Skip to main content
Log in

The status of the CRISPR/Cas9 research in plant–nematode interactions

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

As an important biotic stressor, plant–parasitic nematodes afflict global crop productivity. Deployment of CRISPR/Cas9 system that selectively knock out host susceptibility genes conferred improved nematode tolerance in crop plants.

Abstract

As an important biotic stressor, plant–parasitic nematodes cause a considerable yield decline in crop plants that eventually contributes to a negative impact on global food security. Being obligate plant parasites, the root-knot and cyst nematodes maintain an intricate and sophisticated relationship with their host plants by hijacking the host’s physiological and metabolic pathways for their own benefit. Significant progress has been made toward developing RNAi-based transgenic crops that confer nematode resistance. However, the strategy of host-induced gene silencing that targets nematode effectors is likely to fail because the induced silencing of effectors (which interact with plant R genes) may lead to the development of nematode phenotypes that break resistance. Lately, the CRISPR/Cas9-based genome editing system has been deployed to achieve host resistance against bacteria, fungi, and viruses. In these studies, host susceptibility (S) genes were knocked out to achieve resistance via loss of susceptibility. As the S genes are recessively inherited in plants, induced mutations of the S genes are likely to be long-lasting and confer broad-spectrum resistance. A number of S genes contributing to plant susceptibility to nematodes have been identified in Arabidopsis thaliana, rice, tomato, cucumber, and soybean. A few of these S genes were targeted for CRISPR/Cas9-based knockout experiments to improve nematode tolerance in crop plants. Nevertheless, the CRISPR/Cas9 system was mostly utilized to interrogate the molecular basis of plant–nematode interactions rather than direct research toward achieving tolerance in crop plants. The current standalone article summarizes the progress made so far on CRISPR/Cas9 research in plant–nematode interactions.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

References

  • Ahmad S, Wei X, Sheng Z, Hu P, Tang S (2020) CRISPR/Cas9 for development of disease resistance in plants: recent progress, limitations and future prospects. Brief Funct Genomics. 19:26–39. https://doi.org/10.1093/bfgp/elz041

    Article  CAS  PubMed  Google Scholar 

  • Ali MA, Azeem F, Abbas A, Joyia FA, Li H, Dababat AA (2017) Transgenic strategies for enhancement of nematode resistance in plants. Front Plant Sci 8:750

    PubMed  PubMed Central  Google Scholar 

  • Barbary A, Djian-Caporalino C, Palloix A, Castagnone-Sereno P (2015) Host genetic resistance to root-knot nematodes, Meloidogyne spp., in Solanaceae: from genes to the field. Pest Manag Sci 71:1591–1598

    CAS  PubMed  Google Scholar 

  • Blanvillain-Baufumé S, Reschke M, Solé M, Auguy F, Doucoure H, Szurek B, Meynard D, Portefaix M, Cunnac S, Guiderdoni E, Boch J, Koebnik R (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

    PubMed  Google Scholar 

  • Cabral D, Forero Ballesteros H, de Melo BP, Lourenço-Tessutti IT, Simões de Siqueira KM, Obicci L, Grossi-de-Sa MF, Hemerly AS, de Almeida EJ (2021) The Armadillo BTB Protein ABAP1 is a crucial player in DNA replication and transcription of nematode-induced galls. Front Plant Sci 12:636663

    PubMed  PubMed Central  Google Scholar 

  • Cabrera J, Díaz-Manzano FE, Sanchez M, Rosso MN, Melillo T, Goh T, Fukaki H, Cabello S, Hofmann J, Fenoll C, Escobar C (2014) A role for LATERAL ORGAN BOUNDARIES-DOMAIN 16 during the interaction Arabidopsis-Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development. New Phytol 203:632–645

