Abstract
The conventional breeding of crops struggles to keep up with increasing food needs and ever-adapting pests and pathogens. Global climate changes have imposed another layer of complexity to biological systems, increasing the challenge to obtain improved crop cultivars. These dictate the development and application of novel technologies, like genome editing (GE), that assist targeted and fast breeding programs in crops, with enhanced resistance to pests and pathogens. GE does not require crossings, hence avoiding the introduction of undesirable traits through linkage in elite varieties, speeding up the whole breeding process. Additionally, GE technologies can improve plant protection by directly targeting plant susceptibility (S) genes or virulence factors of pests and pathogens, either through the direct edition of the pest genome or by adding the GE machinery to the plant genome or to microorganisms functioning as biocontrol agents (BCAs). Over the years, GE technology has been continuously evolving and more so with the development of CRISPR/Cas. Here we review the latest advancements of GE to improve plant protection, focusing on CRISPR/Cas-based genome edition of crops and pests and pathogens. We discuss how other technologies, such as host-induced gene silencing (HIGS) and the use of BCAs could benefit from CRISPR/Cas to accelerate the development of green strategies to promote a sustainable agriculture in the future.
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Abbreviations
- BCA:
-
Biocontrol agent
- Cas9:
-
CRISPR-associated protein 9
- CRISPR:
-
Clustered regularly interspaced short palindromic repeats
- DAMPs:
-
Damage-associated molecular patterns
- dsRNA:
-
Double-stranded RNA
- ET:
-
Ethylene
- ETI:
-
Effector-trigged immunity
- ETS:
-
Effector-trigger susceptibility
- GE:
-
Genome editing
- gRNA:
-
Guide RNA
- HIGS:
-
Host-induced gene silencing
- HR:
-
Hypersensitive response
- JA:
-
Jasmonic acid
- MAPK:
-
Mitogen activated protein kinase
- NB-LRR:
-
Nucleotide-binding leucine-rich repeat protein
- PAMPs:
-
Pathogen-associated molecular patterns
- PCD:
-
Programmed cell death
- PR:
-
Pathogenesis-related
- PRR:
-
Pattern recognition receptor
- PTI:
-
Pattern-triggered immunity
- R:
-
Resistance
- RLK:
-
Receptor-like kinase
- RNAi:
-
RNA interference
- RNP:
-
Ribonucleoprotein
- S:
-
Susceptibility
- SA:
-
Salicylic acid
- sRNA:
-
Small RNA
- TAL:
-
Transcription activator-like
- TALEN:
-
Transcription activator-like effector nuclease
- TF:
-
Transcription factor
- TIR:
-
Toll/interleukin-1 receptor
- VIGS:
-
Virus‐induced gene silencing
- ZFN:
-
Zinc finger nuclease
References
Abbruscato P, Nepusz T, Mizzi L et al (2012) OsWRKY22, a monocot wrky gene, plays a role in the resistance response to blast. Mol Plant Pathol 13:828–841. https://doi.org/10.1111/j.1364-3703.2012.00795.x
Acevedo-Garcia J, Spencer D, Thieron H et al (2017) mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnol J 15:367–378. https://doi.org/10.1111/pbi.12631
Albert M, Jehle AK, Mueller K et al (2010) Arabidopsis thaliana pattern recognition receptors for bacterial elongation factor Tu and flagellin can be combined to form functional chimeric receptors. J Biol Chem 285:19035–19042. https://doi.org/10.1074/jbc.M110.124800
Altenbuchner J (2016) Editing of the Bacillus subtilis genome by the CRISPR-Cas9 system. Appl Environ Microbiol 82:5421–5427. https://doi.org/10.1128/AEM.01453-16
Aman R, Ali Z, Butt H et al (2018) RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol 19:1. https://doi.org/10.1186/s13059-017-1381-1
Amari K, Boutant E, Hofmann C et al (2010) A family of plasmodesmal proteins with receptor-Like properties for plant viral movement proteins. PLoS Pathog 6:e1001119. https://doi.org/10.1371/journal.ppat.1001119
Anandalakshmi R, Pruss GJ, Ge X et al (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95:13079–13084. https://doi.org/10.1073/pnas.95.22.13079
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
Antony G, Zhou J, Huang S et al (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–3876. https://doi.org/10.1105/tpc.110.078964
Anzalone AV, Koblan LW, Liu DR (2020) Genome editing with CRISPR–Cas nucleases, base editors, transposases and prime editors. Nat Biotechnol 38:824–844. https://doi.org/10.1038/s41587-020-0561-9
Atarashi H, Jayasinghe WH, Kwon J et al (2020) Artificially edited alleles of the eukaryotic translation initiation factor 4E1 gene differentially reduce susceptibility to Cucumber mosaic virus and Potato virus Y in tomato. Front Microbiol 11:3075. https://doi.org/10.3389/fmicb.2020.564310
Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740. https://doi.org/10.1016/j.soilbio.2008.02.013
Baker KF (1987) Evolving concepts of biological control of plant pathogens. Annu Rev Phytopathol 25:67–85. https://doi.org/10.1146/annurev.py.25.090187.000435
Baltes NJ, Hummel AW, Konecna E et al (2015) Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat Plants 1:15145. https://doi.org/10.1038/nplants.2015.145
Bendahmane A, Kanyuka K, Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–791. https://doi.org/10.1105/tpc.11.5.781
Bernoux M, Ve T, Williams S et al (2011) Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host Microbe 9:200–211. https://doi.org/10.1016/j.chom.2011.02.009
Bi H-L, Xu J, Tan A-J, Huang Y-P (2016) CRISPR/Cas9-mediated targeted gene mutagenesis in Spodoptera litura. Insect Sci 23:469–477. https://doi.org/10.1111/1744-7917.12341
Bisht DS, Bhatia V, Bhattacharya R (2019) Improving plant-resistance to insect-pests and pathogens: the new opportunities through targeted genome editing. Semin Cell Dev Biol 96:65–76. https://doi.org/10.1016/j.semcdb.2019.04.008
