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Multigene CRISPR/Cas9 genome editing of hybrid proline rich proteins (HyPRPs) for sustainable multi-stress tolerance in crops: the review of a promising approach

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Abstract

The recent global climate change has directly impacted major biotic and abiotic stress factors affecting crop productivity worldwide. Therefore, the need of the hour is to develop sustainable multiple stress tolerant crops through modern biotechnological approaches to cope with climate change. Hybrid proline rich proteins (HyPRPs) are the cell-wall structural proteins, which contain an N-terminal repetitive proline-rich domain and a C-terminal conserved eight-cysteine motif domain. HyPRPs are known to regulate multiple abiotic and biotic stress responses in plants. Recently, a few HyPRPs have been characterized as negative regulators of abiotic and biotic stress responses in different plants. Disruption of such negative regulators for desirable positive phenotypic traits has been made possible through the advent of advanced genome engineering tools. In the past few years, CRISPR/Cas9 has emerged as a novel breakthrough technology for crop improvement by target specific editing of known negative regulatory host genes. Here, we have described the mechanism of action and the role of known HyPRPs in regulating different biotic and abiotic stress responses in major crop plants. We have also discussed the importance of the CRISPR/Cas9 based genome editing system in targeting known negative regulatory HyPRPs for multi-stress crop tolerance using the tomato crop model. Application of genome editing to manipulate the HyPRPs of major crop plants holds promise in developing newer stress management methods in this rapidly changing climate and would lead in the future to sustain crop productivity.

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References

  • Abdallah NA, Moses V, Prakash C (2014) The impact of possible climate changes on developing countries. GM Crops Food 5:77–80

    Article  PubMed  PubMed Central  Google Scholar 

  • Ábrahám E, Hourton-Cabassa C, Erdei L, Szabados L (2010) Methods for determination of proline in plants. In: Sunkar R (ed) Plant stress tolerance. Methods in molecular biology (methods and protocols), vol 639. Humana Press

  • Abudayyeh OO, Gootenberg JS, Essletzbichler P et al (2017) RNA targeting with CRISPR-Cas13. Nature 550:280–284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aman R, Ali Z, Butt H et al (2018) RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol 19:1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amitai G, Sorek R (2016) CRISPR-Cas adaptation: insights into the mechanism of action. Nat Rev Microbiol 14:67–76

    Article  CAS  PubMed  Google Scholar 

  • Anders C, Niewoehner O, Duerst A, Jinek M (2014) Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513:569–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersson M, Turesson H, Olsson N, Fält AS, Olsson P et al (2018) Genome editing in potato via CRISPR-Cas9 ribonucleoprotein delivery. Physiol Plant 164:378–384

    Article  CAS  PubMed  Google Scholar 

  • Bari VK, Nassar JA, Kheredin SM et al (2019) CRISPR/Cas9-mediated mutagenesis of CAROTENOID CLEAVAGE DIOXYGENASE 8 in tomato provides resistance against the parasitic weed Phelipanche aegyptiaca. Sci Rep 9:11438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barrangou R, Fremaux C, Deveau H et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    Article  CAS  PubMed  Google Scholar 

  • Bastola DR, Pethe VV, Winicov I (1998) Alfin1, a novel zinc-finger protein in alfalfa roots that binds to promoter elements in the salt-inducible MsPRP2 gene. Plant Mol Biol 38:1123–1135

    Article  CAS  PubMed  Google Scholar 

  • Belhaj K, Chaparro-Garcia A, Kamoun S et al (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Met 9:39

    Article  CAS  Google Scholar 

  • Bernabe-Orts JM, Casas-Rodrigo I, Minguet EG et al (2019) Assessment of Cas12a-mediated gene editing efficiency in plants. Plant Biotechnol J 17:1971–1984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernhardt C, Tierney ML (2000) Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiol 122(3):705–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bin Moon S, Lee JM, Kang JG et al (2018) Highly efficient genome editing by CRISPR-Cpf1 using CRISPR RNA with a uridinylate-rich 3′-overhang. Nat Commun 9:3651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333:1843–1846

