CRISPR/Cas Technology in Resistance to Phytopathogens

Year 2020, Issue: 20, 693 - 702, 31.12.2020

Serap Demirel , Mustafa Usta , Fatih Demirel

https://doi.org/10.31590/ejosat.765369

Cited By: 1

Abstract

The intracellular and extracellular plant pathogens cause economically significant loss to agricultural products worldwide. Genome editing technologies, especially the CRISPR/cas system, have recently been used in different fields in order to improve both quality and yield in agricultural products. The CRISPR/cas system which provides defense in microorganisms against bacteria, archaea, phage and foreign plasmids is a tool that offers unique opportunities for research and regulation of agricultural properties. In this review, the effectiveness of the CRSPR/cas system in the fight against phyto-pathogens causing diseases was discussed. In addition, the current status of modifications through the CRISPR/cas system of genes that play a role in resistance and susceptibility to the host plant against fungi, bacteria and viruses was revealed. The CRISPR/cas system has been shown to be effective in providing resistance to phyto-pathogens that have destructive effects on plants. Advances in genome editing and the production of transgene-free plants with CRISPR/Cas will enable the development of new disease management and control strategies in plant pathology. In the future, it will be possible to develop resistant plants to more than one pathogen simultaneously with CRISPR/cas genome editing technology.

Keywords

CRISPR,, genome editing, phyto-pathogens, plant breeding, sustainable agriculture

Fitopatojenlere Karşı Dayanıklılıkta CRISPR/Cas Teknolojisi

Abstract

Tarım ürünlerinde hem hücre içi hem hücre dışı bitki patojenleri dünya çapında ekonomik olarak önemli kayıplara neden olmaktadır. Genom düzenleme teknolojileri özellikle de CRISPR/cas sistemi, tarım ürünlerinde gerek kalite gerekse verimin iyileştirilmesi amacıyla son zamanlarda farklı alanlarda kullanılmıştır. Bakteri, arkea, faj ve yabancı plazmitlere karşı savunma sağlayan CRISPR/cas sistemi tarımsal özelliklerin araştırılması ve düzenlenmesi için eşsiz fırsatlar sunan bir araçtır. Bu derlemede hastalıklara neden olan fitopatojenlere karşı mücadelede CRSPR/cas sisteminin kullanım etkinliği irdelenmiştir. Ayrıca CRISPR/cas sistemi aracılığıyla fungus, bakteri ve virüslere karşı konukçu bitkide dayanıklılık ve duyarlılıkta rol oynayan genlerin modifikasyonlarının mevcut durumu ortaya konmuştur. Çalışmalar, CRISPR/cas sisteminin bitkilerde fitopatojenlere karşı dayanıklılık sağlamada etkili olduğunu ortaya koymuştur. Genom düzenleme alanındaki ilerlemeler ve CRISPR/cas ile transgen içermeyen bitkilerin elde edilmesi gelecekte bitki patolojisinde yeni hastalık yönetim ve mücadele stratejilerinin geliştirilmesine olanak sağlayabilecektir. Ayrıca gelecekte CRISPR/cas genom düzenleme teknolojisi ile birden fazla patojene eş zamanlı olarak dayanıklı bitkilerin geliştirilmesi de mümkün olabilecektir.