Blanvillain-Baufumé S, Reschke M, Solé M et al (2017) Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnol J 15:306–317. https://doi.org/10.1111/pbi.12613
Borejsza-Wysocka EE, Malnoy M, Aldwinckle HS et al (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
Bos JIB, Armstrong MR, Gilroy EM et al (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci U S A 107:9909–9914. https://doi.org/10.1073/pnas.0914408107
Brauer EK, Balcerzak M, Rocheleau H et al (2020) Genome editing of a deoxynivalenol-induced transcription factor confers resistance to Fusarium graminearum in wheat. Mol Plant-Microbe Interact 33:553–560. https://doi.org/10.1094/MPMI-11-19-0332-R
Brigneti G, Voinnet O, Li W-X et al (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17:6739–6746. https://doi.org/10.1093/emboj/17.22.6739
Cai Q, He B, Kogel KH, Jin H (2018) Cross-kingdom RNA trafficking and environmental RNAi - nature’s blueprint for modern crop protection strategies. Curr Opin Microbiol 46:58–64. https://doi.org/10.1016/j.mib.2018.02.003
Chandrasekaran J, Brumin M, Wolf D et al (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
Chen LQ, Hou BH, Lalonde S et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532. https://doi.org/10.1038/nature09606
Chen LQ, Qu XQ, Hou BH et al (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211. https://doi.org/10.1126/science.1213351
Chen W, Qian Y, Wu X et al (2014) Inhibiting replication of begomoviruses using artificial zinc finger nucleases that target viral-conserved nucleotide motif. Virus Genes 48:494–501. https://doi.org/10.1007/s11262-014-1041-4
Chen J, Lai Y, Wang L et al (2017) CRISPR/Cas9-mediated efficient genome editing via blastospore-based transformation in entomopathogenic fungus Beauveria bassiana. Sci Rep 7:45763. https://doi.org/10.1038/srep45763
Chen K, Wang Y, Zhang R et al (2019) CRISPR/Cas genome editing and precision plant breeding in agriculture. Ann Rev Plant Biol 70:667–697. https://doi.org/10.1146/annurev-arplant-050718-100049
Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants – With special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513. https://doi.org/10.1016/j.micres.2008.08.007
Chu Z, Ouyang Y, Zhang J et al (2004) Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13. Mol Genet Genom 271:111–120. https://doi.org/10.1007/s00438-003-0964-6
Chu Z, Yuan M, Yao J et al (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255. https://doi.org/10.1101/gad.1416306
Cook RJ (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annu Rev Phytopathol 31:53–80. https://doi.org/10.1146/annurev.py.31.090193.000413
De Lorenzo G, Brutus A, Savatin DV et al (2011) Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett 585:1521–1528. https://doi.org/10.1016/j.febslet.2011.04.043
de Toledo Thomazella DP, Brail Q, Dahlbeck D, Staskawicz BJ (2016) CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. bioRxiv. https://doi.org/10.1101/064824
Deng H, Gao R, Liao X, Cai Y (2017) CRISPR system in filamentous fungi: Current achievements and future directions. Gene 627:212–221. https://doi.org/10.1016/j.gene.2017.06.019
Deslandes L, Olivier J, Theulières F et al (2002) Resistance to ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci U S A 99:2404–2409. https://doi.org/10.1073/pnas.032485099
Doehlemann G, Ökmen B, Zhu W, Sharon A (2017) Plant pathogenic fungi. In: The Fungal Kingdom. Eds: John Wiley and Sons, pp. 703–776. https://doi.org/10.1128/microbiolspec.funk-0023-2016
Dong OX, Ronald PC (2019) 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 X, Hong Z, Chatterjee J et al (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229:87–98. https://doi.org/10.1007/s00425-008-0812-3
Du J, Verzaux E, Chaparro-Garcia A et al (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat Plants 1:15034. https://doi.org/10.1038/nplants.2015.34
Dunn DW, Follett PA (2017) The sterile insect technique (sit): an introduction. Entomol Exp Appl 164:151–154. https://doi.org/10.1111/eea.12619
Escobar MA, Civerolo EL, Summerfelt KR, Dandekar AM (2001) RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis. Proc Natl Acad Sci U S A 98:13437–13442. https://doi.org/10.1073/pnas.241276898
Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371. https://doi.org/10.1016/j.pbi.2007.04.020
Fister AS, Landherr L, Maximova SN, Guiltinan MJ (2018) Transient expression of CRISPR/Cas9 machinery targeting TcNPR3 enhances defense response in theobroma cacao. Front Plant Sci 9:268. https://doi.org/10.3389/fpls.2018.00268
Fitch MMM, Manshardt RM, Gonsalves D et al (1992) Virus resistant papaya plants derived from tissues bombarded with the coat protein gene of apaya ringspot virus. Bio/technol 10:1466–1472. https://doi.org/10.1038/nbt1192-1466
Fones HN, Gurr SJ (2017) NOXious gases and the unpredictability of emerging plant pathogens under climate change. BMC Biol 15:36. https://doi.org/10.1186/s12915-017-0376-4
Fones HN, Bebber DP, Chaloner TM et al (2020) Threats to global food security from emerging fungal and oomycete crop pathogens. Nat Food 1:332–342. https://doi.org/10.1038/s43016-020-0075-0
Fraley RT, Rogers SG, Horsch RB et al (1983) Expression of bacterial genes in plant cells. Proc Natl Acad Sci U S A 80:4803–4807. https://doi.org/10.1073/pnas.80.15.4803
Friedrichs S, Takasu Y, Kearns P et al (2019) Meeting report of the OECD conference on “genome editing: applications in agriculture—implications for health, environment and regulation.” Transgenic Res 28:419–463. https://doi.org/10.1007/s11248-019-00154-1
Fromm M, Taylor LP, Walbot V (1985) Expression of genes transferred into monocot and dicot plant cells by electroporation. Proc Natl Acad Sci U S A 82:5824–5828. https://doi.org/10.1073/pnas.82.17.5824
Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A 98:373–378. https://doi.org/10.1073/pnas.98.1.373
Fuentes A, Carlos N, Ruiz Y et al (2015) 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. https://doi.org/10.1094/MPMI-08-15-0181-R
Gao W, Long L, Zhu LF et al (2013) Proteomic and Virus-induced Gene Silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to verticillium dahliae. Mol Cell Proteom 12:3690–3703. https://doi.org/10.1074/mcp.M113.031013
Garcia-Ruiz H (2018) Susceptibility genes to plant viruses. Viruses 10:484. https://doi.org/10.3390/v10090484
Geissler K, Eschen-Lippold L, Naumann K et al (2015) Mutations in the EDR1 gene alter the response of Arabidopsis thaliana to Phytophthora infestans and the bacterial PAMPs flg22 and elf18. Mol Plant-Microbe Interact 28:122–133. https://doi.org/10.1094/MPMI-09-14-0282-R
Ghogare R, Ludwig Y, Bueno GM, Slamet-Loedin IH, Dhingra A (2021) Genome editing reagent delivery in plants. Transgenic Res. https://doi.org/10.1007/s11248-021-00239-w
Ghorbani Faal P, Farsi M, Seifi A, Mirshamsi Kakhki A (2020) Virus-induced CRISPR-Cas9 system improved resistance against tomato yellow leaf curl virus. Mol Biol Rep 47:3369–3376. https://doi.org/10.1007/s11033-020-05409-3
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
Goffré D, Folgarait PJ (2015) Purpureocillium lilacinum, potential agent for biological control of the leaf-cutting ant Acromyrmex lundii. J Invertebr Pathol 130:107–115. https://doi.org/10.1016/j.jip.2015.07.008
Gomez MA, Lin ZD, Moll T et al (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
Gómez-Gómez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13:1155–1163. https://doi.org/10.1105/tpc.13.5.1155
Guo Z, Li Y, Ding S-W (2019) Small RNA-based antimicrobial immunity. Nat Rev Immunol 19:31–44. https://doi.org/10.1038/s41577-018-0071-x
Hammes UZ (2016) Novel roles for phytosulfokine signalling in plant–pathogen interactions. Plant Cell Environ 39:1393–1395. https://doi.org/10.1111/pce.12679
Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296. https://doi.org/10.1038/35005107
Hammond SM, Boettcher S, Caudy AA et al (2001) Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293:1146–1150. https://doi.org/10.1126/science.1064023
Hammond A, Galizi R, Kyrou K et al (2016) A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol 34:78–83. https://doi.org/10.1038/nbt.3439
Hammond AM, Kyrou K, Bruttini M et al (2017) The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLoS Genet 13:e1007039. https://doi.org/10.1371/journal.pgen.1007039
Harper G, Osuji JO, Heslop-Harrison JS, Hull R (1999) Integration of banana Streak Badnavirus into the musa genome: molecular and cytogenetic evidence. Virology 255:207–213. https://doi.org/10.1006/viro.1998.9581
Heu CC, McCullough FM, Luan J, Rasgon JL (2020) CRISPR-Cas9-based genome editing in the silverleaf W\whitefly (Bemisia tabaci). Cris J 3:89–96. https://doi.org/10.1089/crispr.2019.0067
Hille F, Richter H, Wong SP et al (2018) The biology of CRISPR-Cas: backward and forward. Cell 172:1239–1259. https://doi.org/10.1016/j.cell.2017.11.032
Hily J-M, Scorza R, Malinowski T et al (2004) Stability of gene silencing-based resistance to Plum pox virus in transgenic plum (Prunus domestica L.) under field conditions. Transgenic Res 13:427–436. https://doi.org/10.1007/s11248-004-8702-3
Hind SR, Strickler SR, Boyle PC et al (2016) Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nat Plants 2:16128. https://doi.org/10.1038/nplants.2016.128
Horsch RB, Fry JE, Hoffmann NL et al (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231. https://doi.org/10.1126/science.227.4691.1229
Hou Y, Ma W (2020) Natural host-induced gene silencing offers new opportunities to engineer disease resistance. Trends Microbiol 28:109–117. https://doi.org/10.1016/j.tim.2019.08.009
Hsu FC, Chou MY, Chou SJ et al (2013) Submergence confers immunity mediated by the WRKY22 transcription factor in Arabidopsis. Plant Cell 25:2699–2713. https://doi.org/10.1105/tpc.113.114447
Hu Y, Zhang J, Jia H et al (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci 111:E521–E529. https://doi.org/10.1073/pnas.1313271111
Hu Z, Liu G, Gao J et al (2015) Tomato Tm-22 gene confers multiple resistances to TMV, ToMV, PVX, and PVY to cultivated potato. Russ J Plant Physiol 62:101–108. https://doi.org/10.1134/S1021443715010070
Huibers RP, Loonen AEHM, Gao D et al (2013) Powdery mildew resistance in tomato by impairment of SlPMR4 and SlDMR1. PLoS ONE 8:e67467. https://doi.org/10.1371/journal.pone.0067467
Huss P, Raman S (2020) Engineered bacteriophages as programmable biocontrol agents. Curr Opin Biotechnol 61:116–121. https://doi.org/10.1016/j.copbio.2019.11.013
Islam MT, Kim KH, Choi J (2019) Wheat blast in Bangladesh: the current situation and future impacts. Plant Pathol J 35:1–10. https://doi.org/10.5423/PPJ.RW.08.2018.0168
Jaafar ZA, Kieft JS (2019) Viral RNA structure-based strategies to manipulate translation. Nat Rev Microbiol 17:110–123. https://doi.org/10.1038/s41579-018-0117-x
Jahan SN, Åsman AKM, Corcoran P et al (2015) Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. J Exp Bot 66:2785–2794. https://doi.org/10.1093/jxb/erv094
Jansen C, von Wettstein D, Schäfer W et al (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci 102:16892–16897. https://doi.org/10.1073/pnas.0508467102
Jarosch B, Kogel K-H, Schaffrath U (1999) The ambivalence of the barley Mlo locus: mutations conferring resistance against Ppowdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 12:508–514. https://doi.org/10.1094/MPMI.1999.12.6.508