    Article  CAS  PubMed  Google Scholar 

  • Boron AK, Orden JV, Markakis MN, Mouille GA, Dirk V et al (2014) Proline-rich protein-like PRPL1 controls elongation of root hairs in Arabidopsis thaliana. J Exp Bot 65:5485–5495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breseghello F, Coelho ASG (2013) Traditional and modern plant breeding methods with examples in rice (Oryza sativa L.). J Agric Food Chem 61:8277–8286

    Article  CAS  PubMed  Google Scholar 

  • Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166:1292–1297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carroll D (2011) Genome engineering with zinc-finger nucleases. Genetics 188:773–782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chikkaputtaiah C, Debbarma J, Baruah I et al (2017) Molecular genetics and functional genomics of abiotic stress-responsive genes in oilseed rape (Brassica napus L.): a review of recent advances and future. Plant Biotechnol Rep 11:365–384

    Article  Google Scholar 

  • Clasen BM, Stoddard TJ, Luo S, Demorest ZL et al (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176

    Article  CAS  PubMed  Google Scholar 

  • Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B: Biol Sci 363:557–572

    Article  CAS  Google Scholar 

  • D’Ambrosio C, Stigliani AL, Giorio G (2018) CRISPR/Cas9 editing of carotenoid genes in tomato. Trans Res 27:367–378

    Article  CAS  Google Scholar 

  • Davies JP, Kumar S, Sastry-Dent L (2017) Use of zinc-finger nucleases for crop improvement program. Mol Biol Trans Sci 149:47–63

    Article  CAS  Google Scholar 

  • Debbarma J, Sarki YN, Saikia B et al (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

    Article  CAS  PubMed  Google Scholar 

  • Deltcheva E, Chylinski K, Sharma CM et al (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deutch CE, Winicov I (1995) Post-transcriptional regulation of a salt-inducible alfalfa gene encoding a putative chimeric proline-rich cell wall protein. Plant Mol Biol 37017:411–418

    Article  Google Scholar 

  • Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096

    Article  PubMed  CAS  Google Scholar 

  • Dvorakova L, Cvckova F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genom 16:1–16

    Google Scholar 

  • Feng Z, Mao Y, Xu N et al (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA 111:4632–4637

    Article  CAS  PubMed  Google Scholar 

  • Forsyth A, Weeks T, Richael C, Duan H (2016) Transcription activator-like effector nucleases (TALEN)-mediated targeted DNA insertion in potato plants. Front Plant Sci 7:1572

    Article  PubMed  PubMed Central  Google Scholar 

  • Fowler TJ, Bernhardt C, Tierney ML (1999) Characterization and expression of four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins 1. Plant Physiol 121:1081–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentes A, Carlos N, Ruiz Y et al (2016) Field trial and molecular characterization of RNAi-transgenic tomato plants that exhibit resistance to tomato yellow leaf curl geminivirus. Mol Plant-Microbe Interact 29:197–209

    Article  CAS  PubMed  Google Scholar 

  • Gaj T, Gersbach C, Barbas CF III (2013) ZFN, TALEN and CRISPR/Cas-based methods for genome engineering. Trend Biotecnol 31:397–405. https://doi.org/10.1016/j.tibtech.2013.04.004.ZFN

    Article  CAS  Google Scholar 

  • Gangwani L, Mikrut M, Galcheva-gargova Z, Davis RJ (1998) Interaction of ZPR1 with translation elongation factor-1 in proliferating cells. J Cell Biol 143:1471–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao L, Cox DBT, Yan WX et al (2017) Engineered Cpf1 variants with altered PAM specificities. Nat Biotechnol 35:789–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilchrist E, Haughn G (2010) Reverse genetics techniques: engineering loss and gain of gene function in plants. Brief Funct Genom 9:103–110

    Article  CAS  Google Scholar 

  • Godfray HCJ, Crute IR, Haddad L et al (2010) The future of the global food system. Philos Trans R Soc Lond Ser B Biol Sci 365:2769–2777

    Article  Google Scholar 

  • Goodwin W, Pallas JA, Jenkins GI (1996) Transcripts of a gene encoding a putative cell wall-plasma membrane linker protein are specifically cold-induced in Brassica napus. Plant Mol Biol 31:771–781

    Article  CAS  PubMed  Google Scholar 

  • Gothandam KM, Flower RÁ (2010) OsPRP3, a flower specific proline-rich protein of rice, determines extracellular matrix structure of floral organs and its overexpression confers cold-tolerance. Plant Mol Biol 72:125–135

