Chlamydomonas reinhardtii. Sci. Rep., 2020, 10(1), 22158.
[http://dx.doi.org/10.1038/s41598-020-78968-x] [PMID: 33335164]
[99]
Zala, H.N.; Bosamia, T.C.; Shukla, Y.M.; Kumar, S.; Kulkarni, K.S. Genome modifications in crops employing engineered nucleases. Agric. Rev. (Karnal), 2016, 37, 154-159.
[http://dx.doi.org/10.18805/ar.v0iof.9629]
[100]
Sun, N.; Zhao, H. Transcription activator-like effector nucleases (TALENs): a highly efficient and versatile tool for genome editing. Biotechnol. Bioeng., 2013, 110(7), 1811-1821.
[http://dx.doi.org/10.1002/bit.24890] [PMID: 23508559]
[101]
Jia, H.; Wang, N. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One, 2014, 9(4), e93806.
[http://dx.doi.org/10.1371/journal.pone.0093806] [PMID: 24710347]
[102]
Hsu, P.D.; Lander, E.S.; Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 2014, 157(6), 1262-1278.
[http://dx.doi.org/10.1016/j.cell.2014.05.010] [PMID: 24906146]
[103]
Larson, M.H.; Gilbert, L.A.; Wang, X.; Lim, W.A.; Weissman, J.S.; Qi, L.S. CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc., 2013, 8(11), 2180-2196.
[http://dx.doi.org/10.1038/nprot.2013.132] [PMID: 24136345]
[104]
Qi, L.S.; Larson, M.H.; Gilbert, L.A.; Doudna, J.A.; Weissman, J.S.; Arkin, A.P.; Lim, W.A. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 2013, 152(5), 1173-1183.
[http://dx.doi.org/10.1016/j.cell.2013.02.022] [PMID: 23452860]
[105]
Cuartero, J.; Bolarín, M.C.; Asíns, M.J.; Moreno, V. Increasing salt tolerance in the tomato. J. Exp. Bot., 2006, 57(5), 1045-1058.
[http://dx.doi.org/10.1093/jxb/erj102] [PMID: 16520333]
[106]
Kumar, V.; Jain, M. The CRISPR-Cas system for plant genome editing: advances and opportunities. J. Exp. Bot., 2015, 66(1), 47-57.
[http://dx.doi.org/10.1093/jxb/eru429] [PMID: 25371501]
[107]
Xie, K.; Yang, Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant, 2013, 6(6), 1975-1983.
[http://dx.doi.org/10.1093/mp/sst119] [PMID: 23956122]
[108]
Zaidi, S.S-A.; Mansoor, S.; Ali, Z.; Tashkandi, M.; Mahfouz, M.M. Engineering plants for geminivirus resistance with CRISPR/Cas9 system. Trends Plant Sci., 2016, 21(4), 279-281.
[http://dx.doi.org/10.1016/j.tplants.2016.01.023] [PMID: 26880316]
[109]
Zhang, Y.; Showalter, A.M. CRISPR/Cas9 genome editing technology: a valuable tool for understanding plant cell wall biosynthesis and function. Front. Plant Sci., 2020, 11, 589517.
[http://dx.doi.org/10.3389/fpls.2020.589517] [PMID: 33329650]
[110]
Jain, M. Function genomics of abiotic stress tolerance in plants: a CRISPR approach. Front. Plant Sci., 2015, 6, 375.
[http://dx.doi.org/10.3389/fpls.2015.00375] [PMID: 26074938]
[111]
Gayatonde, V.; Vennela, P.R. CRISPR-Cas; A potential technique for crop improvement. Biotech Express, 2017, 4(42), 34-38.
[112]
Zaidi, S.S-A.; Mahas, A.; Vanderschuren, H.; Mahfouz, M.M. Engineering crops of the future: CRISPR approaches to develop climate-resilient and disease-resistant plants. Genome Biol., 2020, 21(1), 289.
[http://dx.doi.org/10.1186/s13059-020-02204-y] [PMID: 33256828]
[113]
Bhatta, B.P.; Malla, S. Improving horticultural crops via CRISPR/Cas9: current Successes and Prospects. Plants (Basel), 2020, 9(10), 1360.
[http://dx.doi.org/10.3390/plants9101360] [PMID: 33066510]
[114]
Zhao, H.; Wolt, J.D. Risk associated with off-target plant genome editing and methods for its limitation. Emerg. Top. Life Sci., 2017, 1(2), 231-240.