Ji X, Si X, Zhang Y et al (2018) Conferring DNA virus resistance with high specificity in plants using virus-inducible genome-editing system. Genome Biol 19:197. https://doi.org/10.1186/s13059-018-1580-4
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
Jia H, Zhang Y, Orbović V et al (2017) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15:817–823. https://doi.org/10.1111/pbi.12677
Jiang N, Yan J, Liang Y et al (2020) Resistance genes and their Interactions with bacterial blight/leaf streak pathogens (Xanthomonas oryzae) in Rice (Oryza sativa L.): an updated review. Rice 13:3. https://doi.org/10.1186/s12284-019-0358-y
Jiao Y, Li Y, Li Y et al (2019) Functional genetic analysis of the leucinostatin biosynthesis transcription regulator lcsL in Purpureocillium lilacinum using CRISPR-Cas9 technology. Appl Microbiol Biotechnol 103:6187–6194. https://doi.org/10.1007/s00253-019-09945-2
Johal GS, Briggs SP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258:985–987. https://doi.org/10.1126/science.1359642
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Kandul NP, Liu J, Sanchez CHM et al (2019) Transforming insect population control with precision guided sterile males with demonstration in flies. Nat Commun 10:84. https://doi.org/10.1038/s41467-018-07964-7
Kasschau KD, Carrington JC (1998) A Counter defensive strategy of plant viruses. Cell 95:461–470. https://doi.org/10.1016/S0092-8674(00)81614-1
Kaur G, Upadhyay SK, Verma PC (2021) An overview of genome‐engineering methods. Genome Eng Crop Improv 1–21
Ke Y, Yuan M, Liu H et al (2020) The versatile functions of OsALDH2B1 provide a genic basis for growth–defense trade-offs in rice. Proc Natl Acad Sci 117:3867–3873. https://doi.org/10.1073/pnas.1918994117
Kim S-B, Kang W-H, Huy HN et al (2017) Divergent evolution of multiple virus-resistance genes from a progenitor in Capsicum spp. New Phytol 213:886–899. https://doi.org/10.1111/nph.14177
Kim YA, Moon H, Park CJ (2019) CRISPR/Cas9-targeted mutagenesis of Os8N3 in rice to confer resistance to Xanthomonas oryzae pv. oryzae. Rice 12(1):1–13. https://doi.org/10.1186/s12284-019-0325-7
Kis A, Hamar É, Tholt G et al (2019) Creating highly efficient resistance against wheat dwarf virus in barley by employing CRISPR/Cas9 system. Plant Biotechnol J 17:1004–1006. https://doi.org/10.1111/pbi.13077
Klein TM, Wolf ED, Wu R, Sanford JC (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327:70–73. https://doi.org/10.1038/327070a0
Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:845. https://doi.org/10.3389/fpls.2019.00845
Kohorn B, Kohorn S (2012) The cell wall-associated kinases, WAKs, as pectin receptors. Front Plant Sci 3:88. https://doi.org/10.3389/fpls.2012.00088
Krappmann S (2017) CRISPR-Cas9, the new kid on the block of fungal molecular biology. Med Mycol 55:16–23. https://doi.org/10.1093/mmy/myw097
Krens FA, Molendijk L, Wullems GJ, Schilperoort RA (1982) In vitro transformation of plant protoplasts with Ti-plasmid DNA. Nature 296:72–74. https://doi.org/10.1038/296072a0
Krol E, Mentzel T, Chinchilla D et al (2010) Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem 285:13471–13479. https://doi.org/10.1074/jbc.M109.097394
Kumar A, Prakash A, Johri BN (2011) Bacillus as PGPR in crop ecosystem. Bact Agrobiol Crop Ecosyst. https://doi.org/10.1007/978-3-642-18357-7_2
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
Kushner DB, Lindenbach BD, Grdzelishvili VZ et al (2003) Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci U S A 100:15764–15769. https://doi.org/10.1073/pnas.2536857100
Kyrou K, Hammond AM, Galizi R et al (2018) A CRISPR–Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat Biotechnol 36:1062–1066. https://doi.org/10.1038/nbt.4245
Lacombe S, Rougon-Cardoso A, Sherwood E et al (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369. https://doi.org/10.1038/nbt.1613
Lapin D, Van den Ackerveken G (2013) Susceptibility to plant disease: more than a failure of host immunity. Trends Plant Sci 18:546–554. https://doi.org/10.1016/j.tplants.2013.05.005
Leung K, Ras E, Ferguson KB et al (2020) Next-generation biological control: the need for integrating genetics and genomics. Biol Rev. https://doi.org/10.1111/brv.12641
Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci 107:2491–2496. https://doi.org/10.1073/pnas.0909080107
Li F, Scott MJ (2016) CRISPR/Cas9-mediated mutagenesis of the white and Sex lethal loci in the invasive pest, Drosophila suzukii. Biochem Biophys Res Commun 469:911–916. https://doi.org/10.1016/j.bbrc.2015.12.081
Li F, Wang A (2019) RNA-Targeted antiviral immunity: more Than just RNA silencing. Trends Microbiol 27:792–805. https://doi.org/10.1016/j.tim.2019.05.007
Li T, Liu B, Spalding MH et al (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392. https://doi.org/10.1038/nbt.2199
Li J-F, Norville JE, Aach J et al (2013) Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691. https://doi.org/10.1038/nbt.2654
Li X, Shin S, Heinen S et al (2015) Transgenic wheat expressing a barley UDP-glucosyltransferase detoxifies deoxynivalenol and provides high levels of resistance to Fusarium graminearum. Mol Plant-Microbe Interact 28:1237–1246. https://doi.org/10.1094/MPMI-03-15-0062-R
Li W, Zhu Z, Chern M et al (2017) A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170:114–126. https://doi.org/10.1016/j.cell.2017.06.008
Li K, Cai D, Wang Z et al (2018) Development of an efficient genome editing tool in Bacillus licheniformis using CRISPR-Cas9 nickase. Appl Environ Microbiol 84:e02608-e2617. https://doi.org/10.1128/AEM.02608-17
Li S, Shen L, Hu P et al (2019) Developing disease-resistant thermosensitive male sterile rice by multiplex gene editing. J Integr Plant Biol 61:1201–1205. https://doi.org/10.1111/jipb.12774