    Article  CAS  PubMed  Google Scholar 

  • Gujjar RS, Karkute S, Rai A (2018) Proline-rich proteins may regulate free cellular proline levels during drought stress in tomato. Curr Sci 114:915–920

    Article  CAS  Google Scholar 

  • Gupta RM, Musunuru K (2014) The emergence of genome-editing technology: ZFNs, TALENs, and CRISPR-Cas9. J Clin Investig 124:4154–4161

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Teng K, Nawaz G et al (2019) Generation of semi-dwarf rice (Oryza sativa L.) lines by CRISPR/Cas9-directed mutagenesis of OsGA20ox2 and proteomic analysis of unveiled changes caused by mutations. 3 Biotech 9:387

    Article  PubMed  Google Scholar 

  • He CY, Zhang JS, Chen SY (2002) A soybean gene encoding a proline-rich protein is regulated by salicylic acid, an endogenous circadian rhythm and by various stresses. Theor Appl Genet 104:1125–1131

    Article  CAS  PubMed  Google Scholar 

  • He Y, Zhu M, Wang L et al (2018) Programmed self-elimination of the CRISPR/Cas9 construct greatly accelerates the isolation of edited and transgene-free rice plants. Mol Plant 11:1210–1213

    Article  CAS  PubMed  Google Scholar 

  • Heler R, Marraffini LA, Bikard D (2014) Adapting to new threats: the generation of memory by CRISPR-Cas immune systems. Mol Microbiol 93:1–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano S, Nishimasu H, Ishitani R, Nureki O (2016) Structural basis for the altered PAM specificities of engineered CRISPR-Cas9. Mol Cell 61:886–894

    Article  CAS  PubMed  Google Scholar 

  • Horvath P, Romero DA, Coute-Monvoisin A-C et al (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190:1401–1412

    Article  CAS  PubMed  Google Scholar 

  • Hsu C-T, Cheng Y-J, Yuan Y-H et al (2019) Application of Cas12a and nCas9-activation-induced cytidine deaminase for genome editing and as a non-sexual strategy to generate homozygous/multiplex edited plants in the allotetraploid genome of tobacco. Plant Mol Biol 101:355–371

    Article  CAS  PubMed  Google Scholar 

  • Hu N, Xian Z, Li N et al (2019) Rapid and user-friendly open-source CRISPR/Cas9 system for single- or multi-site editing of tomato genome. Hort Res 6:1–14

    Article  CAS  Google Scholar 

  • Huang G, Gong S, Xu W, Li P et al (2011) GhHyPRP4, a cotton gene encoding putative hybrid proline-rich protein is preferentially expressed in leaves and involved in plant response to cold stress. Acta Biochim Biophys Sin 43:519–527

    Article  CAS  PubMed  Google Scholar 

  • Javier M, Susana U, Giusto NM et al (2016) Saline and osmotic stresses stimulate PLD/diacylglycerol kinase activities and increase the level of phosphatidic acid and proline in barley roots. Environ Exp Bot. 128:69–78

    Article  CAS  Google Scholar 

  • Jinek M, Jiang F, Taylor DW et al (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343:1247997

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jose M (2005) Expression of the promoter of HyPRP, an embryo-specific gene from Zea mays in maize and tobacco transgenic plants. Gene 356:146–152

    Article  CAS  Google Scholar 

  • Josè-estanyol M, Puigdomènech P (2000) Plant cell wall glycoproteins and their genes. Plant Physiol Biochem 38:97–108

    Article  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324(5923):89–91

    Article  PubMed  CAS  Google Scholar 

  • Khan AO, White CW, Pike JA et al (2019) Optimised insert design for improved single-molecule imaging and quantification through CRISPR-Cas9 mediated knock-in. Sci Rep 9:14219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim H, Kim ST, Ryu J, Kang BC et al (2017) CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat Commun 8:14406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Alptekin B, Budak H (2018) CRISPR/Cas9 genome editing in wheat. Funct Integr Genom 18:31–41