[http://dx.doi.org/10.1042/ETLS20170037]
[115]
Eş, I.; Gavahian, M.; Marti-Quijal, F.J.; Lorenzo, J.M.; Mousavi Khaneghah, A.; Tsatsanis, C.; Kampranis, S.C.; Barba, F.J. The application of the CRISPR-Cas9 genome editing machinery in food and agricultural science: current status, future perspectives, and associated challenges. Biotechnol. Adv., 2019, 37(3), 410-421.
[http://dx.doi.org/10.1016/j.biotechadv.2019.02.006] [PMID: 30779952]
[116]
Kazan, K. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci., 2015, 20(4), 219-229.
[http://dx.doi.org/10.1016/j.tplants.2015.02.001] [PMID: 25731753]
[117]
Feller, U.; Vaseva, I.I. Extreme climatic events: impacts of drought and high temperature on physiological processes in agronomically important plants. Front. Environ. Sci., 2014, 2, 39.
[http://dx.doi.org/10.3389/fenvs.2014.00039]
[118]
Pathak, M.R.; Teixeira da Silva, J.A.; Wani, S.H. Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food, 2014, 5(2), 87-96.
[http://dx.doi.org/10.4161/gmcr.28774] [PMID: 24710064]
[119]
Postel, S.L. For our thirsty world, efficiency or else. Science, 2006, 313(5790), 1046-1047.
[http://dx.doi.org/10.1126/science.1132334]
[120]
Ahuja, I.; de Vos, R.C.; Bones, A.M.; Hall, R.D. Plant molecular stress responses face climate change. Trends Plant Sci., 2010, 15(12), 664-674.
[http://dx.doi.org/10.1016/j.tplants.2010.08.002] [PMID: 20846898]
[121]
Lu, Y.; Li, Y.; Zhang, J.; Xiao, Y.; Yue, Y.; Duan, L.; Zhang, M.; Li, Z. Overexpression of Arabidopsis molybdenum cofactor sulfurase gene confers drought tolerance in maize (Zea mays L.). PLoS One, 2013, 8(1), e52126.
[http://dx.doi.org/10.1371/journal.pone.0052126] [PMID: 23326325]
[122]
Ouyang, S.Q.; Liu, Y.F.; Liu, P.; Lei, G.; He, S.J.; Ma, B.; Zhang, W.K.; Zhang, J.S.; Chen, S.Y. Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J., 2010, 62(2), 316-329.
[http://dx.doi.org/10.1111/j.1365-313X.2010.04146.x] [PMID: 20128882]
[123]
Giri, J.; Vij, S.; Dansana, P.K.; Tyagi, A.K. Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol., 2011, 191(3), 721-732.
[http://dx.doi.org/10.1111/j.1469-8137.2011.03740.x] [PMID: 21534973]
[124]
Pham, J.; Liu, J.; Bennett, M.H.; Mansfield, J.W.; Desikan, R. Arabidopsis histidine kinase 5 regulates salt sensitivity and resistance against bacterial and fungal infection. New Phytol., 2012, 194(1), 168-180.
[http://dx.doi.org/10.1111/j.1469-8137.2011.04033.x] [PMID: 22256998]
[125]
Tran, L-S.P.; Urao, T.; Qin, F.; Maruyama, K.; Kakimoto, T.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. USA, 2007, 104(51), 20623-20628.
[http://dx.doi.org/10.1073/pnas.0706547105] [PMID: 18077346]
[126]
Higuchi, M.; Pischke, M.S.; Mähönen, A.P.; Miyawaki, K.; Hashimoto, Y.; Seki, M.; Kobayashi, M.; Shinozaki, K.; Kato, T.; Tabata, S.; Helariutta, Y.; Sussman, M.R.; Kakimoto, T. In planta functions of the Arabidopsis cytokinin receptor family. Proc. Natl. Acad. Sci. USA, 2004, 101(23), 8821-8826.
[http://dx.doi.org/10.1073/pnas.0402887101] [PMID: 15166290]
[127]
Shou, H.; Bordallo, P.; Fan, J-B.; Yeakley, J.M.; Bibikova, M.; Sheen, J.; Wang, K. Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc. Natl. Acad. Sci. USA, 2004, 101(9), 3298-3303.