Li B, Tang M, Caseys C et al (2020a) Epistatic transcription factor networks differentially modulate Arabidopsis growth and defense. Genetics 214:529–541. https://doi.org/10.1534/genetics.119.302996
Li C, Li W, Zhou Z et al (2020b) A new rice breeding method: CRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene-free bacterial blight-resistant rice. Plant Biotechnol J 18:313–315. https://doi.org/10.1111/pbi.13217
Li W, Deng Y, Ning Y et al (2020c) Exploiting broad-spectrum disease resistance in crops: from molecular dissection to breeding. Annu Rev Plant Biol 71:575–603. https://doi.org/10.1146/annurev-arplant-010720-022215
Lindbo JA, Dougherty WG (1992) Pathogen-derived resistance to a potyvirus: immune and resistant phenotypes in transgenic tobacco expressing altered forms of a potyvirus coat protein nucleotide sequence. Mol Plant-Microbe Interact 5:144–153. https://doi.org/10.1094/mpmi-5-144
Lindner S, Keller B, Pal Singh S et al (2020) Single residues in the LRR domain of the wheat PM3A immune receptor can control the strength and the spectrum of the immune response. Plant J N/a: https://doi.org/10.1111/tpj.14917
Liu D, Chen X, Liu J et al (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
Liu R, Chen L, Jiang Y et al (2015) Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system. Cell Discov 1:15007. https://doi.org/10.1038/celldisc.2015.7
Liu H, Soyars CL, Li J et al (2018) CRISPR/Cas9-mediated resistance to cauliflower mosaic virus. Plant Direct 2:e00047. https://doi.org/10.1002/pld3.47
Lu F, Wang H, Wang S et al (2015) Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR. J Integr Plant Biol 57:641–652. https://doi.org/10.1111/jipb.12306
Lu H, Luo T, Fu H et al (2018) Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis. Nat Plants 4:338–344. https://doi.org/10.1038/s41477-018-0152-7
Lu Y, Tian Y, Shen R et al (2020) Targeted, efficient sequence insertion and replacement in rice. Nat Biotechnol. https://doi.org/10.1038/s41587-020-0581-5
Ma J, Chen J, Wang M et al (2018) Disruption of OsSEC3A increases the content of salicylic acid and induces plant defense responses in rice. J Exp Bot 69:1051–1064. https://doi.org/10.1093/jxb/erx458
Macovei A, Sevilla NR, Cantos C et al (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
Maekawa T, Cheng W, Spiridon LN et al (2011) Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:187–199. https://doi.org/10.1016/j.chom.2011.02.008
Malnoy M, Viola R, Jung MH et al (2016) DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci 7:1904. https://doi.org/10.3389/fpls.2016.01904
Mao Y-B, Cai W-J, Wang J-W et al (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313. https://doi.org/10.1038/nbt1352
McGrann GRD, Stavrinides A, Russell J et al (2014) A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot. J Exp Bot 65:1025–1037. https://doi.org/10.1093/jxb/ert452
Meccariello A, Monti SM, Romanelli A et al (2017) Highly efficient DNA-free gene disruption in the agricultural pest Ceratitis capitata by CRISPR-Cas9 ribonucleoprotein complexes. Sci Rep 7:10061. https://doi.org/10.1038/s41598-017-10347-5
Mehta D, Hirsch-Hoffmann M, Were M et al (2018) A new full-length circular DNA sequencing method for viral-sized genomes reveals that RNAi transgenic plants provoke a shift in geminivirus populations in the field. Nucleic Acids Res 47:e9. https://doi.org/10.1093/nar/gky914
Mehta D, Stürchler A, Anjanappa RB et al (2019) Linking CRISPR-Cas9 interference in cassava to the evolution of editing-resistant geminiviruses. Genome Biol 20:80. https://doi.org/10.1186/s13059-019-1678-3
Melotto M, Underwood W, Koczan J et al (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980. https://doi.org/10.1016/j.cell.2006.06.054
Miya A, Albert P, Shinya T et al (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci 104:19613–19618. https://doi.org/10.1073/pnas.0705147104
Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289. https://doi.org/10.1105/tpc.2.4.279
Narusaka M, Shirasu K, Noutoshi Y et al (2009) RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. Plant J 60:218–226. https://doi.org/10.1111/j.1365-313X.2009.03949.x
Navarro L, Jay F, Nomura K et al (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–967. https://doi.org/10.1126/science.1159505
Nekrasov V, Wang C, Win J et al (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
Nishad R, Ahmed T, Rahman VJ, Kareem A (2020) Modulation of plant defense system in response to microbial interactions. Front Microbiol 11:1298. https://doi.org/10.3389/fmicb.2020.01298
Nishimura MT, Stein M, Hou BH et al (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972. https://doi.org/10.1126/science.1086716
Nødvig CS, Nielsen JB, Kogle ME, Mortensen UH (2015) A CRISPR-Cas9 system for genetic engineering of filamentous fungi. PLoS ONE 10:e0133085. https://doi.org/10.1371/journal.pone.0133085
Nowara D, Gay A, Lacomme C et al (2010) HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–3141. https://doi.org/10.1105/tpc.110.077040
Oliva R, Ji C, Atienza-Grande G et al (2019) Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol 37:1344–1350. https://doi.org/10.1038/s41587-019-0267-z
Ongena M, Jourdan E, Adam A et al (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x
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
Ownley BH, Griffin MR, Klingeman WE et al (2008) Beauveria bassiana: endophytic colonization and plant disease control. J Invertebr Pathol 98:267–270. https://doi.org/10.1016/j.jip.2008.01.010
Panavas T, Serviene E, Brasher J, Nagy PD (2005) Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc Natl Acad Sci 102:7326–7331. https://doi.org/10.1073/pnas.0502604102
