Abstract
Introgression of disease resistance genes (R-genes) to fight against an array of phytopathogens takes several years using conventional breeding approaches. Pathogens develop mechanism(s) to escape plants immune system by evolving new strains/races, thus making them susceptible to disease. Conversely, disruption of host susceptibility factors (or S-genes) provides opportunities for resistance breeding in crops. S-genes are often exploited by phytopathogens to promote their growth and infection. Therefore, identification and targeting of disease susceptibility genes (S-genes) are gaining more attention for the acquisition of resistance in plants. Genome engineering of S-genes results in targeted, transgene-free gene modification through CRISPR-Cas-mediated technology and has been reported in several agriculturally important crops. In this review, we discuss the defense mechanism in plants against phytopathogens, tug of war between R-genes and S-genes, in silico techniques for identification of host-target (S-) genes and pathogen effector molecule(s), CRISPR-Cas-mediated S-gene engineering, its applications, challenges, and future prospects.
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References
Abuqamar S, Ajeb S, Sham A, Rizq M, Iratni ER (2013) A mutation in the expansin-like A2 gene enhances resistance to necrotrophic fungi and hypersensitivity to abiotic stress in Arabidopsis thaliana. Mol Plant Pathol 14:813–827. https://doi.org/10.1111/mpp.12049
Acevedo-Garcia J, Spencer D, Thieron H, Reinstädler A, Hammond-Kosack K, Phillips AL, Panstruga R (2017) MLO-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnol J 15:367. https://doi.org/10.1111/pbi.12631
Achary VMM, Reddy MK (2021) CRISPR-Cas9 mediated mutation in GRAIN WIDTH and WEIGHT2 (GW2) locus improves aleurone layer and grain nutritional quality in rice. Sci Rep 11:21941. https://doi.org/10.1038/s41598-021-00828-z
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Amezrou RI, Audéon C, Rôme Compain J, Gélisse S, Ducasse A, Saintenac C, Lapalu N, Louet C, Orford S, Croll D, Amselem J, Fillinger S, Marcel TC (2023) A secreted protease-like protein in Zymoseptoria tritici is responsible for avirulence on Stb9 resistance gene in wheat. PLOS Pathog 19:e1011376. https://doi.org/10.1371/journal.ppat.1011376
Ammari MG, Gresham CR, McCarthy FM, Nanduri B (2016) HPIDB 2.0: a curated database for host-pathogen interactions. Database : J Biol Databases Curation 2016:baw103. https://doi.org/10.1093/database/baw103
An Y, Wang J, Li C, Revote J, Zhang Y, Naderer T, Hayashida M, Akutsu T, Webb GI, Lithgow T, Song J (2017) SecretEPDB: A comprehensive web-based resource for secreted effector proteins of the bacterial types III, IV, and VI secretion systems. Sci Rep 7:41031. https://doi.org/10.1038/srep41031
Andolfo G, Ercolano MR (2015) Plant innate immunity multicomponent model. Front Plant Sci 6:987. https://doi.org/10.3389/fpls.2015.00987
Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones JDG (2014) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14:1–12. https://doi.org/10.1186/1471-2229-14-120
Andolfo G, Iovieno P, Frusciante L, Ercolano MR (2016) Genome-editing technologies for enhancing plant disease resistance. Front Plant Sci 7:1813. https://doi.org/10.3389/fpls.2016.01813
Andolfo G, Dohm JC, Himmelbauer H (2022) Prediction of NB-LRR resistance genes based on full-length sequence homology. Plant J 110:1592–1602. https://doi.org/10.1111/TPJ.15756
Appiano M, Pavan S, Catalano D, Zheng Z, Bracuto V, Lotti C, Visser RGF, Ricciardi L, Bai Y (2015) Identification of candidate MLO powdery mildew susceptibility genes in cultivated Solanaceae and functional characterization of tobacco NtMLO1. Transgenic Res 24:847–858. https://doi.org/10.1007/S11248-015-9878-4
Azameti MK, Dauda WP (2021) Base Editing in Plants: Applications, Challenges, and Future Prospects. F Plant Sci 12:1531. https://doi.org/10.3389/fpls.2021.664997
Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, Visser R, Theres K, Panstruga R (2007) Naturally Occurring Broad-Spectrum Powdery Mildew Resistance in a Central American Tomato Accession Is Caused by Loss of Mlo Function. Mol Plant Microbe Interact 21:30–39. https://doi.org/10.1094/MPMI-21-1-0030
Bao L, Gao H, Zheng Z, Zhao X, Zhang M, Jiao F, Su C, Qian Y (2020) Integrated Transcriptomic and Un-Targeted Metabolomics Analysis Reveals Mulberry Fruit (Morus atropurpurea) in Response to Sclerotiniose Pathogen Ciboria shiraiana Infection. Int J Mol Sci 21:1789. https://doi.org/10.3390/ijms21051789
Barman HN, Sheng Z, Fiaz S, Zhong M, Wu Y, Cai Y, Wang W, Jiao G, Tang S, Wei X, Hu P (2019) Generation of a new thermo-sensitive genic male sterile rice line by targeted mutagenesis of TMS5 gene through CRISPR/Cas9 system. BMC Plant Biol 19:109. https://doi.org/10.1186/s12870-019-1715-0
Bastet A, Zafirov D, Giovinazzo N, Guyon-Debast A, Nogué F, Robaglia C, Gallois JL (2019) Mimicking natural polymorphism in eIF4E by CRISPR-Cas9 base editing is associated with resistance to potyviruses. Plant Biotechnol J 17:1736–1750. https://doi.org/10.1111/pbi.13096
Bentham A, Burdett H, Anderson PA, Williams SJ, Kobe B (2017) Animal NLRs provide structural insights into plant NLR function. Ann Bot 119:698. https://doi.org/10.1093/AOB/mcw171
Blum M, Chang HY, Chuguransky S, Grego T, Kandasaamy S, Mitchell A, Nuka G, Paysan-Lafosse T, Qureshi M, Raj S, Richardson L, Salazar GA, Williams L, Bork P, Bridge A, Gough J, Haft DH, Letunic I, Marchler-Bauer A, Finn RD (2021) The InterPro protein families and domains database: 20 years on. Nucleic Acids Res 49:D344–D354. https://doi.org/10.1093/nar/gkaa977
Borejsza-Wysocka EE, Malnoy M, Aldwinckle HS, Meng X, Bonasera JM, Nissinen RM, Kim JF, Beer SV (2006) The fire blight resistance of apple clones in which dspe-interacting proteins are silenced. Acta Hortic 704:509–514. https://doi.org/10.17660/ActaHortic.2006.704.80
Borrelli VMG, Brambilla V, Rogowsky P, Marocco A, Lanubile A (2018) The enhancement of plant disease resistance using crispr/cas9 technology. F Plant Sci 9:1245. https://doi.org/10.3389/fpls.2018.01245
Boyd LA, Ridout CO, Sullivan DM, Leach JE, Leung H (2013) Plant–pathogen interactions: disease resistance in modern agriculture. Trends Genet 29:233–240. https://doi.org/10.1016/j.tig.2012.10.011
Cao Y, Zhou H, Zhou X, Li F (2020) Control of Plant Viruses by CRISPR/Cas System-Mediated Adaptive Immunity. F Microbiol 11:593700. https://doi.org/10.3389/fmicb.2020.593700
Carreón-Anguiano KG, Islas-Flores I, Vega-Arreguín J, Sáenz-Carbonell L, Canto-Canché B (2020) Effhunter: A tool for prediction of effector protein candidates in fungal proteomic databases. Biomolecules 10:712. https://doi.org/10.3390/biom10050712
Castro-Moretti FR, Gentzel IN, Mackey D, Alonso AP (2020) Metabolomics as an Emerging Tool for the Study of Plant-Pathogen Interactions. Metabolites 10:52. https://doi.org/10.3390/metabo10020052
Cha JY, Uddin S, Macoy DM, Shin GI, Jeong SY, Ali I, Hwang JW, Ji MG, Lee SC, Park JH, Sultana M, Ryu GR, Ahn G, Lee SY, Kim MG, Kim WY (2023) Nucleoredoxin gene SINRX1 negatively regulates tomato immunity by activating SA signaling pathway. Plant Physiol Biochem 200:107804. https://doi.org/10.1016/J.PLAPHY.2023.107804
Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153. https://doi.org/10.1111/mpp.12375
Chaudhry A, Hassan AU, Khan SH, Abbasi A, Hina A, Khan MT, Abdelsalam NR (2023) The changing landscape of agriculture: role of precision breeding in developing smart crops. Funct Integr Genomic 23:167. https://doi.org/10.1007/S10142-023-01093-1
Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833. https://doi.org/10.1038/35081161
Das A, Sharma N, Prasad M (2019) CRISPR/Cas9: A novel weapon in the arsenal to combat plant diseases. F Plant Sci 9:2008. https://doi.org/10.3389/fpls.2018.02008
Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