    CAS  PubMed  Google Scholar 

  • Caillaud MC, Lecomte P, Jammes F, Quentin M, Pagnotta S, Andrio E, de Almeida EJ, Marfaing N, Gounon P, Abad P, Favery B (2008) MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis. Plant Cell 20:423–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cardi T, Murovec J, Bakhsh A, Boniecka J, Bruegmann T, Bull SE et al (2023) CRISPR/Cas-mediated plant genome editing: outstanding challenges a decade after implementation. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2023.05.012

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhary S, Dutta TK, Tyagi N, Shivakumara TN, Papolu PK, Chobhe KA, Rao U (2019) Host-induced silencing of Mi-msp-1 confers resistance to root-knot nematode Meloidogyne incognita in eggplant. Transgenic Res 28:327–340

    CAS  PubMed  Google Scholar 

  • Chen JS, Hu LL, Sun LH, Lin BR, Huang K, Zhuo K et al (2018) A novel Meloidogyne graminicola effector, MgMO237, interacts with multiple host defence related proteins to manipulate plant basal immunity and promote parasitism. Mol Plant Pathol 19:1942–1955

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnapandi B, Bucki P, Braun Miyara S (2017) SlWRKY45, nematode-responsive tomato WRKY gene, enhances susceptibility to the root knot nematode M. javanica infection. Plant Signal Behav 12:e1356530

    PubMed  PubMed Central  Google Scholar 

  • Clément M, Ketelaar T, Rodiuc N, Banora MY, Smertenko A, Engler G, Abad P, Hussey PJ, de Almeida EJ (2009) Actin-depolymerizing factor2-mediated actin dynamics are essential for root-knot nematode infection of Arabidopsis. Plant Cell 21:2963–2979

    PubMed  PubMed Central  Google Scholar 

  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823

    CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis RH, Pankaj PSJ, Napier J, Matthes MC (2013) The Arabidopsis F-box/Kelch-repeat protein At2g44130 is upregulated in giant cells and promotes nematode susceptibility. Mol Plant Microbe Interact 26:36–43

    CAS  PubMed  Google Scholar 

  • Dash M, Somvanshi VS, Godwin J, Budhwar R, Sreevathsa R, Rao U (2022) Exploring genomic variations in nematode-resistant mutant rice lines. Front Plant Sci 13:823372

    PubMed  PubMed Central  Google Scholar 

  • de Almeida EJ, Kyndt T, Vieira P, Van Cappelle E, Boudolf V, Snchez V, Escobar C, De Veylder L, Engler G, Abad P, Gheysen G (2012) CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites. Plant J 72:185–198

    Google Scholar 

  • Ding S, Cheng X, Wang D, Chen C, Yang S, Wang J, Xu C, Xie H (2022) Aphelenchoides besseyi Ab-FAR-1 interacts with Arabidopsis thaliana AtADF3 to interfere with actin cytoskeleton, and promotes nematode parasitism and pathogenicity. Int J Mol Sci 23:12280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, VandeCasteele C, Faure I, Brunoud G, Pijarowski L, Palloix A, Lefebvre V, Abad P (2007) Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 114:473–486

    CAS  PubMed  Google Scholar 

  • Dong J, Zielinski RE, Hudson ME (2020) t-SNAREs bind the Rhg1 alpha-SNAP and mediate soybean cyst nematode resistance. Plant J 104:318–331

    CAS  PubMed  Google Scholar 

  • Dutta TK, Banakar P, Rao U (2015a) The status of RNAi-based transgenic research in plant nematology. Front Microbiol 5:760

    PubMed  PubMed Central  Google Scholar 

  • Dutta TK, Papolu PK, Banakar P, Choudhary D, Sirohi A, Rao U (2015b) Tomato transgenic plants expressing hairpin construct of a nematode protease gene conferred enhanced resistance to root-knot nematodes. Front Microbiol 6:260

    PubMed  PubMed Central  Google Scholar 

  • Dutta TK, Khan MR, Phani V (2019) Plant-parasitic nematode management via biofumigation using brassica and non-brassica plants: current status and future prospects. Curr Plant Biol 17:17–32