[http://dx.doi.org/10.1073/pnas.0308095100] [PMID: 14960727]
[128]
Ghanem, M.E.; Albacete, A.; Smigocki, A.C.; Frébort, I.; Pospísilová, H.; Martínez-Andújar, C.; Acosta, M.; Sánchez-Bravo, J.; Lutts, S.; Dodd, I.C.; Pérez-Alfocea, F. Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J. Exp. Bot., 2011, 62(1), 125-140.
[http://dx.doi.org/10.1093/jxb/erq266] [PMID: 20959628]
[129]
Habben, J.E.; Bao, X.; Bate, N.J.; DeBruin, J.L.; Dolan, D.; Hasegawa, D.; Helentjaris, T.G.; Lafitte, R.H.; Lovan, N.; Mo, H.; Reimann, K.; Schussler, J.R. Transgenic alteration of ethylene biosynthesis increases grain yield in maize under field drought-stress conditions. Plant Biotechnol. J., 2014, 12(6), 685-693.
[http://dx.doi.org/10.1111/pbi.12172] [PMID: 24618117]
[130]
Kobayashi, F.; Maeta, E.; Terashima, A.; Kawaura, K.; Ogihara, Y.; Takumi, S. Development of abiotic stress tolerance via bZIP-type transcription factor LIP19 in common wheat. J. Exp. Bot., 2008, 59(4), 891-905.
[http://dx.doi.org/10.1093/jxb/ern014] [PMID: 18326864]
[131]
Fowler, D.B.; Breton, G.; Limin, A.E.; Mahfoozi, S.; Sarhan, F. Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol., 2001, 127(4), 1676-1681.
[http://dx.doi.org/10.1104/pp.010483] [PMID: 11743112]
[132]
Poole, R.L. The TAIR database. In: Plant Bioinformatics: Methods and Protocol; Edwards, D., Ed.; Springer Nature: Switzerland, 2007; pp. 179-212.
[133]
Sakuma, Y.; Maruyama, K.; Osakabe, Y.; Qin, F.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell, 2006, 18(5), 1292-1309.
[http://dx.doi.org/10.1105/tpc.105.035881] [PMID: 16617101]
[134]
Sakamoto, H.; Matsuda, O.; Iba, K. ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. Plant J., 2008, 56(3), 411-422.
[http://dx.doi.org/10.1111/j.1365-313X.2008.03614.x] [PMID: 18643991]
[135]
Legnaioli, T.; Cuevas, J.; Mas, P. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J., 2009, 28(23), 3745-3757.
[http://dx.doi.org/10.1038/emboj.2009.297] [PMID: 19816401]
[136]
Zhang, M.; Leng, P.; Zhang, G.; Li, X. Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J. Plant Physiol., 2009, 166(12), 1241-1252.
[http://dx.doi.org/10.1016/j.jplph.2009.01.013] [PMID: 19307046]
[137]
Iuchi, S.; Kobayashi, M.; Taji, T.; Naramoto, M.; Seki, M.; Kato, T.; Tabata, S.; Kakubari, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J., 2001, 27(4), 325-333.
[http://dx.doi.org/10.1046/j.1365-313x.2001.01096.x] [PMID: 11532178]
[138]
Wang, Y.; Beaith, M.; Chalifoux, M.; Ying, J.; Uchacz, T.; Sarvas, C.; Griffiths, R.; Kuzma, M.; Wan, J.; Huang, Y. Shoot-specific down-regulation of protein farnesyltransferase (α-subunit) for yield protection against drought in canola. Mol. Plant, 2009, 2(1), 191-200.
[http://dx.doi.org/10.1093/mp/ssn088] [PMID: 19529821]
[139]
Verslues, P.E.; Bray, E.A. Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J. Exp. Bot., 2006, 57(1), 201-212.
[http://dx.doi.org/10.1093/jxb/erj026] [PMID: 16339784]
[140]
Zeller, G.; Henz, S.R.; Widmer, C.K.; Sachsenberg, T.; Rätsch, G.; Weigel, D.; Laubinger, S. Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J., 2009, 58(6), 1068-1082.
[http://dx.doi.org/10.1111/j.1365-313X.2009.03835.x] [PMID: 19222804]
[141]
Perez, D.E.; Hoyer, J.S.; Johnson, A.I.; Moody, Z.R.; Lopez, J.; Kaplinsky, N.J. BOBBER1 is a noncanonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol., 2009, 151(1), 241-252.