Deng Y, Ning Y, Yang DL, Zhai K, Wang GL, He Z (2020) Molecular Basis of Disease Resistance and Perspectives on Breeding Strategies for Resistance Improvement in Crops. Mol Plant 13:1402–1419). https://doi.org/10.1016/j.molp.2020.09.018
Derevnina L, Petre B, Kellner R, Dagdas YF, Sarowar MN, Giannakopoulou A, de la Concepcion JC, Chaparro-Garcia A, Pennington HG, van West P, Kamoun S (2016) Emerging oomycete threats to plants and animals. Philos Trans R Soc B Biol Sci 371:1709. https://doi.org/10.1098/rstb.2015.0459
Dodds PN, Rathjen JP (2010) Plant immunity: Towards an integrated view of plantĝ€" pathogen interactions. Nat Rev Genet 11:539–548. https://doi.org/10.1038/nrg2812
Dong OX, Ronald PC (2019a) Update on Genetic Engineering for Disease Resistance Genetic Engineering for Disease Resistance in Plants: Recent Progress and Future Perspectives. Plant Physiol 180:26–38. https://doi.org/10.1104/pp.18.01224
Dong OX, Ronald PC (2019b) Genetic Engineering for Disease Resistance in Plants: Recent Progress and Future Perspectives. Plant Physiol 180:26–38. https://doi.org/10.1104/pp.18.01224
Eichmann R, Bischof M, Weis C, Shaw J, Lacomme C, Schweizer P, Duchkov D, Hensel G, Kumlehn J, Hückelhoven R (2010) BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Mol Plant-Microbe Interact 23:1217–1227. https://doi.org/10.1094/MPMI-23-9-1217
Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) Erratum: The arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1981. https://doi.org/10.1105/tpc.cor022
Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014) The past, present and future of breeding rust resistant wheat. F Plant Sci 5:641. https://doi.org/10.3389/fpls.2014.00641
El-Mounadi K, Morales-Floriano ML, Garcia-Ruiz H (2020) Principles, Applications, and Biosafety of Plant Genome Editing Using CRISPR-Cas9. F Plant Sci 11:56. https://doi.org/10.3389/fpls.2020.00056
Ewan R, Pangestuti R, Thornber S, Craig A, Carr C, O’Donnell L, Zhang C, Sadanandom A (2011) Deubiquitinating enzymes AtUBP12 and AtUBP13 and their tobacco homologue NtUBP12 are negative regulators of plant immunity. New Phytol 191:92–106. https://doi.org/10.1111/j.1469-8137.2011.03672.x
Fister AS, Landherr L, Maximova SN, Guiltinan MJ (2018) Transient expression of CRISPR/Cas9 machinery targeting TcNPR3 enhances defense response in theobroma cacao. F Plant Sci 9:268. https://doi.org/10.3389/fpls.2018.00268
Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci 98:373. https://doi.org/10.1073/pnas.98.1.373
Gaj T, Sirk SJ, Shui SL, Liu J (2016) Genome-Editing Technologies: Principles and Applications. Cold Spring Harb Perspect Biol 8:a023754. https://doi.org/10.1101/CSHPERSPECT.A023754
Garcia-Ruiz H, Szurek B, Van den Ackerveken G (2021) Stop helping pathogens: engineering plant susceptibility genes for durable resistance. Curr Opin Biotechnol 70:187–195. https://doi.org/10.1016/J.COPBIO.2021.05.005
Giannakopoulou A, Steele JFC, Segretin ME, Bozkurt TO, Zhou J, Robatzek S, Banfield MJ, Pais M, Kamoun S (2015) Tomato I2 Immune Receptor Can Be Engineered to Confer Partial Resistance to the Oomycete Phytophthora infestans in Addition to the Fungus Fusarium oxysporum. Mol Plant Microbe Interact 28:1316–1329. https://doi.org/10.1094/MPMI-07-15-0147-R
Gomez MA, Lin ZD, Moll T, Chauhan RD, Hayden L, Renninger K, Beyene G, Taylor NJ, Carrington JC, Staskawicz BJ, Bart RS (2019) Simultaneous CRISPR/Cas9-mediated editing of cassava eIF4E isoforms nCBP-1 and nCBP-2 reduces cassava brown streak disease symptom severity and incidence. Plant Biotechnol J 17:421–434. https://doi.org/10.1111/pbi.12987
Gupta PK (2020) SWEET Genes for Disease Resistance in Plants. Trends Genet 36:901–904. https://doi.org/10.1016/j.tig.2020.08.007
Hashimoto M, Neriya Y, Yamaji Y, Namba S (2016) Recessive Resistance to Plant Viruses: Potential Resistance Genes Beyond Translation Initiation Factors. F Microbiol 7:1695. https://doi.org/10.3389/fmicb.2016.01695