    Google Scholar 

  • Dutta TK, Papolu PK, Singh D, Sreevathsa R, Rao U (2020) Expression interference of a number of Heterodera avenae conserved genes perturbs nematode parasitic success in Triticum aestivum. Plant Sci 301:110670

    CAS  PubMed  Google Scholar 

  • Dutta TK, Phani V (2023) The pervasive impact of global climate change on plant-nematode interaction continuum. Front Plant Sci 14:1143889

    PubMed  PubMed Central  Google Scholar 

  • Dutta TK, Vashisth N, Ray S, Phani V, Chinnusamy V, Sirohi A (2023) Functional analysis of a susceptibility gene (HIPP27) in the Arabidopsis thaliana-Meloidogyne incognita pathosystem by using a genome editing strategy. BMC Plant Biol 23:390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elashry A, Okumoto S, Siddique S, Koch W, Kreil DP, Bohlmann H (2013) The AAP gene family for amino acid permeases contributes to development of the cyst nematode Heterodera schachtii in roots of Arabidopsis. Plant Physiol Biochem 70:379–386

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elling AA (2013) Major emerging problems with minor Meloidogyne species. Phytopathology 103:1092–1102

    PubMed  Google Scholar 

  • El-Sappah AH, Islam MM, El-awady H, Yan S, Qi S, Liu J, Cheng G, Liang Y (2019) Tomato natural resistance genes in controlling the root-knot nematode. Genes 10:925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136

    CAS  PubMed  Google Scholar 

  • Escobar C, Barcala M, Portillo M, Almoguera C, Jordano J, Fenoll C (2003) Induction of the Hahsp17.7G4 promoter by root-knot nematodes: involvement of heat-shock elements in promoter activity in giant cells. Mol Plant Microbe Interact 16:1062–1068

    CAS  PubMed  Google Scholar 

  • Eves-van den Akker S (2021) Plant–nematode interactions. Curr Opin Plant Biol 62:102035

    CAS  PubMed  Google Scholar 

  • Evogene-TMG announcement (2018) Evogene and TMG announce collaboration to develop nematode resistant soybean through genome editing. https://www.evogene.com/press_release/evogene-and-tmg-announce-collaboration-to-develop-nematode-resistant-soybean-through-genome-editing/.

  • FAO (2022) Gene editing and agrifood systems. Rome. https://doi.org/10.4060/cc3579en

    Article  Google Scholar 

  • Favery B, Chelysheva LA, Lebris M, Jammes F, Marmagne A, de Almeida-Engler J, Lecomte P, Vaury C, Arkowitz RA, Abad P (2004) Arabidopsis formin AtFH6 is a plasma membrane–associated protein upregulated in giant cells induced by parasitic nematodes. Plant Cell 16:2529–2540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Favery B, Lecomte P, Gil N, Bechtold N, Bouchez D, Dalmasso A, Abad P (1998) RPE, a plant gene involved in early developmental steps of nematode feeding cells. EMBO J 17:6799–6811

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fitoussi N, Borrego E, Kolomiets MV, Qing X, Bucki P, Sela N et al (2021) Oxylipins are implicated as communication signals in tomato–root-knot nematode (Meloidogyne javanica) interaction. Sci Rep 11:326

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gheysen G, Jones JT (2006) Molecular aspects of plant-nematode interactions. In: Perry RN, Moens M (eds) Plant nematology. CAB International Publishers, Wallingford, pp 234–254

    Google Scholar 

  • Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gleason C, Leelarasamee N, Meldau D, Feussner I (2016) OPDA has key role in regulating plant susceptibility to the root-knot nematode Meloidogyne hapla in Arabidopsis. Front Plant Sci 7:1565

    PubMed  PubMed Central  Google Scholar 

  • 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 eIF 4E isoforms nCBP-1 and nCBP-2 reduces cassava brown streak disease symptom severity and incidence. Plant Biotechnol J 17:421–434