[http://dx.doi.org/10.1104/pp.109.142125] [PMID: 19571304]
[142]
Zhang, H.; Ohyama, K.; Boudet, J.; Chen, Z.; Yang, J.; Zhang, M.; Muranaka, T.; Maurel, C.; Zhu, J-K.; Gong, Z. Dolichol biosynthesis and its effects on the unfolded protein response and abiotic stress resistance in Arabidopsis. Plant Cell, 2008, 20(7), 1879-1898.
[http://dx.doi.org/10.1105/tpc.108.061150] [PMID: 18612099]
[143]
Magome, H.; Yamaguchi, S.; Hanada, A.; Kamiya, Y.; Oda, K. The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J., 2008, 56(4), 613-626.
[http://dx.doi.org/10.1111/j.1365-313X.2008.03627.x] [PMID: 18643985]
[144]
Allagulova, ChR.; Gimalov, F.R.; Shakirova, F.M.; Vakhitov, V.A. The plant dehydrins: structure and putative functions. Biochemistry (Mosc.), 2003, 68(9), 945-951.
[http://dx.doi.org/10.1023/A:1026077825584] [PMID: 14606934]
[145]
Rampino, P.; Pataleo, S.; Gerardi, C.; Mita, G.; Perrotta, C. Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant Cell Environ., 2006, 29(12), 2143-2152.
[http://dx.doi.org/10.1111/j.1365-3040.2006.01588.x] [PMID: 17081248]
[146]
Zhou, Q.Y.; Tian, A.G.; Zou, H.F.; Xie, Z.M.; Lei, G.; Huang, J.; Wang, C.M.; Wang, H.W.; Zhang, J.S.; Chen, S.Y. Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol. J., 2008, 6(5), 486-503.
[http://dx.doi.org/10.1111/j.1467-7652.2008.00336.x] [PMID: 18384508]
[147]
Mishkind, M.; Vermeer, J.E.; Darwish, E.; Munnik, T. Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J., 2009, 60(1), 10-21.
[http://dx.doi.org/10.1111/j.1365-313X.2009.03933.x] [PMID: 19500308]
[148]
Werner, T.; Nehnevajova, E.; Köllmer, I.; Novák, O.; Strnad, M.; Krämer, U.; Schmülling, T. Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell, 2010, 22(12), 3905-3920.
[http://dx.doi.org/10.1105/tpc.109.072694] [PMID: 21148816]
[149]
Zhang, Z.; Wang, Y.; Chang, L.; Zhang, T.; An, J.; Liu, Y.; Cao, Y.; Zhao, X.; Sha, X.; Hu, T.; Yang, P. MsZEP, a novel zeaxanthin epoxidase gene from alfalfa (Medicago sativa), confers drought and salt tolerance in transgenic tobacco. Plant Cell Rep., 2016, 35(2), 439-453.
[http://dx.doi.org/10.1007/s00299-015-1895-5] [PMID: 26573680]
[150]
Zhang, Q.; Li, J.; Zhang, W.; Yan, S.; Wang, R.; Zhao, J.; Li, Y.; Qi, Z.; Sun, Z.; Zhu, Z. The putative auxin efflux carrier OsPIN3t is involved in the drought stress response and drought tolerance. Plant J., 2012, 72(5), 805-816.
[http://dx.doi.org/10.1111/j.1365-313X.2012.05121.x] [PMID: 22882529]
[151]
Fujii, H.; Zhu, J-K. An autophosphorylation site of the protein kinase SOS2 is important for salt tolerance in Arabidopsis. Mol. Plant, 2009, 2(1), 183-190.
[http://dx.doi.org/10.1093/mp/ssn087] [PMID: 19529820]
[152]
Im, Y.J.; Ji, M.; Lee, A.; Killens, R.; Grunden, A.M.; Boss, W.F. Expression of Pyrococcus furiosus superoxide reductase in Arabidopsis enhances heat tolerance. Plant Physiol., 2009, 151(2), 893-904.
[http://dx.doi.org/10.1104/pp.109.145409] [PMID: 19684226]
[153]
Halliwell, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol., 2006, 141(2), 312-322.
[http://dx.doi.org/10.1104/pp.106.077073] [PMID: 16760481]
[154]
Osakabe, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L-S.P. Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J. Exp. Bot., 2013, 64(2), 445-458.