Hasley JAR, Navet N, Tian M (2021) CRISPR/Cas9-mediated mutagenesis of sweet basil candidate susceptibility gene ObDMR6 enhances downy mildew resistance. PloS One 16:e0253245. https://doi.org/10.1371/journal.pone.0253245
Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12:934–940. https://doi.org/10.1111/pbi.12201
Henningsen EC, Omidvar V, Della Coletta R, Michno JM, Gilbert E, Li F, Miller ME, Myers CL, Gordon SP, Vogel JP, Steffenson BJ, Kianian SF, Hirsch CD, Figueroa M (2021) Identification of Candidate Susceptibility Genes to Puccinia graminis f. sp. tritici in Wheat. F Plant Sci 12:657796. https://doi.org/10.3389/fpls.2021.657796
Hong Y, Meng J, He X, Zhang Y, Liu Y, Zhang C, Qi H, Luan Y (2021) Editing mir482b and mir482c simultaneously by crispr/cas9 enhanced tomato resistance to phytophthora infestans. Phytopathol 111:1008–1016. https://doi.org/10.1094/PHYTO-08-20-0360-R
Huibers RP, Loonen AEHM, Gao D, Van den Ackerveken G, Visser RGF, Bai Y (2013) Powdery Mildew Resistance in Tomato by Impairment of SlPMR4 and SlDMR1. PLOS ONE 8:e67467. https://doi.org/10.1371/journal.pone.0067467
Ismail M, Mbinda W, Masaki H (2021) Breeding Strategies and Challenges in the Improvement of Blast Disease Resistance in Finger Millet. A Current Review. F Plant Sci 11:602882. https://doi.org/10.3389/fpls.2020.602882
Jacob P, Avni A, Bendahmane A (2018) Translational Research: Exploring and Creating Genetic Diversity. Trends Plant Sci 23:42–52. https://doi.org/10.1016/j.tplants.2017.10.002
Jaganathan D, Bohra A, Thudi M, Varshney RK (2020) Fine mapping and gene cloning in the post-NGS era: advances and prospects. Theor Appl Genet 133:1791–1810. https://doi.org/10.1007/s00122-020-03560-w
Jehl MA, Arnold R, Rattei T (2011) Effective-A database of predicted secreted bacterial proteins. Nucleic Acids Res 39:591–595. https://doi.org/10.1093/nar/gkq1154
Jia H, Orbovic V, Jones JB, Wang N (2016) Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4:dCsLOB1.3 infection. Plant Biotechnol J 14:1291–1301. https://doi.org/10.1111/pbi.12495
Jogam P, Sandhya D, Alok A, Peddaboina V, Singh SP, Abbagani S, Zhang B, Allini VR (2023) Editing of TOM1 gene in tobacco using CRISPR/Cas9 confers resistance to Tobacco mosaic virus. Mol Bio Rep 50:5165–5176. https://doi.org/10.1007/S11033-023-08440-2/METRICS
Jupe F, Witek K, Verweij W, Śliwka J, Pritchard L, Etherington GJ, Maclean D, Cock PJ, Leggett RM, Bryan GJ, Cardle L, Hein I, Jones JDG (2013) Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J 76:530. https://doi.org/10.1111/TPJ.12307
Kamoun S, Furzer O, Jones JDG, Judelson HS, Ali GS, Dalio RJD, Roy SG, Schena L, Zambounis A, Panabières F, Cahill D, Ruocco M, Figueiredo A, Chen XR, Hulvey J, Stam R, Lamour K, Gijzen M, Tyler BM, Govers F (2015) The Top 10 oomycete pathogens in molecular plant pathology. Mol Plant Pathol 16:413–434. https://doi.org/10.1111/MPP.12190
Kapos P, Devendrakumar KT, Li X (2019) Plant NLRs: From discovery to application. Plant Sci 279:3–18. https://doi.org/10.1016/j.plantsci.2018.03.010
Karmakar S, Das P, Panda D, Xie K, Baig MJ, Molla KA (2022) A detailed landscape of CRISPR-Cas-mediated plant disease and pest management. Plant Sci 323:111376. https://doi.org/10.1016/j.plantsci.2022.111376
Kieu NP, Lenman M, Wang ES, Petersen L, Andreasson E (2021) Mutations introduced in susceptibility genes through CRISPR/Cas9 genome editing confer increased late blight resistance in potatoes. Sci Rep 11:4487. https://doi.org/10.1038/s41598-021-83972-w
Kim DS, Hwang BK (2012) The pepper MLO gene, CaMLO2, is involved in the susceptibility cell-death response and bacterial and oomycete proliferation. Plant J 72:843–855. https://doi.org/10.1111/TPJ.12003
Klap C, Yeshayahou E, Bolger AM, Arazi T, Gupta SK, Shabtai S, Usadel B, Salts Y, Barg R (2017) Tomato facultative parthenocarpy results from SlAGAMOUSLIKE 6 loss of function. Plant Biotechnol J 15:634-647. https://doi.org/10.1111/pbi.12662