    CAS  PubMed  Google Scholar 

  • Gruner K, Esser T, Acevedo-Garcia J, Freh M, Habig M, Strugala R, Stukenbrock E, Schaffrath U, Panstruga R (2020) Evidence for allele- specific levels of enhanced susceptibility of wheat mlo mutants to the hemibiotrophic fungal pathogen Magnaporthe oryzae pv. Triticum Genes 11:517

    CAS  PubMed  Google Scholar 

  • Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358–368

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Zhao W, Qiao H, Li C, Sun L, Yang R, Ma S, Ma J, Song S, Wang S (2022) SlWRKY45 interacts with jasmonate-ZIM domain proteins to negatively regulate defense against the root-knot nematode Meloidogyne incognita in tomato. Hortic Res 9:uhac197

    PubMed  PubMed Central  Google Scholar 

  • Huang Q, Lin B, Cao Y, Zhang Y, Song H, Huang C, Sun T, Long C, Liao J, Zhuo K (2023) CRISPR/Cas9-mediated mutagenesis of the susceptibility gene OsHPP04 in rice confers enhanced resistance to rice root-knot nematode. Front Plant Sci 14:1134653

    PubMed  PubMed Central  Google Scholar 

  • Jiang F, Doudna JA (2017) CRISPR–Cas9 structures and mechanisms. Annu Rev Biophys 46:505–529

    CAS  PubMed  Google Scholar 

  • Jin J, Hewezi T, Baum TJ (2011) The Arabidopsis bHLH25 and bHLH27 transcription factors contribute to susceptibility to the cyst nematode Heterodera schachtii. Plant J 65:319–328

    CAS  PubMed  Google Scholar 

  • Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang J (2016) Application of CRISPR/Cas9-mediated genome editing for studying soybean resistance to soybean cyst nematode. Doctoral thesis, University of Missouri, Columbia, Missouri, USA.

  • Kikuchi T, Eves-van den Akker S, Jones JT (2017) Genome evolution of plant-parasitic nematodes. Annu Rev Phytopathol 55:333–354

    CAS  PubMed  Google Scholar 

  • Li S, Lin D, Zhang Y, Deng M, Chen Y, Lv B, Li B, Lei Y, Wang Y, Zhao L, Liang Y, Liu J, Chen K, Liu Z, Xiao J, Qiu J-L, Gao C (2022a) Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 602:455–460

    CAS  PubMed  Google Scholar 

  • Li Z, Huang Q, Lin B, Guo B, Wang J, Huang C, Liao J, Zhuo K (2022b) CRISPR/Cas9-targeted mutagenesis of a representative member of a novel PR10/Bet v1-like protein subfamily significantly reduces rice plant height and defense against Meloidogyne graminicola. Phytopathol Res 4:38

    CAS  Google Scholar 

  • Liang G, Zhang H, Lou D, Yu D (2016) Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing. Sci Rep 6:21451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin B, Zhuo K, Chen S, Hu L, Sun L, Wang X, Zhang L-H, Liao J (2016) A novel nematode effector suppresses plant immunity by activating host reactive oxygen species-scavenging system. New Phytol 209:1159–1173

    CAS  PubMed  Google Scholar 

  • Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826

    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

    CAS  PubMed  Google Scholar 

  • Mantelin S, Thorpe P, Jones JT (2017) Translational biology of nematode effectors. Or, to put it another way, functional analysis of effectors–what’s the point? Nematology 19:251–261

    CAS  Google Scholar 

  • Mehta D (2023) EU proposal on CRISPR-edited crops is welcome—but not enough. Nature 619:437. https://doi.org/10.1038/d41586-023-02328-8

    Article  CAS  PubMed  Google Scholar 

  • Mejias J, Bazin J, Truong NM, Chen Y, Marteu N, Bouteiller N et al (2021) The root-knot nematode effector MiEFF18 interacts with the plant core spliceosomal protein SmD1 required for giant cell formation. New Phytol 229:3408–3423