Pavan S, Jacobsen E, Visser RGF, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1–12. https://doi.org/10.1007/s11032-009-9323-6
Peng A, Chen S, Lei T et al (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 et al (2016) Knockdown of MLO genes reduces susceptibility to powdery mildew in grapevine. Hortic Res 3:16016. https://doi.org/10.1038/hortres.2016.16
Petersen M, Brodersen P, Naested H et al (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120. https://doi.org/10.1016/S0092-8674(00)00213-0
Pfeilmeier S, George J, Morel A et al (2019) Expression of the Arabidopsis thaliana immune receptor EFR in Medicago truncatula reduces infection by a root pathogenic bacterium, but not nitrogen-fixing rhizobial symbiosis. Plant Biotechnol J 17:569–579. https://doi.org/10.1111/pbi.12999
Phukan UJ, Jeena GS, Tripathi V, Shukla RK (2017) Regulation of Apetala2/Ethylene response factors in plants. Front Plant Sci 8:150. https://doi.org/10.3389/fpls.2017.00150
Pramanik D, Shelake RM, Park J et al (2021) CRISPR/Cas9-mediated generation of pathogen-resistant tomato against tomato yellow leaf curl virus and powdery mildew. Internat J Mol Scie 22:1878. https://doi.org/10.3390/ijms22041878
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
Qiao Y, Liu L, Xiong Q et al (2013) Oomycete pathogens encode RNA silencing suppressors. Nat Genet 45:330–333. https://doi.org/10.1038/ng.2525
Rairdan GJ, Collier SM, Sacco MA et al (2008) The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 20:739–751. https://doi.org/10.1105/tpc.107.056036
Rakha M, Bouba N, Ramasamy S et al (2017) Evaluation of wild tomato accessions (Solanum spp.) for resistance to two-spotted spider mite (Tetranychus urticae Koch) based on trichome type and acylsugar content. Genet Resour Crop Evol 64:1011–1022. https://doi.org/10.1007/s10722-016-0421-0
Rohrlich C, Merle I, Hassani IM et al (2018) Variation in physiological host range in three strains of two species of the entomopathogenic fungus Beauveria. PLoS ONE 13:e0199199. https://doi.org/10.1371/journal.pone.0199199
Römer P, Recht S, Strauß T et al (2010) Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas Oryzae Pv Oryzae. New Phytol 187:1048–1057. https://doi.org/10.1111/j.1469-8137.2010.03217.x
Roy A, Zhai Y, Ortiz J et al (2019) Multiplexed editing of a begomovirus genome restricts escape mutant formation and disease development. PLoS ONE 14:e0223765. https://doi.org/10.1371/journal.pone.0223765
Rybicki EP (2019) CRISPR–Cas9 strikes out in cassava. Nat Biotechnol 37:727–728. https://doi.org/10.1038/s41587-019-0169-0
Ryder LS, Harris BD, Soanes DM et al (2012) Saprotrophic competitiveness and biocontrol fitness of a genetically modified strain of the plant-growth-promoting fungus Trichoderma hamatum GD12. Microbiology. https://doi.org/10.1099/mic.0.051854-0
Santillán Martínez MI, Bracuto V, Koseoglou E et al (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
Savary S, Willocquet L, Pethybridge SJ et al (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439. https://doi.org/10.1038/s41559-018-0793-y
Savenkov EI, Valkonen JPT (2001) Coat protein gene-mediated resistance to Potato virus A in transgenic plants is suppressed following infection with another potyvirus. J Gen Virol 82:2275–2278. https://doi.org/10.1099/0022-1317-82-9-2275
Schwartz AR, Potnis N, Timilsina S et al (2015) Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front Microbiol 6:535. https://doi.org/10.3389/fmicb.2015.00535
Schwessinger B, Bahar O, Thomas N et al (2015) Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLoS Pathog 11:e1004809. https://doi.org/10.1371/journal.ppat.1004809
Scorza R, Ravelonandro M, Callahan AM et al (1994) Transgenic plums (Prunus domestica L.) express the plum pox virus coat protein gene. Plant Cell Rep 14:18–22. https://doi.org/10.1007/BF00233291
Shan Q, Wang Y, Li J et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688. https://doi.org/10.1038/nbt.2650
Shang Y, Duan Z, Huang W et al (2012) Improving UV resistance and virulence of Beauveria bassiana by genetic engineering with an exogenous tyrosinase gene. J Invertebr Pathol 109:105–109. https://doi.org/10.1016/j.jip.2011.10.004
Shen X, Liu H, Yuan B et al (2011) OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant Cell Environ 34:179–191. https://doi.org/10.1111/j.1365-3040.2010.02219.x
Shi Z, Zhang Y, Maximova SN, Guiltinan MJ (2013) TcNPR3 from Theobroma cacao functions as a repressor of the pathogen defense response. BMC Plant Biol 13:204. https://doi.org/10.1186/1471-2229-13-204
So Y, Park S-Y, Park E-H et al (2017) A highly efficient CRISPR-Cas9-mediated large genomic deletion in Bacillus subtilis. Front Microbiol 8:1167. https://doi.org/10.3389/fmicb.2017.01167
Song J-J, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of argonaute and its implications for RISC slicer Activity. Science 305:1434–1437. https://doi.org/10.1126/science.1102514
Spassova MI, Prins TW, Folkertsma RT et al (2001) The tomato gene Sw5 is a member of the coiled coil, nucleotide binding, leucine-rich repeat class of plant resistance genes and confers resistance to TSWV in tobacco. Mol Breed 7:151–161. https://doi.org/10.1023/A:1011363119763
St Leger RJ, Joshi L, Bidochka MJ, Roberts DW (1996) Construction of an improved mycoinsecticide overexpressing a toxic protease. Proc Natl Acad Sci U S A 93:6349–6354. https://doi.org/10.1073/pnas.93.13.6349
St Leger RJ, Wang C (2010) Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Appl Microbiol Biotechnol 85(901):907. https://doi.org/10.1007/s00253-009-2306-z
Streubel J, Pesce C, Hutin M et al (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819. https://doi.org/10.1111/nph.12411