Koseoglou E, van der Wolf JM, Visser RGF, Bai Y (2022) Susceptibility reversed: modified plant susceptibility genes for resistance to bacteria. Trends Plant Sci 27:69–79. https://doi.org/10.1016/J.TPLANTS.2021.07.018
Kourelis J, Sakai T, Adachi H, Kamoun S (2021) RefPlantNLR: a comprehensive collection of experimentally validated plant NLRs. PLoS Biology 19:e3001124. https://doi.org/10.1371/journal.pbio.3001124
Kusch S, Panstruga R (2017) MLO-Based Resistance: An Apparently Universal “Weapon” to Defeat Powdery Mildew Disease. Mol Plant-Microbe Interact 30:179–189. https://doi.org/10.1094/MPMI-12-16-0255-CR
Langner T, Kamoun S, Belhaj K (2018) CRISPR Crops: Plant genome editing toward disease resistance. Ann Rev Phytopathol 56:479–512. https://doi.org/10.1146/annurev-phyto-080417-050158
Larkin RP, Brewer MT (2020) Effects of Crop Rotation and Biocontrol Amendments on Rhizoctonia Disease of Potato and Soil Microbial Communities. Agriculture 10:128. https://doi.org/10.3390/agriculture10040128
Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392. https://doi.org/10.1038/NBT.2199
Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, Lin Q, Luo W, Wu G, Li H (2016) Reassessment of the Four Yield-related Genes Gn1a, DEP1, GS3, and IPA1 in Rice Using a CRISPR/Cas9 System. F Plant Sci 7:377. https://doi.org/10.3389/fpls.2016.00377
Li A, Jia S, Yobi A, Ge Z, Sato SJ, Zhang C, Clemente TE, Holding DR (2018) Editing of an alpha-kafirin gene family increases digestibility and protein. Plant Physiol 177:1425–1438. https://doi.org/10.1104/pp.18.00200
Li C, Brant E, Budak H, Zhang B (2021) CRISPR/Cas: a Nobel Prize award-winning precise genome editing technology for gene therapy and crop improvement. J Zhejiang Univ Sci B 22:253–284. https://doi.org/10.1631/JZUS.B2100009
Li C, Chu W, Gill RA, Sang S, Shi Y, Hu X, Yang Y, Zaman QU, Zhang B (2022) Computational Tools and Resources for CRISPR/Cas Genome Editing. Genom Proteom Bioinform. https://doi.org/10.1016/J.GPB.2022.02.006
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 63:3899–3911. https://doi.org/10.1093/jxb/ers079
Lu W, Deng F, Jia J, Chen X, Li J, Wen Q, Li T, Meng Y, Shan W (2020) The Arabidopsis thaliana gene AtERF019 negatively regulates plant resistance to Phytophthora parasitica by suppressing PAMP-triggered immunity. Mol Plant Pathol 21:1179–1193. https://doi.org/10.1111/MPP.12971
Macovei A, Sevilla NR, Cantos C, Jonson GB, Slamet-Loedin I, Čermák T, Voytas DF, Choi IR, Chadha-Mohanty P (2018) Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant Biotechnol J 16:1918–1927. https://doi.org/10.1111/pbi.12927
Malnoy M, Viola R, Jung MH, Koo OJ, Kim S, Kim JS, Velasco R, Nagamangala Kanchiswamy C (2016) DNA-Free Genetically Edited Grapevine and Apple Protoplast Using CRISPR/Cas9 Ribonucleoproteins. F Plant Sci 7:1904. https://doi.org/10.3389/fpls.2016.01904
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. https://doi.org/10.1016/j.tplants.2019.09.006
Masoodi KZ, Ahmed N, Mir MA, Bhat B, Shafi A, Mansoor S, Rasool RS, Yaseen M, Dar ZA, Mir JI, Andrabi SM, Ganai NA (2022) Comparative transcriptomics unravels new genes imparting scab resistance in apple (Malus x domestica Borkh.). Funct Integr Genomic 22:1315–1330. https://doi.org/10.1007/S10142-022-00889-X
Melotto M, Underwood W, Sheng YH (2008) Role of Stomata in Plant Innate Immunity and Foliar Bacterial Diseases. Annu Rev Phytopathol 46:101–122. https://doi.org/10.1146/annurev.phyto.121107.104959
Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134. https://doi.org/10.1016/j.pbi.2005.01.002
Miao LX, Jiang M, Zhang YC, Yang XF, Zhang HQ, Zhang ZF, Wang YZ, Jiang GH (2016) Genomic identification, phylogeny, and expression analysis of MLO genes involved in susceptibility to powdery mildew in Fragaria vesca. Genetics Mol Res 15:gmr.15038400. https://doi.org/10.4238/gmr.15038400