[http://dx.doi.org/10.1093/jxb/ers354] [PMID: 23307915]
[155]
Marshall, A.; Aalen, R.B.; Audenaert, D.; Beeckman, T.; Broadley, MR.; Butenko, M.A.; Caño-Delgado, A.I.; de Vries, S.; Dresselhaus, T.; Felix, G.; Graham, N.S.; Foulkes, J.; Granier, C.; Greb, T.; Grossniklaus, U.; Hammond, J.P.; Heidstra, R.; Hodgman, C.; Hothorn, M.; Inzé, D.; Ostergaard, L.; Russinova, E.; Simon, R.; Skirycz, A.; Stahl, Y.; Zipfel, C.; De Smet, I. Tackling drought stress: receptor-like kinases present new approaches. Plant Cell, 2012, 24(6), 2262-2278.
[http://dx.doi.org/10.1105%2Ftpc.112.096677] [PMID: 22693282]
[156]
Osakabe, Y.; Maruyama, K.; Seki, M.; Satou, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell, 2005, 17(4), 1105-1119.
[http://dx.doi.org/10.1105/tpc.104.027474] [PMID: 15772289]
[157]
Osakabe, Y.; Mizuno, S.; Tanaka, H.; Maruyama, K.; Osakabe, K.; Todaka, D.; Fujita, Y.; Kobayashi, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J. Biol. Chem., 2010, 285(12), 9190-9201.
[http://dx.doi.org/10.1074/jbc.M109.051938] [PMID: 20089852]
[158]
Hua, D.; Wang, C.; He, J.; Liao, H.; Duan, Y.; Zhu, Z.; Guo, Y.; Chen, Z.; Gong, Z. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell, 2012, 24(6), 2546-2561.
[http://dx.doi.org/10.1105/tpc.112.100107] [PMID: 22730405]
[159]
Nongpiur, R.; Soni, P.; Karan, R.; Singla-Pareek, S.L.; Pareek, A. Histidine kinases in plants: cross talk between hormone and stress responses. Plant Signal. Behav., 2012, 7(10), 1230-1237.
[http://dx.doi.org/10.4161/psb.21516] [PMID: 22902699]
[160]
Teige, M.; Scheikl, E.; Eulgem, T.; Dóczi, R.; Ichimura, K.; Shinozaki, K.; Dangl, J.L.; Hirt, H. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell, 2004, 15(1), 141-152.
[http://dx.doi.org/10.1016/j.molcel.2004.06.023] [PMID: 15225555]
[161]
Yamaguchi-Shinozaki, K.; Shinozaki, K. Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci., 2005, 10(2), 88-94.
[http://dx.doi.org/10.1016/j.tplants.2004.12.012] [PMID: 15708346]
[162]
Yoshida, T.; Fujita, Y.; Sayama, H.; Kidokoro, S.; Maruyama, K.; Mizoi, J.; Shinozaki, K.; Yamaguchi-Shinozaki, K. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J., 2010, 61(4), 672-685.
[http://dx.doi.org/10.1111/j.1365-313X.2009.04092.x] [PMID: 19947981]
[163]
Oh, S-J.; Song, S.I.; Kim, Y.S.; Jang, H-J.; Kim, S.Y.; Kim, M.; Kim, Y-K.; Nahm, B.H.; Kim, J-K. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol., 2005, 138(1), 341-351.
[http://dx.doi.org/10.1104/pp.104.059147] [PMID: 15834008]
[164]
Abe, H.; Urao, T.; Ito, T.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell, 2003, 15(1), 63-78.
[http://dx.doi.org/10.1105/tpc.006130] [PMID: 12509522]
[165]
Seo, P.J.; Lee, S.B.; Suh, M.C.; Park, M-J.; Go, Y.S.; Park, C-M. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell, 2011, 23(3), 1138-1152.
[http://dx.doi.org/10.1105/tpc.111.083485] [PMID: 21398568]
[166]
Lippold, F.; Sanchez, D.H.; Musialak, M.; Schlereth, A.; Scheible, W-R.; Hincha, D.K.; Udvardi, M.K. AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. Plant Physiol., 2009, 149(4), 1761-1772.