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krumbach K, Sonntag CK, Eggeling L, Marienhagen J (2019) CRISPR/Cas12a mediated genome editing to introduce amino acid substitutions into the mechanosensitive channel MscCG of Corynebacterium glutamicum. ACS Synth Biol 8:2726–2734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Front Chem 6:1–14

    Article  CAS  Google Scholar 

  • Lee JK, Jeong E, Lee J et al (2018) Directed evolution of CRISPR-Cas9 to increase its specificity. Nat Commun 9:3048

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li J, Ouyang B, Wang T et al (2016) HyPRP1 gene suppressed by multiple stresses plays a negative role in abiotic stress tolerance in tomato. Front Plant Sci 7:1–14

    Google Scholar 

  • Li R, Liu C, Zhao R et al (2019) CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol 19:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang Z, Chen K, Li T et al (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:14261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang M, Li Z, Wang W et al (2019) A CRISPR-Cas12a-derived biosensing platform for the highly sensitive detection of diverse small molecules. Nat Commun 10:3672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lindbo JA (2012) A historical overview of RNAi in plants. Methods Mol Biol 894:1–16

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Chen X, Liu J, Ye J, Guo Z (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63:3899–3912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Sultan MARF, Liu XL et al (2015) Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum). PLoS ONE 10:1–29

    Google Scholar 

  • Liu H, Ding Y, Zhou Y et al (2017) CRISPR-P 2.0: an improved CRISPR-Cas9 tool for genome editing in plants. Mol Plant 10:530–532

    Article  CAS  PubMed  Google Scholar 

  • Makarova KS, Wolf YI, Alkhnbashi OS et al (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manghwar H, Lindsey K, Zhang X, Jin S (2019) CRISPR/Cas system: recent advances and future prospects for genome editing. Trends Plant Sci 24:1102–1125

    Article  CAS  PubMed  Google Scholar 

  • Marraffini LA (2015) CRISPR-Cas immunity in prokaryotes. Nature 526:55–61

    Article  CAS  PubMed  Google Scholar 

  • Marwein R, Debbarma J, Sarki YN, Baruah I et al (2019) Genetic engineering/genome editing approaches to modulate signaling processes in abiotic stress tolerance. In: Iqbal M (ed) Plant signaling molecules. Elsevier, Amsterdam, pp 63–82

    Chapter  Google Scholar 

  • Mellacheruvu S, Tamirisa S, Vudem DR, Khareedu VR (2016) Pigeonpea hybrid-proline-rich protein (CcHyPRP) confers biotic and abiotic stress tolerance in transgenic rice. Front Plant Sci 6:1–13

    Article  Google Scholar 

  • Mojica FJM, Rodriguez-Valera F (2016) The discovery of CRISPR in archaea and bacteria. FEBS J 283:3162–3169

    Article  CAS  PubMed  Google Scholar 

  • Musunuru K (2017) Genome editing: the recent history and perspective in cardiovascular diseases. J Am Coll Cardiol 70:2808–2821

    Article  PubMed  PubMed Central  Google Scholar 

  • Nadakuduti SS, Buell CR, Voytas D, Starker C et al (2018) Genome editing for crop improvement—applications in clonally propagated polyploids with a focus on potato (Solanum tuberosum L.). Front Plant Sci 9:1607

    Article  PubMed  PubMed Central  Google Scholar 

  • Neto LB, De Oliveira RR, Wiebke-strohm B et al (2013) Identification of the soybean HyPRP family and specific gene response to Asian soybean rust disease. Genet Mol Biol 224:214–224

    Article  Google Scholar 

  • Otte O, Barz W (2000) Characterization and oxidative in vitro cross-linking of an extensin-like protein and a proline-rich protein purified from chickpea cell walls. Phytochemistry 53:1–5

    Article  CAS  PubMed  Google Scholar 

  • Pan C, Ye L, Qin L et al (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:2–10

    Article  CAS  Google Scholar 

  • Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537

    PubMed  PubMed Central  Google Scholar 

  • Peer R, Rivlin G, Golobovitch S et al (2015) Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees. Planta 241:941–951

    Article  CAS  PubMed  Google Scholar 

  • Peng T, Jia M-M, Liu J-H (2015) RNAi-based functional elucidation of PtrPRP, a gene encoding a hybrid proline rich protein, in cold tolerance of Poncirus trifoliata. Front Plant Sci 6:1–12