Moniruzzaman M, Zhong Y, Yan H, Yuanda L, Jiang B (2020) Exploration of Susceptible Genes with Clustered Regularly Interspaced Short Palindromic Repeats – Tissue-Specific Knockout ( CRISPR-TSKO ) to Enhance Host Resistance Exploration of Susceptible Genes with Clustered Regula. Crit Rev Plant Sci 39:387–417. https://doi.org/10.1080/07352689.2020.1810970
Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S (2017) Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep 7:482. https://doi.org/10.1038/s41598-017-00578-x
Ngou BPM, Ahn HK, Ding P, Jones JDG (2021) Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592:110–115. https://doi.org/10.1038/S41586-021-03315-7
Ngou BPM, Ding P, Jones JDG (2022) Thirty years of resistance: Zig-zag through the plant immune system. Plant Cell 34:1447–1478. https://doi.org/10.1093/plcell/koac041
Ortigosa A, Gimenez-Ibanez S, Leonhardt N, Solano R (2019) Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of SlJAZ2. Plant Biotechnol J 17:665–673. https://doi.org/10.1111/pbi.13006
Osuna-Cruz CM, Paytuvi-Gallart A, Donato AD, Sundesha V, Andolfo G, Cigliano RA, Sanseverino W, Ercolano MR (2017) PRGdb 3.0: a comprehensive platform for prediction and analysis of plant disease resistance genes. Nuc Acids Res 46:1197–1201. https://doi.org/10.1093/nar/gkx1119
Patterson EL, Saski C, Küpper A, Beffa R, Gaines TA (2019) Omics Potential in Herbicide-Resistant Weed Management. Plants 8:607. https://doi.org/10.3390/plants8120607
Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J 15:1509–1519. https://doi.org/10.1111/pbi.12733
Pessina S, Lenzi L, Perazzolli M, Campa M, Dalla Costa L, Urso S, Valè G, Salamini F, Velasco R, Malnoy M (2016) Knockdown of MLO genes reduces susceptibility to powdery mildew in grapevine. Hortic Res 3:16016. https://doi.org/10.1038/hortres.2016.16
Pyott DE, Sheehan E, Molnar A (2016) Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Pathol 17:1276–1288. https://doi.org/10.1111/mpp.12417
Rao VS, Srinivas K, Sujini GN, Kumar GNS (2014) Protein-Protein Interaction Detection: Methods and Analysis. Int J Proteomics 2014:147648. https://doi.org/10.1155/2014/147648
Sánchez-Vallet A, Fouché S, Fudal I, Hartmann FE, Soyer JL, Tellier A, Croll D (2018) The Genome Biology of Effector Gene Evolution in Filamentous Plant Pathogens. Annu Rev Phytopathol 56:21–40. https://doi.org/10.1146/ANNUREV-PHYTO-080516-035303
Sanfaçon H (2015) Plant Translation Factors and Virus Resistance. Viruses 7:3392–3419. https://doi.org/10.3390/v7072778
Santillán Martínez MI, Bracuto V, Koseoglou E, Appiano M, Jacobsen E, Visser RGF, Wolters AMA, Bai Y (2020) CRISPR/Cas9-targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew. BMC Plant Biol 20:284. https://doi.org/10.1186/s12870-020-02497-y
Schindler M, Pommerenke C (2004) PathoPlant : A Database on Plant-Pathogen Interactions. In Silico Biol 4:529–536
Sperschneider J, Dodds PN (2022) EffectorP 3.0: Prediction of Apoplastic and Cytoplasmic Effectors in Fungi and Oomycetes. Mol Plant-Microbe Int 35:146–156. https://doi.org/10.1094/MPMI-08-21-0201-R
Staal J, Van Den Berg N, Guo N, Xing H, Zhu L, Zhou Y, Li X, Zhao J (2018) Metabolomics Analysis of Soybean Hypocotyls in Response to Phytophthora sojae Infection. Front Plant Sci 9:1530. https://doi.org/10.3389/fpls.2018.01530
Sufyan M, Daraz U, Hyder S, Zulfiqar U, Iqbal R, Eldin SM, Rafiq F, Mahmood N, Shahzad K, Uzair M, Fiaz S, Ali I (2023) An overview of genome engineering in plants, including its scope, technologies, progress and grand challenges. Funct Int Genomic 23:1–25. https://doi.org/10.1007/S10142-023-01036-W
Sun K, Wolters AMA, Loonen AEH, Huibers RP, van der Vlugt R, Goverse A, Jacobsen E, Visser RGF, Bai Y (2016a) Down-regulation of Arabidopsis DND1 orthologs in potato and tomato leads to broad-spectrum resistance to late blight and powdery mildew. Transgenic Res 25:123–138. https://doi.org/10.1007/S11248-015-9921-5
Sun K, Wolters AMA, Vossen JH, Rouwet ME, Loonen AEH, Jacobsen E, Visser RGF, Bai Y (2016b) Silencing of six susceptibility genes results in potato late blight resistance. Transgenic Res 25:731–742. https://doi.org/10.1007/S11248-016-9964-2