    CAS  PubMed  Google Scholar 

  • Mejias J, Truong NM, Abad P, Favery B, Quentin M (2019) Plant proteins and processes targeted by parasitic nematode effectors. Front Plant Sci 10:970

    PubMed  PubMed Central  Google Scholar 

  • Mejias J, Chen Y, Bazin J, Truong NM, Mulet K, Noureddine Y, Jaubert-Possamai S, Ranty-Roby S, Soulé S, Abad P, Crespi MD, Favery B, Quentin M (2022) Silencing the conserved small nuclear ribonucleoprotein SmD1 target gene alters susceptibility to root-knot nematodes in plants. Plant Physiol 189:1741–1756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, Davis EL (2013) Nematode effector proteins: an emerging paradigm of parasitism. New Phytol 199:879–894

    PubMed  Google Scholar 

  • Molla KA, Sretenovic S, Bansal KC, Qi Y (2021) Precise plant genome editing using base editors and prime editors. Nat Plants 7:1166–1187

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Noureddine Y, da Rocha M, An J, Médina C, Mejias J, Mulet K, Quentin M, Abad P, Zouine M, Favery B, Jaubert-Possamai S (2023) AUXIN RESPONSIVE FACTOR-8 regulates development of feeding site induced by root knot nematodes in tomato. J Exp Bot 74:5752–5766. https://doi.org/10.1093/jxb/erad208

    Article  PubMed  Google Scholar 

  • Oikawa K, Fujisaki K, Shimizu M, Takeda T, Saitoh H, Hirabuchi A, Hiraka Y, Bialas A, Langner T, Kellner R, Bozkurt TO, Cesari S, Kroj T, Maidment JHR, Banfield MJ, Kamoun S, Terauchi R (2020) The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity. bioRxiv. https://doi.org/10.1101/2020.12.01.406389

    Article  Google Scholar 

  • Oliva R, Ji C, Atienza-Grande G, Huguet-Tapia JC, Perez-Quintero A, Li T, Eom JS, Li C, Nguyen H, Liu B, Auguy F, Sciallano C, Luu VT, Dossa GS, Cunnac S, Schmidt SM, Slamet-Loedin IH, Cruz CV, Szurek B, Frommer WB, White FF, Yang B (2019) Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol 37:1344–1350

    CAS  PubMed  PubMed Central  Google Scholar 

  • Olmo R, Cabrera J, Fenoll C, Escobar C (2019) A role for ALF4 during gall and giant cell development in the biotic interaction between Arabidopsis and Meloidogyne spp. Physiol Plant 165:17–28

    CAS  PubMed  Google Scholar 

  • Paal J, Henselewski H, Muth J, Meksem K, Menéndez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297

    CAS  PubMed  Google Scholar 

  • Pariyar SR, Nakarmi J, Anwer MA, Siddique S, Ilyas M, Elashry A, Dababat AA, Leon J, Grundler FM (2018) Amino acid permease 6 modulates host response to cyst nematodes in wheat and Arabidopsis. Nematology 20:737–750

    CAS  Google Scholar 

  • Pariyar SR, Dababat AA, Sannemann W, Erginbas-Orakci G, Elashry A, Siddique S, Morgounov A, Leon J, Grundler FM (2016) Genome-wide association study in wheat identifies resistance to the cereal cyst nematode Heterodera filipjevi. Phytopathology 106:1128–1138

    CAS  PubMed  Google Scholar 

  • Pavan S, Jacobsen E, Visser RG, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1–12

    PubMed  Google Scholar 

  • Phani V, Khan MR, Dutta TK (2021) Plant-parasitic nematodes as a potential threat to protected agriculture: current status and management options. Crop Prot 144:105573

    Google Scholar 

  • Phani V, Gowda MT, Dutta TK (2023) Grafting vegetable crops to manage plant-parasitic nematodes: a review. J Pest Sci. https://doi.org/10.1007/s10340-023-01658-w