Keywords

CRISPR,, genom düzenleme,, fitopatojenler,, bitki ıslahı,, sürdürülebilir tarım,

References

• Abudayyeh, O. O., Gootenberg, J. S., Konermann, S., Joung, J., Slaymaker, I. M., Cox, D. B., ... & Severinov, K. (2016). C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353(6299), aaf5573.
• Abudayyeh, O. O., Gootenberg, J. S., Essletzbichler, P., Han, S., Joung, J., Belanto, J. J., ... & Lander, E. S. (2017). RNA targeting with CRISPR–Cas13. Nature, 550(7675), 280-284.
• AKBUDAK, M. A., & Kontbay, K. (2017). Yeni Nesil Genom Düzenleme Teknikleri: ZFN, TALEN, CRISPR’lar ve Bitkilerde Kullanımı. Tarla Bitkileri Merkez Araştırma Enstitüsü Dergisi, 26(1), 111-126.
• Ali, Z., Abulfaraj, A., Idris, A., Ali, S., Tashkandi, M., & Mahfouz, M. M. (2015). CRISPR/Cas9-mediated viral interference in plants. Genome biology, 16(1), 238.
• Ali, Z., Ali, S., Tashkandi, M., Zaidi, S. S. E. A., & Mahfouz, M. M. (2016). CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Scientific reports, 6(1), 1-13.
• Aman, R., Ali, Z., Butt, H., Mahas, A., Aljedaani, F., Khan, M. Z., ... & Mahfouz, M. (2018). RNA virus interference via CRISPR/Cas13a system in plants. Genome biology, 19(1), 1-9.
• Arora, L., & Narula, A. (2017). Gene editing and crop improvement using CRISPR-Cas9 system. Frontiers in plant science, 8, 1932.
• Ateş Sönmezoğlu, Ö., Yıldırım, A., Türk, Ü., & Yanar, Y. (2019). Bazı Yerel Makarnalık Buğday Çeşitlerinde Küllemeye (Blumeria graminis f. sp. tritici) Karşı Dayanıklılığın Belirlenmesi. Avrupa Bilim ve Teknoloji Dergisi, (17), 944-950.
• Baltes, N. J., Hummel, A. W., Konecna, E., Cegan, R., Bruns, A. N., Bisaro, D. M., & Voytas, D. F. (2015). Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nature Plants, 1(10), 1-4.
• Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., ... & Horvath, P. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315(5819), 1709-1712.
• Bayat, H., Naderi, F., Khan, A. H., Memarnejadian, A., & Rahimpour, A. (2018). The impact of crispr-cas system on antiviral therapy. Advanced Pharmaceutical Bulletin, 8(4), 591.
• Borrelli, V. M., Brambilla, V., Rogowsky, P., Marocco, A., & Lanubile, A. (2018). The enhancement of plant disease resistance using CRISPR/Cas9 technology. Frontiers in plant science, 9, 1245.
• Bortesi, L., & Fischer, R. (2015). The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnology advances, 33(1), 41-52.
• Bragard, C., Caciagli, P., Lemaire, O., Lopez-Moya, J. J., MacFarlane, S., Peters, D., ... & Torrance, L. (2013). Status and prospects of plant virus control through interference with vector transmission. Annual review of phytopathology, 51, 177-201.
• Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., ... & Gal‐On, A. (2016). Development of broad virus resistance in non‐transgenic cucumber using CRISPR/Cas9 technology. Molecular plant pathology, 17(7), 1140-1153.
• Christopoulou, M., Wo, S. R. C., Kozik, A., McHale, L. K., Truco, M. J., Wroblewski, T., & Michelmore, R. W. (2015). Genome-wide architecture of disease resistance genes in lettuce. G3: Genes, Genomes, Genetics, 5(12), 2655-2669.
• Consonni, C., Humphry, M. E., Hartmann, H. A., Livaja, M., Durner, J., Westphal, L., ... & Somerville, S. C. (2006). Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nature genetics, 38(6), 716-720.
• Dai, W. J., Zhu, L. Y., Yan, Z. Y., Xu, Y., Wang, Q. L., & Lu, X. J. (2016). CRISPR-Cas9 for in vivo gene therapy: Promise and hurdles. Molecular Therapy-Nucleic Acids, 5, e349.
• De Toledo Thomazella, D. P., Brail, Q., Dahlbeck, D., & Staskawicz, B. (2016). CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. BioRxiv, 064824.
• Ding, S. W., & Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell, 130(3), 413-426.
• Doehlemann, G., Ökmen, B., Zhu, W., Sharon, A. (2017). Plant Pathogenic Fungi. The Fungal Kingdom: 703-726, Washington-American.