Tanaka K, Heil M (2021) Damage-Associated Molecular Patterns (DAMPs) in Plant Innate Immunity: Applying the Danger Model and Evolutionary Perspectives. Annu Rev Phytopathol 59:53–75. https://doi.org/10.1146/annurev-phyto-082718-100146
Thomazella DP, Seong K, Mackelprang R, Dahlbeck D, Geng Y, Gill US, Qi T, Pham J, Giuseppe P, Lee CY, Ortega A, Cho MJ, Hutton SF, Staskawicz B (2021) Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. Proc Natl Acad Sci USA 118:e2026152118. https://doi.org/10.1073/pnas.2026152118
Thordal-Christensen H (2020) A holistic view on plant effector-triggered immunity presented as an iceberg model. Cell Mol Life Sci 77:3963–3976. https://doi.org/10.1007/S00018-020-03515-W
Toda N, Rustenholz C, Baud A, Le Paslier MC, Amselem J, Merdinoglu D, Faivre-Rampant P (2020) NLGenomeSweeper: A Tool for Genome-Wide NBS-LRR Resistance Gene Identification. Genes 11:333. https://doi.org/10.3390/genes11030333
Tripathi JN, Ntui VO, Shah T, Tripathi L (2021) CRISPR/Cas9-mediated editing of DMR6 orthologue in banana (Musa spp.) confers enhanced resistance to bacterial disease. Plant Biotechnol J 19:1291–1293. https://doi.org/10.1111/pbi.13614
Trujillo M, Ichimura K, Casais C, Shirasu K (2008) Negative Regulation of PAMP-Triggered Immunity by an E3 Ubiquitin Ligase Triplet in Arabidopsis. Curr Biol 18:1396–1401. https://doi.org/10.1016/j.cub.2008.07.085
Tyagi S, Kumar R, Kumar V, Won SY, Shukla P (2021) Engineering disease resistant plants through CRISPR-Cas9 technology. GM Crops Food 12:125–144. https://doi.org/10.1080/21645698.2020.1831729
Uppalapati SR, Ishiga Y, Doraiswamy V, Bedair M, Mittal S, Chen J, Nakashima J, Tang Y, Tadege M, Ratet P, Chen R, Schultheiss H, Mysore KS (2012) Loss of abaxial leaf epicuticular wax in Medicago truncatula irg1/palm Mutants results in reduced spore differentiation of anthracnose and nonhost rust pathogens. Plant Cell 24:353–370. https://doi.org/10.1105/tpc.111.093104
Urban M, Cuzick A, Seager J, Wood V, Rutherford K, Venkatesh SY, De Silva N, Martinez MC, Pedro H, Yates AD, Hassani-Pak K, Hammond-Kosack KE (2020) PHI-base: The pathogen-host interactions database. Nuc Acids Res 48:D613–D620. https://doi.org/10.1093/nar/gkz904
Van Schie CCN, Takken FLW (2014) Susceptibility genes 101: How to be a good host. Ann Rev Phytopathol 52:551–581. https://doi.org/10.1146/annurev-phyto-102313-045854
Van Wersch S, Tian L, Hoy R, Li X (2020) Plant NLRs: The Whistleblowers of Plant Immunity. Plant Commun 1:100016. https://doi.org/10.1016/J.XPLC.2019.100016
Veillet F, Durand M, Kroj T, Cesari S, Gallois JL (2020) Precision Breeding Made Real with CRISPR: Illustration through Genetic Resistance to Pathogens. Plant Commun 1:100102. https://doi.org/10.1016/J.XPLC.2020.100102
Von Saint PV, Zhang W, Kanawati B, Geist B, Faus-Keßler T, Schmitt-Kopplin P, Schäffner AR (2011) The arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23:4124–4145. https://doi.org/10.1105/tpc.111.088443
Wang A (2015) Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Ann Rev Phytopathol 53:45–66. https://doi.org/10.1146/annurev-phyto-080614-120001
Wang A, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 13:795–803. https://doi.org/10.1111/j.1364-3703.2012.00791.x
Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GED (2012) A Common Signaling Process that Promotes Mycorrhizal and Oomycete Colonization of Plants. Curr Biol 22:2242–2246. https://doi.org/10.1016/J.CUB.2012.09.043
Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, 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 F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K (2016) Enhanced Rice Blast Resistance by CRISPR/Cas9-Targeted Mutagenesis of the ERF Transcription Factor Gene OsERF922. PLOS ONE 11:e0154027. https://doi.org/10.1371/journal.pone.0154027
Wang Yansu, Wang P, Guo Y, Huang S, Chen Y, Xu L (2021) prPred: A Predictor to Identify Plant Resistance Proteins by Incorporating k-Spaced Amino Acid (Group) Pairs. Front Bioeng Biotechnol 8:645520. https://doi.org/10.3389/fbioe.2020.645520