    Article  Google Scholar 

  • Pires D, Vicente CS, Menéndez E, Faria JM, Rusinque L, Camacho MJ, Inácio ML (2022) The fight against plant-parasitic nematodes: current status of bacterial and fungal biocontrol agents. Pathogens 11:1178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pixley KV, Falck-Zepeda JB, Giller KE, Glenna LL, Gould F, Mallory-Smith CA et al (2019) Genome editing, gene drives, and synthetic biology: will they contribute to disease resistant crops, and who will benefit? Annu Rev Phytopathol 57:165–188

    CAS  PubMed  Google Scholar 

  • Pixley KV, Falck-Zepeda JB, Paarlberg RL, Phillips PW, Slamet-Loedin IH, Dhugga KS, Campos H, Gutterson N (2022) Genome-edited crops for improved food security of smallholder farmers. Nat Genet 54:364–367

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Radakovic ZS, Anjam MS, Escobar E, Chopra D, Cabrera J, Silva AC, Escobar C, Sobczak M, Grundler FM, Siddique S (2018) Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii. Mol Plant Pathol 19:1917–1928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Różańska E, Krępski T, Wiśniewska A (2023) Mutations in selected ABA-related genes reduce level of Arabidopsis thaliana susceptibility to the beet cyst nematode Heterodera schachtii. Plants 12:2299

    PubMed  PubMed Central  Google Scholar 

  • Shivakumara TN, Chaudhary S, Kamaraju D, Dutta TK, Papolu PK, Banakar P, Sreevathsa R, Singh B, Manjaiah KM, Rao U (2017) Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant. Front Plant Sci 8:473

    PubMed  PubMed Central  Google Scholar 

  • Siddique S, Eves-van den Akker S (2022) Nematode management through genome editing. In: Sikora RA, Desaeger J, Molendijk LPG (eds) Integrated nematode management state-of-the-art and visions for the future. CAB International, Wallingford, pp 408–413

    Google Scholar 

  • Siddique S, Radakovic ZS, Hiltl C, Pellegrin C, Baum TJ, Beasley H, Bent AF, Chitambo O, Chopra D, Danchin EGJ, Grenier E, Habash SSS, Hasan MS, Helder J, Heweji T, Holbein J, Holterman M, Janakowski S, Koutsovoulos GD, Kranse OP, Lozano-Torres JL, Maier TR, Masonbrink RE, Mendy B, Riemer E, Sobzak M, Sonawala U, Sterken MG, Thorpe P, van Steenbrugge JJM, Zahid N, Grundler F, Eves-van den Akker S (2022) The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5. Nat Commun 13:6190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song H, Lin B, Huang Q, Sun L, Chen J, Hu L, Zhuo K, Liao J (2021) The Meloidogyne graminicola effector MgMO289 targets a novel copper metallochaperone to suppress immunity in rice. J Exp Bot 72:5638–5655

    CAS  PubMed  Google Scholar 

  • Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki R, Yamada M, Higaki T, Aida M, Kubo M, Tsai AY, Sawa S (2021) PUCHI regulates giant cell morphology during root-knot nematode infection in Arabidopsis thaliana. Front Plant Sci 12:755610

    PubMed  PubMed Central  Google Scholar 

  • Suzuki R, Kanno Y, Abril-Urias P, Seo M, Escobar C, Tsai AY-L, Sawa S (2022) Local auxin synthesis mediated by YUCCA4 induced during root-knot nematode infection positively regulates gall growth and nematode development. Front Plant Sci 13:1019427

    PubMed  PubMed Central  Google Scholar 

  • Tripathi L, Dhugga KS, Ntui VO, Runo S, Syombua ED, Muiruri S, Wen Z, Tripathi JN (2022) Genome editing for sustainable agriculture in Africa. Front Genome Edit 4:876697