Sun Q, Lin L, Liu D et al (2018) CRISPR/Cas9-mediated multiplex genome editing of the BnWRKY11 and BnWRKY70 genes in Brassica napus L. Int J Mol Sci 19:2716. https://doi.org/10.3390/ijms19092716
Swiderski MR, Birker D, Jones JDG (2009) The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol Plant-Microbe Interact 22:157–165. https://doi.org/10.1094/MPMI-22-2-0157
Tabara H, Sarkissian M, Kelly WG et al (1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99:123–132. https://doi.org/10.1016/S0092-8674(00)81644-X
Tashkandi M, Ali Z, Aljedaani F et al (2018) Engineering resistance against Tomato yellow leaf curl virus via the CRISPR/Cas9 system in tomato. Plant Signal Behav 13:e1525996. https://doi.org/10.1080/15592324.2018.1525996
Thordal-Christensen H (2020) A holistic view on plant effector-triggered immunity presented as an iceberg model. Cell Mol Life Sci. https://doi.org/10.1007/s00018-020-03515-w
Toopaang W, Phonghanpot S, Punya J et al (2017) Targeted disruption of the polyketide synthase gene pks15 affects virulence against insects and phagocytic survival in the fungus Beauveria bassiana. Fungal Biol 121:664–675. https://doi.org/10.1016/j.funbio.2017.04.007
Trębicki P, Finlay K (2018) Pests and diseases under climate change; its threat to food security. In: Food security and climate change. Chichester: John Wiley and Sons Ltd. 229–249. https://doi.org/10.1002/9781119180661.ch11
Tripathi JN, Ntui VO, Ron M et al (2019) CRISPR/Cas9 editing of endogenous banana streak virus in the B genome of Musa spp. overcomes a major challenge in banana breeding. Commun Biol. 2:46. https://doi.org/10.1038/s42003-019-0288-7
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, Kesiraju K, Saakre M et al (2020) Genome editing for resistance to insect pests: an emerging Tool for crop improvement. ACS Omega 5:20674–20683. https://doi.org/10.1021/acsomega.0c01435
Uchiyama A, Shimada-Beltran H, Levy A et al (2014) The Arabidopsis synaptotagmin SYTA regulates the cell-to-cell movement of diverse plant viruses. Front Plant Sci 5:584. https://doi.org/10.3389/fpls.2014.00584
Udompaisarn S, Toopaang W, Sae-Ueng U et al (2020) The polyketide synthase PKS15 has a crucial role in cell wall formation in Beauveria bassiana. Sci Rep 10:12630. https://doi.org/10.1038/s41598-020-69417-w
van der Krol AR, Mur LA, Beld M et al (1990) Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–299. https://doi.org/10.1105/tpc.2.4.291
van Schie CCN, Takken FLW (2014) Susceptibility genes 101: how to be a good host. Annu Rev Phytopathol 52:551–581. https://doi.org/10.1146/annurev-phyto-102313-045854
Verma M, Brar SK, Tyagi RD et al (2007) Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochem Eng J 37:1–20. https://doi.org/10.1016/j.bej.2007.05.012
Voinnet O, Pinto YM, Baulcombe DC (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96:14147–14152. https://doi.org/10.1073/pnas.96.24.14147
Wang M, Dean RA (2020) Movement of small RNAs in and between plants and fungi. Mol Plant Pathol 21:589–601. https://doi.org/10.1111/mpp.12911
Wang C, St Leger RJ (2007) A scorpion neurotoxin increases the potency of a fungal insecticide. Nat Biotechnol 25:1455–1456. https://doi.org/10.1038/nbt1357
Wang Y, Wang Y (2018) Trick or treat: Microbial pathogens evolved apoplastic effectors modulating plant susceptibility to infection. Mol Plant-Microbe Interact 31:6–12. https://doi.org/10.1094/MPMI-07-17-0177-FI
Wang Y, Cheng X, Shan Q et al (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 et al (2016a) 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 G, Liu Z, Lin R et al (2016b) Biosynthesis of antibiotic leucinostatins in bio-control fungus Purpureocillium lilacinum and their inhibition on Phytophthora revealed by genome mining. PLoS Pathog 12:e1005685. https://doi.org/10.1371/journal.ppat.1005685
Wang X, Guo R, Tu M et al (2017) Ectopic expression of the wild grape WRKY transcription factor vqWRKY52 in Arabidopsis thaliana enhances resistance to the biotrophic pathogen powdery mildew but not to the necrotrophic pathogen botrytis cinerea. Front Plant Sci 8:97. https://doi.org/10.3389/fpls.2017.00097
Wang X, Tu M, Wang D et al (2018) CRISPR/Cas9-mediated efficient targeted mutagenesis in grape in the first generation. Plant Biotechnol J 16:844–855. https://doi.org/10.1111/pbi.12832
Wang J, Hu M, Wang J et al (2019) Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364:eaav5870. https://doi.org/10.1126/science.aav5870
Wang L, Chen S, Peng A et al (2019b) CRISPR/Cas9-mediated editing of CsWRKY22 reduces susceptibility to Xanthomonas citri subsp. citri in Wanjincheng orange (Citrus sinensis (L.) Osbeck). Plant Biotechnol Rep 13:501–510. https://doi.org/10.1007/s11816-019-00556-x
Whitham S, Dinesh-Kumar SP, Choi D et al (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115. https://doi.org/10.1016/0092-8674(94)90283-6
Whitham S, McCormick S, Baker B (1996) The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc Natl Acad Sci 93:8776–8781. https://doi.org/10.1073/pnas.93.16.8776
Windbichler N, Menichelli M, Papathanos PA et al (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:212–215. https://doi.org/10.1038/nature09937
Won S-J, Kwon J-H, Kim D-H, Ahn Y-S (2019) The Effect of Bacillus licheniformis MH48 on control of foliar fungal diseases and growth promotion of Camellia oleifera seedlings in the coastal reclaimed land of Korea. Pathogens 8:6. https://doi.org/10.3390/pathogens8010006
Xu Z, Xu X, Gong Q et al (2019) Engineering broad-spectrum bacterial blight resistance by simultaneously disrupting variable TALE-binding elements of multiple susceptibility genes in rice. Mol Plant 12:1434–1446. https://doi.org/10.1016/j.molp.2019.08.006