Yan Z, Appiano M, van Tuinen A, Meijer-Dekens F, Schipper D, Gao D, Huibers R, Visser RGF, Bai Y, Wolters AMA (2021) Discovery and characterization of a novel tomato mlo mutant from an ems mutagenized micro-tom population. Genes 12:719. https://doi.org/10.3390/GENES12050719/S1
Yang B, Yang B (2020) Grand Challenges in Genome Editing in Plants. Front Genome Ed 2:1–3. https://doi.org/10.3389/fgeed.2020.00002
Yang S, Li H, He H, Zhou Y, Zhang Z (2019) Critical assessment and performance improvement of plant-pathogen protein-protein interaction prediction methods. Brief Bioinform 20:274–287. https://doi.org/10.1093/bib/bbx123
Yuan M, Jiang Z, Bi G, Nomura K, Liu M, Wang Y, Cai B, Zhou JM, He SY, Xin XF (2021a) Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592:105. https://doi.org/10.1038/S41586-021-03316-6
Yuan M, Ngou BPM, Ding P, Xin XF (2021) PTI-ETI crosstalk: an integrative view of plant immunity. Curr Opin Plant Biol 62:102030. https://doi.org/10.1016/J.PBI.2021.102030
Zaidi SS, Mukhtar MS, Mansoor S (2018) Genome Editing : Targeting Susceptibility Genes for Plant Disease Resistance. Trends Biotechnol 36:898–906. https://doi.org/10.1016/j.tibtech.2018.04.005
Zaidi SS, Mahas A, Vanderschuren H, Mahfouz MM (2020) Engineering crops of the future: CRISPR approaches to develop climate-resilient and disease-resistant plants. Genome Biol 21:1–19. https://doi.org/10.1186/s13059-020-02204-y
Zhang K, Halitschke R, Yin C, Liu CJ, Gan SS (2013) Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc Natl Acad Sci USA 110:14807. https://doi.org/10.1073/pnas.1302702110
Zhang Y, Bai Y, Wu G, Zou S, Chen Y, Gao C, Tang D (2017) Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J Cell Mol Biol 91:714–724. https://doi.org/10.1111/tpj.13599
Zhang R, Chen S, Meng X, Chai Z, Wang D, Yuan Y, Chen K, Jiang L, Li J, Gao C (2021) Generating broad-spectrum tolerance to ALS-inhibiting herbicides in rice by base editing. Science China Life Sciences 64:1624–1633. https://doi.org/10.1007/s11427-020-1800-5
Zhang H, Zheng D, Song F, Jiang M (2022) Expression Patterns and Functional Analysis of 11 E3 Ubiquitin Ligase Genes in Rice. Front Plant Sci 13:1–14. https://doi.org/10.3389/fpls.2022.840360
Zhang T, Xu N, Amanullah S, Gao P (2023) Genome-wide identification, evolution, and expression analysis of MLO gene family in melon (Cucumis melo L.). F Plant Sci 14:493. https://doi.org/10.3389/fpls.2023.1144317
Zheng Z, Appiano M, Pavan S, Bracuto V, Ricciardi L, Visser RGF, Wolters AMA, Bai Y (2016) Genome-wide study of the tomato SlMLO gene family and its functional characterization in response to the powdery mildew fungus oidium neolycopersici. F Plant Sci 7:380. https://doi.org/10.3389/fpls.2016.00380
Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Huang S, Liu S, Vera Cruz C, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J Cell Mol Biol 82:632–643. https://doi.org/10.1111/tpj.12838
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The authors are thankful to the Department of Biotechnology, Government of India, for funding the project “Application of Bioinformatics and Computational Biology in Agriculture-BIC” (BT/PR40193/BTIS/137/23/2021).
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RB, SK, JSS, and DS have written and drafted the manuscript. SK and DS have prepared the figures. RB and DS have conceived and coordinated the project. RB and JSS were involved in language editing. The manuscript is seen and approved by all the authors.
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Bishnoi, R., Kaur, S., Sandhu, J.S. et al. Genome engineering of disease susceptibility genes for enhancing resistance in plants. Funct Integr Genomics 23, 207 (2023). https://doi.org/10.1007/s10142-023-01133-w
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DOI: https://doi.org/10.1007/s10142-023-01133-w