    Google Scholar 

  • Truong NM, Chen Y, Mejias J, Soulé S, Mulet K, Jaouannet M, Jaubert-Possamai S, Sawa S, Abad P, Favery B, Quentin M (2021) The Meloidogyne incognita nuclear effector MiEFF1 interacts with Arabidopsis cytosolic glyceraldehyde-3-phosphate dehydrogenases to promote parasitism. Front Plant Sci 12:641480

    PubMed  PubMed Central  Google Scholar 

  • Uranga M, Daròs JA (2022) Tools and targets: the dual role of plant viruses in CRISPR–Cas genome editing. Plant Genome e20220

  • Van Der Vossen EAG, Van Der Voort JNAMR, Kanyuka K, Bendahmane A, Sandbrink H, Baulcombe DC, Bakker J, Stiekema WJ, Klein-Lankhorst RM (2000) Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J 23:567–576

    PubMed  Google Scholar 

  • van Schie CC, Takken FL (2014) Susceptibility genes 101: how to be a good host. Annu Rev Phytopathol 52:551–581

    PubMed  Google Scholar 

  • van Steenbrugge JJ, van den Elsen S, Holterman M, Lozano-Torres JL, Putker V, Thorpe P, Goverse A, Sterken MG, Smant G, Helder J (2023) Comparative genomics among cyst nematodes reveals distinct evolutionary histories among effector families and an irregular distribution of effector-associated promoter motifs. Mol Ecol 32:1515–1529

    PubMed  Google Scholar 

  • Verhoeven A, Finkers-Tomczak A, Prins P, Valkenburg-van Raaij DR, van Schaik CC, Overmars H, van Steenbrugge JJM, Tacken W, Varossieau K, Slootweg EJ, Kappers IF, Quentin M, Goverse A, Sterken MG, Smant G (2022) The root-knot nematode effector MiMSP32 targets host 12-oxophytodienoate reductase 2 (OPR2) to regulate plant susceptibility. New Phytol. https://doi.org/10.1111/nph.18653

    Article  PubMed  PubMed Central  Google Scholar 

  • Verma A, Lee C, Morriss S, Odu F, Kenning C, Rizzo N et al (2018) The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites. New Phytol 219:697–713

    CAS  PubMed  Google Scholar 

  • Vieira P, De Clercq A, Stals H, Van Leene J, Van De Slijke E, Van Isterdael G, Eeckhout D, Persiau G, Van Damme D, Verkest A, de Souza JDA, Glab J, Abad P, Engler G, Inze D, de Veylder L, De Jaeger G, de Almeida EJ (2014) The cyclin-dependent kinase inhibitor KRP6 induces mitosis and impairs cytokinesis in giant cells induced by plant-parasitic nematodes in Arabidopsis. Plant Cell 26:2633–2647

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira P, Gleason C (2019) Plant-parasitic nematode effectors-insights into their diversity and new tools for their identification. Curr Opin Plant Biol 50:37–43

    CAS  PubMed  Google Scholar 

  • Voytas DF (2013) Plant genome engineering with sequence-specific nucleases. Annu Rev Plant Biol 64:327–350

    CAS  PubMed  Google Scholar 

  • Wang LH, Gu XH, Hua MY, Mao SL, Zhang ZH, Peng DL, Yun XF, Zhang BX (2009) A SCAR marker linked to the N gene for resistance to root knot nematodes (Meloidogyne spp.) in pepper (Capsicum annuum L.). Sci Hortic 122:318–322

    CAS  Google Scholar 

  • Wang X, Cheng R, Xu D, Huang R, Li H, Jin L, Wu Y, Tang J, Sun C, Peng D, Chu C, Guo X (2023) MG1 interacts with a protease inhibitor and confers resistance to rice root-knot nematode. Nat Commun 14:3354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Warmerdam S, Sterken MG, van Schaik C, Oortwijn MEP, Sukarta OCA, Lozano-Torres JL, Dicke M, Helder J, Kammenga JE, Goverse A, Bakker J, Smant G (2018) Genome-wide association mapping of the architecture of susceptibility to the root-knot nematode Meloidogyne incognita in Arabidopsis thaliana. New Phytol 218:724–737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Warmerdam S, Sterken MG, van Schaik C, Oortwijn MEP, Lozano-Torres JL, Bakker J, Goverse A, Smant G (2019) Mediator of tolerance to abiotic stress ERF6 regulates susceptibility of Arabidopsis to Meloidogyne incognita. Mol Plant Pathol 20:137–152