    Google Scholar 

  • Peters K, Breitsameter L, Gerowitt B (2014) Impact of climate change on weeds in agriculture: a review. Agron Sustain Dev 34:707–721

    Article  Google Scholar 

  • Priyanka B, Sekhar K, Reddy VD, Rao KV (2010) Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol J 8:76–87

    Article  CAS  PubMed  Google Scholar 

  • Puchta H (2017) Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Curr Opin Plant Biol 36:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ramu VS, Swetha TN, Sheela SH et al (2016) Simultaneous expression of regulatory genes associated with specific drought-adaptive traits improves drought adaptation in peanut. Plant Biotechnol J 14:1008–1020

    Article  CAS  PubMed  Google Scholar 

  • Ran Y, Patron N, Kay P et al (2018) Zinc finger nuclease-mediated precision genome editing of an endogenous gene in hexaploid bread wheat (Triticum aestivum) using a DNA repair template. Plant Biotechnol J 16:2088–2101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruchita S, Rohit S (2017) Effect of global warming on Indian agriculture. J Climatol Weather Forecast 5:1–5

    Google Scholar 

  • Sanchez-Leon S, Gil-Humanes J, Ozuna CV et al (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16:902–910

    Article  CAS  PubMed  Google Scholar 

  • Schiml S, Fauser F, Puchta H (2016) CRISPR/Cas-mediated site-specific mutagenesis in Arabidopsis thaliana using Cas9 nucleases and paired nickases. Methods Mol Biol 1469:111–122

    Article  CAS  PubMed  Google Scholar 

  • Selma S, Bernabe-Orts JM, Vazquez-Vilar M et al (2019) Strong gene activation in plants with genome-wide specificity using a new orthogonal CRISPR/Cas9-based programmable transcriptional activator. Plant Biotechnol J 17:1703–1705

    PubMed  PubMed Central  Google Scholar 

  • Shan Q, Wang Y, Li J et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotecnol 31:686–688

    Article  CAS  Google Scholar 

  • Shan Q, Baltes NJ, Atkins P et al (2018) ZFN, TALEN and CRISPR-Cas9 mediated homology directed gene insertion in Arabidopsis: a disconnect between somatic and germinal cells. J Genet Genom 45:681–684

    Article  Google Scholar 

  • Shmakov S, Abudayyeh OO, Makarova KS et al (2015) Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol Cell 60:385–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh D, Chaudhary S, Kumar R et al (2016) RNA interference technology—applications and limitations. InTech, Croatia

    Book  Google Scholar 

  • Soyars CL, Peterson BA, Burr CA, Nimchuk ZL (2018) Cutting edge genetics: CRISPR/Cas9 editing of plant genomes. Plant Cell Physiol 59:1608–1620

    Article  CAS  PubMed  Google Scholar 

  • Sundaresan S, Philosoph-hadas S, Ma C et al (2018) The tomato hybrid proline-rich protein regulates the abscission zone competence to respond to ethylene signals. Hortic Res 5:28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan J, Zhuo C, Guo Z (2013) Nitric oxide mediates cold- and dehydration-induced expression of a novel MfHyPRP that confers tolerance to abiotic stress. Physiol Plant 149(3):310–320

    CAS  PubMed  Google Scholar 

  • Tang X, Lowder LG, Zhang T et al (2017) A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants 3:17103

    Article  PubMed  Google Scholar 

  • Tian S, Jiang L, Gao Q et al (2017) Efficient CRISPR/Cas9-based gene knockout in watermelon. Plant Cell Rep 36:399–406

    Article  CAS  PubMed  Google Scholar 

  • Veillet F, Perrot L, Chauvin L et al (2019) Transgene-free genome editing in tomato and potato plants using Agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int J Mol Sci 20:402

    Article  PubMed Central  CAS  Google Scholar 

  • Weyman PD, Pan Z, Feng Q, Gilchrist DG, Bostock RM (2006) DEA 1, a circadian- and cold-regulated tomato gene, protects yeast cells from freezing death. Plant Mol Biol 62(4–5):547–559