Xue W-H, Xu N, Yuan X-B et al (2018) CRISPR/Cas9-mediated knockout of two eye pigmentation genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Biochem Mol Biol 93:19–26. https://doi.org/10.1016/j.ibmb.2017.12.003
Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 148:219–222. https://doi.org/10.1016/j.molbiopara.2006.03.013
Yang Z, Li Y (2018) Dissection of RNAi-based antiviral immunity in plants. Curr Opin Virol 32:88–99. https://doi.org/10.1016/j.coviro.2018.08.003
Yi Y, Li Z, Song C, Kuipers OP (2018) Exploring plant-microbe interactions of the rhizobacteria Bacillus subtilis and Bacillus mycoides by use of the CRISPR-Cas9 system. Environ Microbiol 20:4245–4260. https://doi.org/10.1111/1462-2920.14305
Yuan T, Li X, Xiao J, Wang S (2011) Characterization of Xanthomonas oryzae-responsive cis-acting element in the promoter of rice race-specific susceptibility gene Xa13. Mol Plant 4:300–309. https://doi.org/10.1093/mp/ssq076
Zafar K, Khan MZ, Amin I et al (2020) Precise CRISPR-Cas9 mediated genome editing in super basmati rice for resistance against bacterial blight by targeting the major susceptibility gene. Front Plant Sci 11:575. https://doi.org/10.3389/fpls.2020.00575
Zaidi SSA, 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
Zambryski P, Joos H, Genetello C et al (1983) Ti plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity. EMBO J 2:2143–2150. https://doi.org/10.1002/j.1460-2075.1983.tb01715.x
Zeng X, Luo Y, Vu NTQ et al (2020) CRISPR/Cas9-mediated mutation of OsSWEET14 in rice cv. Zhonghua11 confers resistance to Xanthomonas oryzae pv. oryzae without yield penalty. BMC Plant Biol. 20:313. https://doi.org/10.1186/s12870-020-02524-y
Zhan X, Zhang F, Zhong Z et al (2019) Generation of virus-resistant potato plants by RNA genome targeting. Plant Biotechnol J 17:1814–1822. https://doi.org/10.1111/pbi.13102
Zhan Y, Xu Y, Zheng P et al (2020) Establishment and application of multiplexed CRISPR interference system in Bacillus licheniformis. Appl Microbiol Biotechnol 104:391–403. https://doi.org/10.1007/s00253-019-10230-5
Zhang K, Duan X, Wu J (2016) Multigene disruption in undomesticated Bacillus subtilis ATCC 6051a using the CRISPR/Cas9 system. Sci Rep 6:27943. https://doi.org/10.1038/srep27943
Zhang Y, Bai Y, Wu G et al (2017a) Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J 91:714–724. https://doi.org/10.1111/tpj.13599
Zhang Y, Zhao L, Zhao J et al (2017b) S5H/DMR6 Encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiol 175:1082–1093. https://doi.org/10.1104/pp.17.00695
Zhang Z, Ge X, Luo X et al (2018) Simultaneous editing of two copies of GH14-3-3D confers enhanced transgene-clean plant defense against Verticillium dahliae in allotetraploid upland cotton. Front Plant Sci 9:842. https://doi.org/10.3389/fpls.2018.00842
Zhang T, Zhao Y, Ye J et al (2019) Establishing CRISPR/Cas13a immune system conferring RNA virus resistance in both dicot and monocot plants. Plant Biotechnol J 17:1185–1187. https://doi.org/10.1111/pbi.13095
Zhang M, Liu Q, Yang X et al (2020a) CRISPR/Cas9-mediated mutagenesis of Clpsk1 in watermelon to confer resistance to Fusarium oxysporum f.sp. niveum. Plant Cell Rep 39:589–595. https://doi.org/10.1007/s00299-020-02516-0
Zhang Y, Pribil M, Palmgren M, Gao C (2020b) A CRISPR way for accelerating improvement of food crops. Nat Food 1:200–205. https://doi.org/10.1038/s43016-020-0051-8
Zhou J, Peng Z, Long J et al (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–643. https://doi.org/10.1111/tpj.12838
Zhou C, Zhu L, Xie Y et al (2017) Bacillus licheniformis SA03 confers increased saline–alkaline Tolerance in chrysanthemum plants by induction of abscisic acid accumulation. Front Plant Sci 8:1143. https://doi.org/10.3389/fpls.2017.01143
Zhou X, Liao H, Chern M et al (2018) Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc Natl Acad Sci 115:3174–3179. https://doi.org/10.1073/pnas.1705927115
Zhou C, Liu H, Yuan F et al (2019) Development and application of a CRISPR/Cas9 system for Bacillus licheniformis genome editing. Int J Biol Macromol 122:329–337. https://doi.org/10.1016/j.ijbiomac.2018.10.170
Zhu Z, Yin J, Chern M et al (2020) New insights into bsr-d1-mediated broad-spectrum resistance to rice blast. Mol Plant Pathol 21:951–960. https://doi.org/10.1111/mpp.12941
Zipfel C, Kunze G, Chinchilla D et al (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR Restricts Agrobacterium-mediated transformation. Cell 125:749–760. https://doi.org/10.1016/j.cell.2006.03.037
Zou G, Ying SH, Shen ZC, Feng MG (2006) Multi-sited mutations of beta-tubulin are involved in benzimidazole resistance and thermotolerance of fungal biocontrol agent Beauveria bassiana. Environ Microbiol 8:2096–2105. https://doi.org/10.1111/j.1462-2920.2006.01086.x
Zsögön A, Čermák T, Naves ER et al (2018) De novo domestication of wild tomato using genome editing. Nat Biotechnol 36:1211–1216. https://doi.org/10.1038/nbt.4272
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We are grateful to all the researchers whose contributions have been cited, which have helped us to prepare this review paper. We apologize to those authors whose excellent work could not be cited due to space limitations.
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This review was funded by the European Social Fund (ALT20-05-3559-FSE-000036) and the Fundação para a Ciência e Tecnologia (FCT) based on RCM 23/2018 March, 8.
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Rato, C., Carvalho, M.F., Azevedo, C. et al. Genome editing for resistance against plant pests and pathogens. Transgenic Res 30, 427–459 (2021). https://doi.org/10.1007/s11248-021-00262-x
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DOI: https://doi.org/10.1007/s11248-021-00262-x