    CAS  PubMed  Google Scholar 

  • Wheatley MS, Yang Y (2021) Versatile applications of the CRISPR/Cas toolkit in plant pathology and disease management. Phytopathology 111:1080–1090

    CAS  PubMed  Google Scholar 

  • Wubben MJ 2nd, Su H, Rodermel SR, Baum TJ (2001) Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol Plant Microbe Interact 14:1206–1212

    CAS  PubMed  Google Scholar 

  • Xu Z, Xu X, Gong Q, Li Z, Li Y, Wang S, Yang Y, Ma W, Liu L, Zhu B, Zou L, Chen G (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

    CAS  PubMed  Google Scholar 

  • Zaidi SS, Mukhtar MS, Mansoor S (2018) Genome editing: targeting susceptibility genes for plant disease resistance. Trends Biotechnol 36:898–906

    CAS  PubMed  Google Scholar 

  • Zafirov D, Giovinazzo N, Bastet A, Gallois JL (2021) When a knockout is an Achilles’ heel: resistance to one potyvirus species triggers hypersusceptibility to another one in Arabidopsis thaliana. Mol Plant Pathol 22:334–347

    CAS  PubMed  Google Scholar 

  • Zhang X, Wang D, Chen J, Wu D, Feng X, Yu F (2021) Nematode RALF-like 1 targets soybean Malectin-like receptor kinase to facilitate parasitism. Front Plant Sci 12:775508

    PubMed  PubMed Central  Google Scholar 

  • Zhang X, Li S, Li X, Song M, Ma S, Tian Y, Gao L (2023) Peat-based hairy root transformation using Rhizobium rhizogenes as a rapid and efficient tool for easily exploring potential genes related to root-knot nematode parasitism and host response. Plant Methods 19:22

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Li L, Liu Q, Liu P, Li S, Yang D, Chen Y, Pagnotta S, Favery B, Abad P, Jian H (2019) A MIF-like effector suppresses plant immunity and facilitates nematode parasitism by interacting with plant annexins. J Exp Bot 70:5943–5958

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Liang J, Huang H, Yang J, Feng J, Sun L, Yang R, Zhao M, Wang J, Wang S (2023) Tomato defence against Meloidogyne incognita by jasmonic acid-mediated fine-tuning of kaempferol homeostasis. New Phytol. https://doi.org/10.1111/nph.18837

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Zhao D, Duan Y, Chen L, Fan H, Wang Y, Liu X, Chen L-Q, Xuan Y, Zhu X (2023a) AtSWEET1 negatively regulates plant susceptibility to root-knot nematode disease. Front Plant Sci 14:1010348

    PubMed  PubMed Central  Google Scholar 

  • Zhou D, Godinez-Vidal D, He J, Teixeira M, Guo J, Wei L, Norman JMV, Kaloshian I (2023b) A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes. Plant Physiol. https://doi.org/10.1093/plphys/kiad253

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

TKD and SR wrote the first draft. TKD, SR and VP prepared the illustrations. TKD edited the final draft. All the authors read and approved the final draft.

Corresponding author

Correspondence to Tushar K. Dutta.

Ethics declarations

Conflict of interest

Authors declare that they have no potential conflict of interests.

Additional information

Communicated by Gerhard Leubner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dutta, T.K., Ray, S. & Phani, V. The status of the CRISPR/Cas9 research in plant–nematode interactions. Planta 258, 103 (2023). https://doi.org/10.1007/s00425-023-04259-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-023-04259-0

Keywords

Navigation