    Article  CAS  PubMed  Google Scholar 

  • Winicov I, Bastola DR (1999) Transgenic overexpression of the transcription factor Alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants 1. Plant Physiol 120:473–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolter F, Puchta H (2018) The CRISPR/Cas revolution reaches the RNA world: Cas13, a new Swiss Army knife for plant biologists. Plant J Cell Mol Biol 94:767–775

    Article  CAS  Google Scholar 

  • Wu X, Scott DA, Kriz AJ et al (2014) Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat Biotechnol 32:670–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao G, Zhang S, Liang Z et al (2019) Identification of Mycobacterium abscessus species and subspecies using the Cas12a/sgRNA-based nucleic acid detection platform. Eur J Clin Microbiol Infect Dis. https://doi.org/10.1007/s10096-019-03757-y

    Article  PubMed  Google Scholar 

  • Yan WX, Mirzazadeh R, Garnerone S et al (2017) BLISS is a versatile and quantitative method for genome-wide profiling of DNA double-strand breaks. Nat Commun 8:15058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Zhang Y, Wang X et al (2018) HyPRP1 performs a role in negatively regulating cotton resistance to V. dahliae via the thickening of cell walls and ROS accumulation. BMC Plant 1–18:339

    Article  CAS  Google Scholar 

  • Yeom S, Seo E, Oh S et al (2012) A common plant cell-wall protein HyPRP1 has dual roles as a positive regulator of cell death and a negative regulator of basal defense against pathogens. Plant J 69:755–768

    Article  CAS  PubMed  Google Scholar 

  • Zaidi SS-E-A, Mahfouz MM, Mansoor S (2017) CRISPR-Cpf1: a new tool for plant genome editing. Trends Plant Sci 22:550–553

    Article  CAS  PubMed  Google Scholar 

  • Zegaoui Z, Boumediene TH, Planchais S (2017) Variation in relative water content, proline accumulation and stress gene expression in two cowpea landraces under drought. J Plant Physiol 218:26–34

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Liang Z, Zong Y et al (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Zhang R, Gao J et al (2019) Highly efficient and heritable targeted mutagenesis in wheat via the Agrobacterium tumefaciens-mediated CRISPR/Cas9 system. Int J Mol Sci 20:4257

    Article  CAS  PubMed Central  Google Scholar 

  • Zhou J, Xin X, He Y et al (2019) Multiplex QTL editing of grain-related genes improves yield in elite rice varieties. Plant Cell Rep 38:475–485

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Authors would like to acknowledge Science and Engineering Research Board (SERB), Govt. of India for the financial support to C. C. in the form of Ramanujan Fellowship (SB/S2/RJN-078/2014) and Early Career Research Award (ECR/2016/001288).

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Authors and Affiliations

  1. Biological Sciences and Technology Division, CSIR-North East Institute of Science and Technology (CSIR-NEIST), Jorhat, Assam, 785006, India

    Banashree Saikia, Sanjay Singh, Johni Debbarma, Hariprasanna Dekaboruah & Channakeshavaiah Chikkaputtaiah

  2. Academy of Scientific and Innovative Research (AcSIR), CSIR-NEIST Campus, Jorhat, Assam, 785006, India

    Banashree Saikia, Johni Debbarma, Natarajan Velmurugan, Hariprasanna Dekaboruah & Channakeshavaiah Chikkaputtaiah

  3. Biological Sciences Division, Branch Laboratory-Itanagar, CSIR-NEIST, Naharlagun, Arunachal Pradesh, 791110, India

    Natarajan Velmurugan

  4. Central Muga Eri Research and Training Institute (CMER&TI), Lahdoigarh, Jorhat, Assam, 785700, India

    Kallare P. Arunkumar

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  2. Sanjay Singh
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  3. Johni Debbarma
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  4. Natarajan Velmurugan
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  6. Kallare P. Arunkumar
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  7. Channakeshavaiah Chikkaputtaiah
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Correspondence to Channakeshavaiah Chikkaputtaiah.

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Saikia, B., Singh, S., Debbarma, J. et al. Multigene CRISPR/Cas9 genome editing of hybrid proline rich proteins (HyPRPs) for sustainable multi-stress tolerance in crops: the review of a promising approach. Physiol Mol Biol Plants 26, 857–869 (2020). https://doi.org/10.1007/s12298-020-00782-6

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