• Dunn, D. A., & Pinkert, C. A. (2014). Gene editing. In Transgenic Animal Technology (pp. 229-248). Elsevier.
• FAO, (2017). The Future of Food and Agriculture – Trends and Challenges. Rome, Italy.
• Fonseca, S., Chico, J. M., & Solano, R. (2009). The jasmonate pathway: the ligand, the receptor and the core signalling module. Current opinion in plant biology, 12(5), 539-547.
• Gao, J., Wang, G., Ma, S., Xie, X., Wu, X., Zhang, X., ... & Xia, Q. (2015). CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant molecular biology, 87(1-2), 99-110.
• Gibbs, A., & Ohshima, K. (2010). Potyviruses and the digital revolution. Annual review of phytopathology, 48, 205-223.
• Gómez, P., Rodríguez-Hernández, A. M., Moury, B., & Aranda, M. A. (2009). Genetic resistance for the sustainable control of plant virus diseases: breeding, mechanisms and durability. European journal of plant pathology, 125(1), 1-22.
• Gomez, M. A., Lin, Z. D., Moll, T., Chauhan, R. D., Hayden, L., Renninger, K., ... & Bart, R. S. (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 biotechnology journal, 17(2), 421-434.
• Griggs, D., Smith, M. S., Rockström, J., Öhman, M. C., Gaffney, O., Glaser, G., ... & Shyamsundar, P. (2014). An integrated framework for sustainable development goals. Ecology and Society, 19(4).
• Hanley-Bowdoin, L., Bejarano, E. R., Robertson, D., & Mansoor, S. (2013). Geminiviruses: masters at redirecting and reprogramming plant processes. Nature Reviews Microbiology, 11(11), 777-788.
• Herrera-Estrella, L., Depicker, A., Van Montagu, M., & Schell, J. (1983). Expression of chimaeric genes transferred into plant cells using a Ti-plasmid-derived vector. Nature, 303(5914), 209-213.
• Horvath, P., & Barrangou, R. (2010). CRISPR/Cas, the immune system of bacteria and archaea. Science, 327(5962), 167-170.
• Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., & Nakata, A. (1987). Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. Journal of bacteriology, 169(12), 5429-5433.
• Jansen, R., Embden, J. D. V., Gaastra, W., & Schouls, L. M. (2002). Identification of genes that are associated with DNA repeats in prokaryotes. Molecular microbiology, 43(6), 1565-1575.
• Javed, M. R., Sadaf, M., Ahmed, T., Jamil, A., Nawaz, M., Abbas, H., & Ijaz, A. (2018). CRISPR-Cas system: history and prospects as a genome editing tool in microorganisms. Current microbiology, 75(12), 1675-1683.
• Ji, X., Zhang, H., Zhang, Y., Wang, Y., & Gao, C. (2015). Establishing a CRISPR–Cas-like immune system conferring DNA virus resistance in plants. Nature Plants, 1(10), 1-4.
• Jia, H., Orbovic, V., Jones, J. B., & Wang, N. (2016). Modification of the PthA4 effector binding elements in Type I Cs LOB 1 promoter using Cas9/sg RNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4: dCs LOB 1.3 infection. Plant biotechnology journal, 14(5), 1291-1301.
• Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B., & Weeks, D. P. (2013). Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic acids research, 41(20), e188-e188.
• Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012). A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. science, 337(6096), 816-821.
• Jones, J. D., & Dangl, J. L. (2006). The plant immune system. nature, 444(7117), 323-329.
• Karimi, Z., Ahmadi, A., Najafi, A., & Ranjbar, R. (2018). Bacterial CRISPR regions: general features and their potential for epidemiological molecular typing studies. The open microbiology journal, 12, 59.
• Kang, B. C., Yeam, I., & Jahn, M. M. (2005a). Genetics of plant virus resistance. Annu. Rev. Phytopathol., 43, 581-621.
• Kang, B. C., Yeam, I., Frantz, J. D., Murphy, J. F., & Jahn, M. M. (2005b). The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. The Plant Journal, 42(3), 392-405.
• Kim, H., & Kim, J. S. (2014). A guide to genome engineering with programmable nucleases. Nature Reviews Genetics, 15(5), 321-334.
• Kis, A., Hamar, É., Tholt, G., Bán, R., & Havelda, Z. (2019). Creating highly efficient resistance against wheat dwarf virus in barley by employing CRISPR/Cas9 system. Plant biotechnology journal, 17(6), 1004.
• Klein, T. M., Fromm, M., Weissinger, A., Tomes, D., Schaaf, S., Sletten, M., & Sanford, J. C. (1988). Transfer of foreign genes into intact maize cells with high-velocity microprojectiles. Proceedings of the National Academy of Sciences, 85(12), 4305-4309.
• Kloepper, J. W., Ryu, C. M., & Zhang, S. (2004). Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology, 94(11), 1259-1266.
• Lau, C. H. (2018). Applications of crispr-cas in bioengineering, biotechnology, and translational research. The CRISPR journal, 1(6), 379-404.
• Leach, J. E., Vera Cruz, C. M., Bai, J., & Leung, H. (2001). Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annual review of phytopathology, 39(1), 187-224.
• Li, T., Liu, B., Spalding, M. H., Weeks, D. P., & Yang, B. (2012). High-efficiency TALEN-based gene editing produces disease-resistant rice. Nature biotechnology, 30(5), 390.
• Liu, L., Li, X., Ma, J., Li, Z., You, L., Wang, J., ... & Wang, Y. (2017). The molecular architecture for RNA-guided RNA cleavage by Cas13a. Cell, 170(4), 714-726.
• Lyngkjær, M., Newton, A., Atzema, J., & Baker, S. (2000). The barley mlo-gene: an important powdery mildew resistance source.
• Macovei, A., Sevilla, N. R., Cantos, C., Jonson, G. B., Slamet‐Loedin, I., Čermák, T., ... & Chadha‐Mohanty, P. (2018). Novel alleles of rice eIF4G generated by CRISPR/Cas9‐targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant biotechnology journal, 16(11), 1918-1927.
• Mahas, A., & Mahfouz, M. (2018). Engineering virus resistance via CRISPR–Cas systems. Current opinion in virology, 32, 1-8.
• Mahy, B. W. J., van Regenmortel, M. H. V. (2009). Desk Encyclopedia of Plant and Fungal Virology. Cambridge, MA: Academic Press.
• Maxson-Stein, K., He, S. Y., Hammerschmidt, R., & Jones, A. L. (2002). Effect of treating apple trees with acibenzolar-S-methyl on fire blight and expression of pathogenesis-related protein genes. Plant disease, 86(7), 785-790.
• Malnoy, M., Viola, R., Jung, M. H., Koo, O. J., Kim, S., Kim, J. S., ... & Nagamangala Kanchiswamy, C. (2016). DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Frontiers in plant science, 7, 1904.
• Miklis, M., Consonni, C., Bhat, R. A., Lipka, V., Schulze-Lefert, P., & Panstruga, R. (2007). Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiology, 144(2), 1132-1143.
• Mojica, F. J., García-Martínez, J., & Soria, E. (2005). Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. Journal of molecular evolution, 60(2), 174-182.
• 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. Scientific reports, 7(1), 1-6.
• Ortigosa, A., Gimenez‐Ibanez, S., Leonhardt, N., & Solano, R. (2019). Design of a bacterial speck resistant tomato by CRISPR/Cas9‐mediated editing of Sl JAZ 2. Plant biotechnology journal, 17(3), 665-673.
• Osakabe, Y., Watanabe, T., Sugano, S. S., Ueta, R., Ishihara, R., Shinozaki, K., & Osakabe, K. (2016). Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Scientific reports, 6, 26685.
• Pacher, M., & Puchta, H. (2017). From classical mutagenesis to nuclease‐based breeding–directing natural DNA repair for a natural end‐product. The Plant Journal, 90(4), 819-833.
• Peng, A., Chen, S., Lei, T., Xu, L., He, Y., Wu, L., ... & Zou, X. (2017). Engineering canker‐resistant plants through CRISPR/Cas9‐targeted editing of the susceptibility gene Cs LOB 1 promoter in citrus. Plant biotechnology journal, 15(12), 1509-1519.
• Piffanelli, P., Ramsay, L., Waugh, R., Benabdelmouna, A., D'Hont, A., Hollricher, K., ... & Panstruga, R. (2004). A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature, 430(7002), 887-891.
• Piqué, N., Miñana-Galbis, D., Merino, S., & Tomás, J. M. (2015). Virulence factors of Erwinia amylovora: a review. International journal of molecular sciences, 16(6), 12836-12854.
• Pradhanang, P. M., Ji, P., Momol, M. T., Olson, S. M., Mayfield, J. L., & Jones, J. B. (2005). Application of acibenzolar-S-methyl enhances host resistance in tomato against Ralstonia solanacearum. Plant disease, 89(9), 989-993.
• Price, A. A., Sampson, T. R., Ratner, H. K., Grakoui, A., & Weiss, D. S. (2015). Cas9-mediated targeting of viral RNA in eukaryotic cells. Proceedings of the National Academy of Sciences, 112(19), 6164-6169.
• Price, A. A., Grakoui, A., & Weiss, D. S. (2016). Harnessing the prokaryotic adaptive immune system as a eukaryotic antiviral defense. Trends in microbiology, 24(4), 294-306.
• Puchta, H. (2005). The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. Journal of experimental botany, 56(409), 1-14.
• Puchta, H., Dujon, B., & Hohn, B. (1993). Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic acids research, 21(22), 5034-5040.
• Puchta, H., Dujon, B., & Hohn, B. (1996). Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proceedings of the National Academy of Sciences, 93(10), 5055-5060.
• Pyott, D. E., Sheehan, E., & Molnar, A. (2016). Engineering of CRISPR/Cas9‐mediated potyvirus resistance in transgene‐free Arabidopsis plants. Molecular plant pathology, 17(8), 1276-1288.
• Revers, F., & García, J. A. (2015). Molecular biology of potyviruses. In Advances in virus research (Vol. 92, pp. 101-199). Academic Press.
• Salomon, S., & Puchta, H. (1998). Capture of genomic and T‐DNA sequences during double‐strand break repair in somatic plant cells. The EMBO journal, 17(20), 6086-6095.
• Sampson, T. R., Saroj, S. D., Llewellyn, A. C., Tzeng, Y. L., & Weiss, D. S. (2013). A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature, 497(7448), 254-257.
• Sander, J. D., & Joung, J. K. (2014). CRISPR-Cas systems for editing, regulating and targeting genomes. Nature biotechnology, 32(4), 347-355.
• Sanfaçon, H. (2015). Plant translation factors and virus resistance. Viruses, 7(7), 3392-3419.
• Scheben, A., & Edwards, D. (2018). Towards a more predictable plant breeding pipeline with CRISPR/Cas-induced allelic series to optimize quantitative and qualitative traits. Current opinion in plant biology, 45, 218-225.
• Sen, Y., van der Wolf, J., Visser, R. G., & van Heusden, S. (2015). Bacterial canker of tomato: current knowledge of detection, management, resistance, and interactions. Plant Disease, 99(1), 4-13.
• Shi, J., & Lai, J. (2015). Patterns of genomic changes with crop domestication and breeding. Current opinion in plant biology, 24, 47-53.
• Singh, O. V., Ghai, S., Paul, D., & Jain, R. K. (2006). Genetically modified crops: success, safety assessment, and public concern. Applied microbiology and biotechnology, 71(5), 598-607.
• Sobiczewski, P. (2008). Bacterial diseases of plants: Epidemiology, diagnostics and control. Zemdirbyste, 95, 151-157.
• Svitashev, S., Young, J. K., Schwartz, C., Gao, H., Falco, S. C., & Cigan, A. M. (2015). Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant physiology, 169(2), 931-945.
• Tashkandi, M., Ali, Z., Aljedaani, F., Shami, A., & Mahfouz, M. M. (2018). Engineering resistance against Tomato yellow leaf curl virus via the CRISPR/Cas9 system in tomato. Plant signaling & behavior, 13(10), e1525996.
• Tilman, D., Balzer, C., Hill, J., & Befort, B. L. (2011). Global food demand and the sustainable intensification of agriculture. Proceedings of the national academy of sciences, 108(50), 20260-20264.
• Vicente Muñoz, I., Sarrocco, S., Vannacci, G. (2017). CRISPR-CAS for the Genome Editing of Two Trichoderma spp. Beneficial Isolates. Journal Plant Pathology, 99: S63.
• Vicente Muñoz, I., Sarrocco, S., Malfatti, L., Baroncelli, R., Vannacci, G. (2019). CRISPR-Cas for Fungal Genome Editing: A New Tool for the Management of Plant Diseases. Frontiers in Plant Science, 10: 135.
• Walsh, J. A., & Jenner, C. E. (2002). Turnip mosaic virus and the quest for durable resistance. Molecular plant pathology, 3(5), 289-300.
• Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., & Jaenisch, R. (2013). One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153(4), 910-918.
• Wang, X., Tu, M., Wang, D., Liu, J., Li, Y., Li, Z., ... & Wang, X. (2018a). CRISPR/Cas9‐mediated efficient targeted mutagenesis in grape in the first generation. Plant biotechnology journal, 16(4), 844-855.
• Wang, Q., Cobine, P. A., & Coleman, J. J. (2018b). Efficient genome editing in Fusarium oxysporum based on CRISPR/Cas9 ribonucleoprotein complexes. Fungal Genetics and Biology, 117, 21-29.
• Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., & Qiu, J. L. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature biotechnology, 32(9), 947-951.
• Wang, F., Wang, C., Liu, P., Lei, C., Hao, W., Gao, Y., ... & Zhao, K. (2016). Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PloS one, 11(4), e0154027.
• Watson, A., Ghosh, S., Williams, M. J., Cuddy, W. S., Simmonds, J., Rey, M. D., ... & Adamski, N. M. (2018). Speed breeding is a powerful tool to accelerate crop research and breeding. Nature plants, 4(1), 23-29.
• Yeam, I., Cavatorta, J. R., Ripoll, D. R., Kang, B. C., & Jahn, M. M. (2007). Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. The Plant Cell, 19(9), 2913-2928.
• Yin, K., & Qiu, J. L. (2019). Genome editing for plant disease resistance: applications and perspectives. Philosophical Transactions of the Royal Society B, 374(1767), 20180322.
• Zaidi, S. S. E. A., Tashkandi, M., Mansoor, S., & Mahfouz, M. M. (2016). Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Frontiers in plant science, 7, 1673.
• Zerbini, F. M., Briddon, R. W., Idris, A., Martin, D. P., Moriones, E., Navas-Castillo, J., ... & Consortium, I. R. (2017). ICTV virus taxonomy profile: Geminiviridae. The Journal of general virology, 98(2), 131.
• Zhan, X., Zhang, F., Zhong, Z., Chen, R., Wang, Y., Chang, L., ... & Zhang, J. (2019). Generation of virus‐resistant potato plants by RNA genome targeting. Plant biotechnology journal, 17(9), 1814-1822.
• Zhang, H., Zhang, J., Wei, P., Zhang, B., Gou, F., Feng, Z., ... & Zhu, J. K. (2014). The CRISPR/C as9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant biotechnology journal, 12(6), 797-807.
• Zhang, Y., Bai, Y., Wu, G., Zou, S., Chen, Y., Gao, C., & Tang, D. (2017). Simultaneous modification of three homoeologs of Ta EDR 1 by genome editing enhances powdery mildew resistance in wheat. The Plant Journal, 91(4), 714-724.
• Zhang, T., Zheng, Q., Yi, X., An, H., Zhao, Y., Ma, S., & Zhou, G. (2018). Establishing RNA virus resistance in plants by harnessing CRISPR immune system. Plant biotechnology journal, 16(8), 1415-1423.
• Zheng, X. Y., Spivey, N. W., Zeng, W., Liu, P. P., Fu, Z. Q., Klessig, D. F., ... & Dong, X. (2012). Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell host & microbe, 11(6), 587-596.
• Zheng, Z., Appiano, M., Pavan, S., Bracuto, V., Ricciardi, L., Visser, R.G.F., Wolters, A.M.A., 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. Frontiers in Plant Science, 7: 380.
• Zhou, J., Peng, Z., Long, J., Sosso, D., Liu, B., Eom, J. S., ... & White, F. F. (2015). Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. The Plant Journal, 82(4), 632-643.
• Ziebell, H. (2016). Plant defence and viral interference. In Plant-Virus Interactions (pp. 123-159). Springer, Cham.