[http://dx.doi.org/10.1104/pp.108.134874] [PMID: 19211694]
[167]
Fahad, S.; Hussain, S.; Bano, A.; Saud, S.; Hassan, S.; Shan, D.; Khan, F.A.; Khan, F.; Chen, Y.; Wu, C.; Tabassum, M.A.; Chun, M.X.; Afzal, M.; Jan, A.; Jan, M.T.; Huang, J. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ. Sci. Pollut. Res. Int., 2015, 22(7), 4907-4921.
[http://dx.doi.org/10.1007/s11356-014-3754-2] [PMID: 25369916]
[168]
Himmelbach, A.; Yang, Y.; Grill, E. Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol., 2003, 6(5), 470-479.
[http://dx.doi.org/10.1016/S1369-5266(03)00090-6] [PMID: 12972048]
[169]
Verslues, P.E.; Zhu, J-K. New developments in abscisic acid perception and metabolism. Curr. Opin. Plant Biol., 2007, 10(5), 447-452.
[http://dx.doi.org/10.1016/j.pbi.2007.08.004] [PMID: 17875396]
[170]
Qin, X.; Zeevaart, J.A. Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol., 2002, 128(2), 544-551.
[http://dx.doi.org/10.1104/pp.010663] [PMID: 11842158]
[171]
Ma, Q-H. Genetic engineering of cytokinins and their application to agriculture. Crit. Rev. Biotechnol., 2008, 28(3), 213-232.
[http://dx.doi.org/10.1080/07388550802262205] [PMID: 18855152]
[172]
Huynh, N.; Vantoai, T.; Streeter, J.; Banowetz, G. Regulation of flooding tolerance of SAG12:ipt Arabidopsis plants by cytokinin. J. Exp. Bot., 2005, 56(415), 1397-1407.
[http://dx.doi.org/10.1093/jxb/eri141] [PMID: 15797940]
[173]
Rivero, R.M.; Shulaev, V.; Blumwald, E. Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol., 2009, 150(3), 1530-1540.
[http://dx.doi.org/10.1104/pp.109.139378] [PMID: 19411371]
[174]
Krishna, P. Brassinosteroid-mediated stress responses. J. Plant Growth Regul., 2003, 22(4), 289-297.
[http://dx.doi.org/10.1007/s00344-003-0058-z] [PMID: 14676968]
[175]
Hayat, S.; Maheshwari, P.; Wani, A.S.; Irfan, M.; Alyemeni, M.N.; Ahmad, A. Comparative effect of 28 homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L. Plant Physiol. Biochem., 2012, 53, 61-68.
[http://dx.doi.org/10.1016/j.plaphy.2012.01.011] [PMID: 22322250]
[176]
Divi, U.K.; Krishna, P. Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. N. Biotechnol., 2009, 26(3-4), 131-136.
[http://dx.doi.org/10.1016/j.nbt.2009.07.006] [PMID: 19631770]
[177]
Khatodia, S.; Bhatotia, K.; Passricha, N.; Khurana, S.M.; Tuteja, N. The CRISPR/Cas genome-editing tool: application in improvement of crops. Front. Plant Sci., 2016, 7, 506.
[http://dx.doi.org/10.3389/fpls.2016.00506] [PMID: 27148329]
[178]
Sharma, S.; Kaur, R.; Singh, A. Recent advances in CRISPR/Cas mediated genome editing for crop improvement. Plant Biotechnol. Rep., 2017, 11, 193-207.
[http://dx.doi.org/10.1007/s11816-017-0446-7]
[179]
Globus, R.; Qimron, U. A Technological and regulatory outlook on CRISPR crop editing. J. Cell. Biochem., 2018, 119(2), 1291-1298.
[PMID: 28731201]
[180]
Zetsche, B.; Volz, S.E.; Zhang, F. A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat. Biotechnol., 2015, 33(2), 139-142.
[http://dx.doi.org/10.1038/nbt.3149] [PMID: 25643054]
[181]
Polstein, L.R.; Gersbach, C.A. A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat. Chem. Biol., 2015, 11(3), 198-200.
[http://dx.doi.org/10.1038/nchembio.1753] [PMID: 25664691]
[182]
Gao, P.; Bai, X.; Yang, L.; Lv, D.; Pan, X.; Li, Y.; Cai, H.; Ji, W.; Chen, Q.; Zhu, Y. osa-MIR393: a salinity- and alkaline stress-related microRNA gene. Mol. Biol. Rep., 2011, 38(1), 237-242.
[http://dx.doi.org/10.1007/s11033-010-0100-8] [PMID: 20336383]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy