The Emerging Role of 2OGDs as Candidate Targets for Engineering Crops with Broad-Spectrum Disease Resistance
Abstract
:1. Introduction
2. The Discoveries of 2OGD-Mediated Broad-Spectrum Disease Resistance
3. The Roles of Phytohormones in Broad-Spectrum Disease Resistance
4. Regulating Plant BSR with 2OGDs via Altering the Levels of Phytohormones
5. Conclusions and Perspectives
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Savary, S.; Willocquet, L.; Pethybridge, S.J.; Esker, P.; McRoberts, N.; Nelson, A. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019, 3, 430–439. [Google Scholar] [CrossRef] [PubMed]
- Jones, J.D.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [PubMed]
- Tsuda, K.; Katagiri, F. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 2010, 13, 459–465. [Google Scholar] [CrossRef] [PubMed]
- Cui, H.T.; Tsuda, K.; Parker, J.E. Effector-triggered immunity: From pathogen perception to robust defense. Annu. Rev. Plant Biol. 2015, 66, 487–511. [Google Scholar] [CrossRef] [PubMed]
- Couto, D.; Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 2016, 16, 537–552. [Google Scholar] [CrossRef]
- Yu, X.; Feng, B.M.; He, P.; Shan, L.B. From chaos to harmony: Responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 2017, 55, 109–137. [Google Scholar] [CrossRef]
- Peng, Y.J.; van Wersch, R.; Zhang, Y.L. Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity. Mol. Plant Microbe Interact. 2018, 31, 403–409. [Google Scholar] [CrossRef]
- Kou, Y.J.; Wang, S.P. Broad-spectrum and durability: Understanding of quantitative disease resistance. Curr. Opin. Plant Biol. 2010, 13, 181–185. [Google Scholar] [CrossRef]
- Li, W.; Deng, Y.W.; Ning, Y.S.; He, Z.H.; Wang, G.L. Exploiting broad-spectrum disease resistance in crops: From molecular dissection to breeding. Annu. Rev. Plant Biol. 2020, 71, 575–603. [Google Scholar] [CrossRef] [PubMed]
- Forsyth, A.; Mansfield, J.W.; Grabov, N.; de Torres, M.; Sinapidou, E.; Grant, M.R. Genetic dissection of basal resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol. Plant Microbe Interact. 2010, 23, 1545–1552. [Google Scholar]
- Robatzek, S.; Chinchilla, D.; Boller, T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 2006, 20, 537–542. [Google Scholar] [CrossRef]
- Robatzek, S.; Bittel, P.; Chinchilla, D.; Köchner, P.; Felix, G.; Shiu, S.H.; Boller, T. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 2007, 64, 539–547. [Google Scholar] [CrossRef]
- Kunze, G.; Zipfel, C.; Robatzek, S.; Niehaus, K.; Boller, T.; Felix, G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 2004, 16, 3496–3507. [Google Scholar] [CrossRef]
- Lacombe, S.; Rougon-Cardoso, A.; Sherwood, E.; Peeters, N.; Dahlbeck, D.; van Esse, H.P.; Smoker, M.; Rallapalli, G.; Thomma, B.P.; Staskawicz, B.; et al. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 2010, 28, 365–369. [Google Scholar] [CrossRef]
- Boschi, F.; Schvartzman, C.; Murchio, S.; Ferreira, V.; Siri, M.I.; Galván, G.A.; Smoker, M.; Stransfeld, L.; Zipfel, C.; Vilaró, F.L.; et al. Enhanced bacterial wilt resistance in potato through expression of Arabidopsis EFR and introgression of quantitative resistance from Solanum commersonii. Front. Plant Sci. 2017, 8, 1642. [Google Scholar] [CrossRef]
- Pfeilmeier, S.; George, J.; Morel, A.; Roy, S.; Smoker, M.; Stransfeld, L.; Downie, J.A.; Peeters, N.; Malone, J.G.; Zipfel, C. 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. 2019, 17, 569–579. [Google Scholar] [CrossRef]
- Schwessinger, B.; Bahar, O.; Thomas, N.; Holton, N.; Nekrasov, V.; Ruan, D.L.; Canlas, P.E.; Daudi, A.; Petzold, C.J.; Singan, V.R.; et al. Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLoS Pathog. 2015, 11, e1004809. [Google Scholar] [CrossRef]
- Song, W.Y.; Wang, G.L.; Chen, L.L.; Kim, H.S.; Pi, L.Y.; Holsten, T.; Gardner, J.; Wang, B.; Zhai, W.X.; Zhu, L.H.; et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 1995, 270, 1804–1806. [Google Scholar] [CrossRef]
- Wang, G.L.; Song, W.Y.; Ruan, D.L.; Sideris, S.; Ronald, P.C. The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. Mol. Plant Microbe Interact. 1996, 9, 850–855. [Google Scholar] [CrossRef]
- Holton, N.; Nekrasov, V.; Ronald, P.C.; Zipfel, C. The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLoS Pathog. 2015, 11, e1004602. [Google Scholar] [CrossRef]
- Omar, A.A.; Murata, M.M.; El-Shamy, H.A.; Graham, J.H.; Grosser, J.W. Enhanced resistance to citrus canker in transgenic mandarin expressing Xa21 from rice. Transgenic Res. 2018, 27, 179–191. [Google Scholar] [CrossRef]
- Tripathi, J.N.; Lorenzen, J.; Bahar, O.; Ronald, P.; Tripathi, L. Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnol. J. 2014, 12, 663–673. [Google Scholar] [CrossRef]
- Liu, B.; Li, J.F.; Ao, Y.; Qu, J.W.; Li, Z.Q.; Su, J.B.; Zhang, Y.; Liu, J.; Feng, D.R.; Qi, K.B.; et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 2012, 24, 3406–3419. [Google Scholar] [CrossRef]
- Du, J.; Verzaux, E.; Chaparro-Garcia, A.; Bijsterbosch, G.; Keizer, L.C.; Zhou, J.; Liebrand, T.W.; Xie, C.; Govers, F.; Robatzek, S. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat. Plants 2015, 1, 15034. [Google Scholar] [CrossRef]
- Lee, S.C.; Hwang, I.S.; Choi, H.W.; Hwang, B.K. Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol. 2008, 148, 1004–1020. [Google Scholar] [CrossRef]
- Jia, Z.C.; Gou, J.Q.; Sun, Y.M.; Yuan, L.; Tang, Q.; Yang, X.Y.; Pei, Y.; Luo, K.M. Enhanced resistance to fungal pathogens in transgenic Populus tomentosa Carr. by overexpression of an nsLTP-like antimicrobial protein gene from motherwort (Leonurus japonicus). Tree Physiol. 2010, 30, 1599–1605. [Google Scholar] [CrossRef]
- Yang, X.Y.; Li, J.; Li, X.B.; She, R.; Pei, Y. Isolation and characterization of a novel thermostable non-specific lipid transfer protein-like antimicrobial protein from motherwort (Leonurus japonicus Houtt) seeds. Peptides 2006, 27, 3122–3128. [Google Scholar] [CrossRef]
- Wang, N.; Tang, C.L.; Fan, X.; He, M.Y.; Gan, P.F.; Zhang, S.; Hu, Z.Y.; Wang, X.D.; Yan, T.; Shu, W.X.; et al. Inactivation of a wheat protein kinase gene confers broad-spectrum resistance to rust fungi. Cell 2022, 185, 2961–2974. [Google Scholar] [CrossRef]
- Kang, L.; Li, J.X.; Zhao, T.H.; Xiao, F.M.; Tang, X.Y.; Thilmony, R.; He, S.Y.; Zhou, J.M. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc. Natl. Acad. Sci. USA 2003, 100, 3519–3524. [Google Scholar] [CrossRef]
- Lu, M.; Tang, X.Y.; Zhou, J.M. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 2001, 13, 437–447. [Google Scholar] [CrossRef]
- Assaad, F.F.; Qiu, J.L.; Youngs, H.; Ehrhardt, D.; Zimmerli, L.; Kalde, M.; Wanner, G.; Peck, S.C.; Edwards, H.; Ramonell, K.; et al. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 2004, 15, 5118–5129. [Google Scholar] [CrossRef] [PubMed]
- Collins, N.C.; Thordal-Christensen, H.; Lipka, V.; Bau, S.; Kombrink, E.; Qiu, J.L.; Hückelhoven, R.; Stein, M.; Freialdenhoven, A.; Somerville, S.C.; et al. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 2003, 425, 973–977. [Google Scholar] [CrossRef] [PubMed]
- Lipka, V.; Dittgen, J.; Bednarek, P.; Bhat, R.; Wiermer, M.; Stein, M.; Landtag, J.; Brandt, W.; Rosahl, S.; Scheel, D.; et al. Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005, 310, 1180–1183. [Google Scholar] [PubMed]
- Stein, M.; Dittgen, J.; Sánchez-Rodríguez, C.; Hou, B.H.; Molina, A.; Schulze-Lefert, P.; Lipka, V.; Somerville, S. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 2006, 18, 731–746. [Google Scholar] [CrossRef] [PubMed]
- Loehrer, M.; Langenbach, C.; Goellner, K.; Conrath, U.; Schaffrath, U. Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol. Plant Microbe Interact. 2008, 21, 1421–1430. [Google Scholar] [CrossRef] [PubMed]
- Krattinger, S.G.; Lagudah, E.S.; Spielmeyer, W.; Singh, R.P.; Huerta-Espino, J.; McFadden, H.; Bossolini, E.; Selter, L.L.; Keller, B. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 2009, 323, 1360–1363. [Google Scholar] [PubMed]
- Lagudah, E.S.; Krattinger, S.G.; Herrera-Foessel, S.A.; Singh, R.P.; Huerta-Espino, J.; Spielmeyer, W.; Brown-Guedira, G.; Selter, L.L.; Keller, B. Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor. Appl. Genet. 2009, 119, 889–898. [Google Scholar] [CrossRef] [PubMed]
- Spielmeyer, W.; Mago, R.; Wellings, C.; Ayliffe, M. Lr67 and Lr34 rust resistance genes have much in common-they confer broad spectrum resistance to multiple pathogens in wheat. BMC Plant Biol. 2013, 13, 96. [Google Scholar] [PubMed]
- Herrera-Foessel, S.A.; Singh, R.P.; Lillemo, M.; Huerta-Espino, J.; Bhavani, S.; Singh, S.; Lan, C.X.; Calvo-Salazar, V.; Lagudah, E.S. Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor. Appl. Genet. 2014, 127, 781–789. [Google Scholar] [CrossRef] [PubMed]
- Moore, J.W.; Herrera-Foessel, S.; Lan, C.X.; Schnippenkoetter, W.; Ayliffe, M.; Huerta-Espino, J.; Lillemo, M.; Viccars, L.; Milne, R.; Periyannan, S.; et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 2015, 47, 1494–1498. [Google Scholar] [CrossRef]
- Wang, Y.H.; Tan, J.Y.; Wu, Z.M.; VandenLangenberg, K.; Wehner, T.C.; Wen, C.L.; Zheng, X.Y.; Owens, K.; Thornton, A.; Bang, H.H.; et al. STAYGREEN, STAY HEALTHY: A loss-of-susceptibility mutation in the STAYGREEN gene provides durable, broadspectrum disease resistances for over 50 years of US cucumber production. New Phytol. 2019, 221, 415–430. [Google Scholar] [CrossRef] [PubMed]
- Farrow, S.C.; Facchini, P.J. Functional diversity of 2-oxoglutarate/Fe(II)-dependent dioxygenases in plant metabolism. Front. Plant Sci. 2014, 5, 524. [Google Scholar] [CrossRef] [PubMed]
- Kawai, Y.; Ono, E.; Mizutani, M. Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. Plant J. 2014, 78, 328–343. [Google Scholar] [CrossRef]
- Martinez, S.; Hausinger, R.P. Catalytic mechanisms of Fe(II)- and 2-oxoglutarate-dependent oxygenases. J. Biol. Chem. 2015, 290, 20702–20711. [Google Scholar] [CrossRef] [PubMed]
- Markolovic, S.; Wilkins, S.E.; Schofield, C.J. Protein hydroxylation catalyzed by 2-oxoglutarate-dependent oxygenases. J. Biol. Chem. 2015, 290, 20712–20722. [Google Scholar] [CrossRef] [PubMed]
- Islam, M.S.; Leissing, T.M.; Chowdhury, R.; Hopkinson, R.J.; Schofield, C.J. 2-oxoglutarate-dependent oxygenases. Annu. Rev. Biochem. 2018, 87, 585–620. [Google Scholar] [CrossRef] [PubMed]
- Nadi, R.; Mateo-Bonmati, E.; Juan-Vicente, L.; Micol, J.L. The 2OGD superfamily: Emerging functions in plant epigenetics and hormone metabolism. Mol. Plant 2018, 11, 1222–1224. [Google Scholar] [CrossRef]
- Falnes, P.Ø.; Johansen, R.F.; Seeberg, E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 2002, 419, 178–182. [Google Scholar] [CrossRef] [PubMed]
- Trewick, S.C.; Henshaw, T.F.; Hausinger, R.P.; Lindahl, T.; Sedgwick, B. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 2002, 419, 174–178. [Google Scholar] [CrossRef]
- Martínez-Pérez, M.; Aparicio, F.; López-Gresa, M.P.; Bellés, J.M.; Sánchez-Navarro, J.A.; Pallás, V. Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc. Natl. Acad. Sci. USA 2017, 114, 10755–10760. [Google Scholar] [CrossRef]
- Duan, H.C.; Wei, L.H.; Zhang, C.; Wang, Y.; Chen, L.; Lu, Z.; Chen, P.R.; He, C.; Jia, G. ALKBH10B is an RNA N6-methyladenosine demethylase affecting Arabidopsis floral transition. Plant Cell 2017, 29, 2995–3011. [Google Scholar] [CrossRef]
- Ozer, A.; Bruick, R.K. Non-heme dioxygenases: Cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol. 2007, 3, 144–153. [Google Scholar] [CrossRef]
- Keskiaho, K.; Hieta, R.; Sormunen, R.; Myllyharju, J. Chlamydomonas reinhardtii has multiple prolyl 4-hydroxylases, one of which is essential for proper cell wall assembly. Plant Cell 2007, 19, 256–269. [Google Scholar] [CrossRef] [PubMed]
- Van Damme, M.; Andel, A.; Huibers, R.P.; Panstruga, R.; Weisbeek, P.J.; Van den Ackerveken, G. Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica. Mol. Plant Microbe Interact. 2005, 6, 583–592. [Google Scholar] [CrossRef]
- Van Damme, M.; Huibers, R.P.; Elberse, J.; Van den Ackerveken, G. Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew. Plant J. 2008, 54, 785–793. [Google Scholar] [CrossRef]
- Zeilmaker, T.; Ludwig, N.R.; Elberse, J.; Seidl, M.F.; Berke, L.; Van Doorn, A.; Schuurink, R.C.; Snel, B.; Van den Ackerveken, G. DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J. 2015, 81, 210–222. [Google Scholar] [CrossRef]
- Sun, K.L.; van Tuinen, A.; van Kan, J.A.L.; Wolters, A.A.; Jacobsen, E.; Visser, R.G.F.; Bai, Y.L. Silencing of DND1 in potato and tomato impedes conidial germination, attachment and hyphal growth of Botrytis cinerea. BMC Plant Biol. 2017, 17, 235. [Google Scholar] [CrossRef]
- Kieu, N.P.; Lenman, M.; Wang, E.S.; Petersen, B.L.; Andreasson, E. Mutations introduced in susceptibility genes through CRISPR/Cas9 genome editing confer increased late blight resistance in potatoes. Sci. Rep. 2021, 11, 4487. [Google Scholar] [CrossRef]
- Thomazella, D.P.T.; Seong, K.; Mackelprang, R.; Dahlbeck, D.; Geng, Y.; Gill, U.S.; Qi, T.C.; Pham, J.; Giuseppe, P.; Lee, C.Y.; et al. Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. USA 2021, 118, e2026152118. [Google Scholar] [CrossRef] [PubMed]
- Hasley, J.A.R.; Navet, N.; Tian, M.Y. CRISPR/Cas9-mediated mutagenesis of sweet basil candidate susceptibility gene ObDMR6 enhances downy mildew resistance. PLoS ONE 2021, 16, e0253245. [Google Scholar] [CrossRef]
- Liang, B.B.; Bai, Y.J.; Zang, C.Q.; Pei, X.; Xie, J.H.; Lin, Y.; Liu, X.Z.; Ahsan, T.; Liang, C.H. Overexpression of the first peanut-susceptible gene, AhS5H1 or AhS5H2, enhanced susceptibility to Pst DC3000 in Arabidopsis. Int. J. Mol. Sci. 2023, 24, 14210. [Google Scholar] [CrossRef]
- Low, Y.C.; Lawton, M.A.; Di, R. Validation of barley 2OGO gene as a functional orthologue of Arabidopsis DMR6 gene in Fusarium head blight susceptibility. Sci. Rep. 2020, 10, 9935. [Google Scholar] [CrossRef]
- Tripathi, J.N.; Ntui, V.O.; Shah, T.; Tripathi, L. CRISPR/Cas9-mediated editing of DMR6 orthologue in banana (Musa spp.) confers enhanced resistance to bacterial disease. Plant Biotechnol. J. 2021, 19, 1291–1293. [Google Scholar] [CrossRef] [PubMed]
- Liang, B.B.; Wang, H.; Yang, C.; Wang, L.Y.; Qi, L.L.; Guo, Z.J.; Chen, X.J. Salicylic acid is required for broad-spectrum disease resistance in rice. Int. J. Mol. Sci. 2022, 23, 1354. [Google Scholar] [CrossRef]
- Zhang, Y.J.; Yu, Q.L.; Gao, S.L.; Yu, N.N.; Zhao, L.; Wang, J.B.; Zhao, J.Z.; Huang, P.; Yao, L.B.; Wang, M.; et al. Disruption of the primary salicylic acid hydroxylases in rice enhances broad-spectrum resistance against pathogens. Plant Cell Environ. 2022, 45, 2211–2225. [Google Scholar] [CrossRef]
- Liu, X.; Yu, Y.; Yao, W.; Yin, Z.L.; Wang, Y.B.; Huang, Z.J.; Zhou, J.Q.; Liu, J.L.; Lu, X.D.; Wang, F.; et al. CRISPR/Cas9-mediated simultaneous mutation of three salicylic acid 5-hydroxylase (OsS5H) genes confers broad-spectrum disease resistance in rice. Plant Biotechnol. J. 2023, 21, 1873–1886. [Google Scholar] [CrossRef]
- Shan, X.C.; Goodwin, P.H. Silencing an ACC oxidase gene affects the susceptible host response of Nicotiana benthamiana to infection by Colletotrichum orbiculare. Plant Cell Rep. 2006, 25, 241–247. [Google Scholar] [CrossRef]
- Iwai, T.; Miyasaka, A.; Seo, S.; Ohashi, Y. Contribution of ethylene biosynthesis for resistance to blast fungus infection in young rice plants. Plant Physiol. 2006, 142, 1202–1215. [Google Scholar] [CrossRef]
- Dziurka, M.; Janeczko, A.; Juhász, C.; Gullner, G.; Oklestková, J.; Novák, O.; Saja, D.; Skoczowski, A.; Tóbiás, I.; Barna, B. Local and systemic hormonal responses in pepper leaves during compatible and incompatible pepper-tobamovirus interactions. Plant Physiol. Biochem. 2016, 109, 355–364. [Google Scholar] [CrossRef]
- Zheng, H.Y.; Dong, L.L.; Han, X.Y.; Jin, H.B.; Yin, C.C.; Han, Y.L.; Li, B.; Qin, H.J.; Zhang, J.S.; Shen, Q.H.; et al. The TuMYB46L-TuACO3 module regulates ethylene biosynthesis in einkorn wheat defense to powdery mildew. New Phytol. 2020, 225, 2526–2541. [Google Scholar] [CrossRef]
- Caarls, L.; Elberse, J.; Awwanah, M.; Ludwig, N.R.; De Vries, M.; Zeilmaker, T.; Van Wees, S.C.; Schuurink, R.C.; Ackerveken, G.V.D. Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc. Natl. Acad. Sci. USA 2017, 114, 6388–6393. [Google Scholar] [CrossRef]
- Smirnova, E.; Marquis, V.; Poirier, L.; Aubert, Y.; Zumsteg, J.; Ménard, R.; Miesch, L.; Heitz, T. Jasmonic Acid Oxidase 2 hydroxylates jasmonic acid and represses basal defense and resistance responses against Botrytis cinerea infection. Mol. Plant 2017, 10, 1159–1173. [Google Scholar] [CrossRef]
- Marquis, V.; Smirnova, E.; Graindorge, S.; Delcros, P.; Villette, C.; Zumsteg, J.; Heintz, D.; Heitz, T. Broad-spectrum stress tolerance conferred by suppressing jasmonate signaling attenuation in Arabidopsis JASMONIC ACID OXIDASE mutants. Plant J. 2022, 109, 856–872. [Google Scholar] [CrossRef]
- Zhang, Y.L.; Li, X. Salicylic acid: Biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 2019, 50, 29–36. [Google Scholar] [CrossRef]
- Ding, P.T.; Ding, Y.L. Stories of salicylic acid: A plant defense hormone. Trends Plant Sci. 2020, 25, 549–565. [Google Scholar] [CrossRef]
- Malamy, J.; Carr, J.P.; Klessig, D.F.; Raskin, I. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 1990, 250, 1002–1004. [Google Scholar] [CrossRef]
- Métraux, J.P.; Signer, H.; Ryals, J.; Ward, E.; Wyss-Benz, M.; Gaudin, J.; Raschdorf, K.; Schmid, E.; Blum, W.; Inverardi, B. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 1990, 250, 1004–1006. [Google Scholar] [CrossRef]
- Kim, D.S.; Hwang, B.K. An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J. Exp. Bot. 2014, 65, 2295–2306. [Google Scholar] [CrossRef]
- Hao, Q.Q.; Wang, W.Q.; Han, X.L.; Wu, J.Z.; Lyu, B.; Chen, F.J.; Caplan, A.; Li, C.X.; Wu, J.J.; Wang, W.; et al. Isochorismate-based salicylic acid biosynthesis confers basal resistance to Fusarium graminearum in barley. Mol. Plant Pathol. 2018, 19, 1995–2010. [Google Scholar] [CrossRef]
- Li, Y.X.; Zhang, W.; Dong, H.X.; Liu, Z.Y.; Ma, J.; Zhang, X.Y. Salicylic acid in Populus tomentosa is a remote signalling molecule induced by Botryosphaeria dothidea infection. Sci. Rep. 2018, 8, 14059. [Google Scholar] [CrossRef]
- Ullah, C.; Tsai, C.J.; Unsicker, S.B.; Xue, L.; Reichelt, M.; Gershenzon, J.; Hammerbacher, A. Salicylic acid activates poplar defense against the biotrophic rust fungus Melampsora larici-populina via increased biosynthesis of catechin and proanthocyanidins. New Phytol. 2019, 221, 960–975. [Google Scholar] [CrossRef]
- Ullah, C.; Unsicker, S.B.; Reichelt, M.; Gershenzon, J.; Hammerbacher, A. Accumulation of catechin and proanthocyanidins in black poplar stems after infection by plectosphaerella populi: Hormonal regulation, biosynthesis and antifungal activity. Front. Plant Sci. 2019, 10, 1441. [Google Scholar] [CrossRef]
- Wang, H.; Gong, W.F.; Wang, Y.; Ma, Q. Contribution of a WRKY transcription factor, ShWRKY81, to powdery mildew resistance in wild tomato. Int. J. Mol. Sci. 2023, 24, 2583. [Google Scholar] [CrossRef]
- Nawrath, C.; Métraux, J.P. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 1999, 11, 1393–1404. [Google Scholar]
- Wildermuth, M.C.; Dewdney, J.; Wu, G.; Ausubel, F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 2001, 414, 562–565. [Google Scholar] [CrossRef]
- Gaffney, T.; Friedrich, L.; Vernooij, B.; Negrotto, D.; Nye, G.; Uknes, S.; Ward, E.; Kessmann, H.; Ryals, J. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 1993, 261, 754–756. [Google Scholar] [CrossRef]
- Delaney, T.P.; Uknes, S.; Vernooij, B.; Friedrich, L.; Weymann, K.; Negrotto, D.; Gaffney, T.; Gut-Rella, M.; Kessmann, H.; Ward, E.; et al. A central role of salicylic acid in plant disease resistance. Science 1994, 266, 1247–1250. [Google Scholar] [CrossRef]
- Conrath, U.; Chen, Z.; Ricigliano, J.R.; Klessig, D.F. Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. Proc. Natl. Acad. Sci. USA 1995, 92, 7143–7147. [Google Scholar] [CrossRef]
- Knoth, C.; Salus, M.S.; Girke, T.; Eulgem, T. The synthetic elicitor 3,5-dichloroanthranilic acid induces NPR1-dependent and NPR1-independent mechanisms of disease resistance in Arabidopsis. Plant Physiol. 2009, 150, 333–347. [Google Scholar] [CrossRef]
- Cui, Z.N.; Ito, J.; Dohi, H.; Amemiya, Y.; Nishida, Y. Molecular design and synthesis of novel salicyl glycoconjugates as elicitors against plant diseases. PLoS ONE 2014, 9, e108338. [Google Scholar] [CrossRef]
- Wang, Y.; Liu, J.H. Exogenous treatment with salicylic acid attenuates occurrence of citrus canker in susceptible navel orange (Citrus sinensis Osbeck). J. Plant Physiol. 2012, 169, 1143–1149. [Google Scholar] [CrossRef]
- Lefevere, H.; Bauters, L.; Gheysen, G. Salicylic acid biosynthesis in plants. Front. Plant Sci. 2020, 11, 338. [Google Scholar] [CrossRef]
- Cao, H.; Bowling, S.A.; Gordon, A.S.; Dong, X.N. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 1994, 6, 1583–1592. [Google Scholar] [CrossRef]
- Castelló, M.J.; Medina-Puche, L.; Lamilla, J.; Tornero, P. NPR1 paralogs of Arabidopsis and their role in salicylic acid perception. PLoS ONE 2018, 13, e0209835. [Google Scholar] [CrossRef]
- Ding, Y.L.; Sun, T.J.; Ao, K.; Peng, Y.J.; Zhang, Y.X.; Li, X.; Zhang, Y.L. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 2018, 173, 1454–1467. [Google Scholar] [CrossRef]
- van Loon, L.C.; Rep, M.; Pieterse, C.M. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 2006, 44, 135–162. [Google Scholar] [CrossRef]
- De Geyter, N.; Gholami, A.; Goormachtig, S.; Goossens, A. Transcriptional machineries in jasmonate elicited plant secondary metabolism. Trends Plant Sci. 2012, 17, 349–359. [Google Scholar] [CrossRef]
- Wasternack, C.; Hause, B. Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 2013, 111, 1021–1058. [Google Scholar] [CrossRef]
- Li, M.Y.; Yu, G.H.; Cao, C.L.; Liu, P. Metabolism, signaling, and transport of jasmonates. Plant Commun. 2021, 2, 100231. [Google Scholar] [CrossRef]
- Howe, G.A.; Major, I.T.; Koo, A.J. Modularity in jasmonate signaling for multistress resilience. Annu. Rev. Plant Biol. 2018, 69, 387–415. [Google Scholar] [CrossRef]
- Vijayan, P.; Shockey, J.; Lévesque, C.A.; Cook, R.J.; Browse, J. A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. USA 1998, 95, 7209–7214. [Google Scholar] [CrossRef]
- Thaler, J.S.; Owen, B.; Higgins, V.J. The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol. 2004, 135, 530–538. [Google Scholar] [CrossRef]
- Yan, Y.X.; Christensen, S.; Isakeit, T.; Engelberth, J.; Meeley, R.; Hayward, A.; Emery, R.J.; Kolomiets, M.V. Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. Plant Cell 2012, 24, 1420–1436. [Google Scholar] [CrossRef] [PubMed]
- Thomma, B.P.; Eggermont, K.; Penninckx, I.A.; Mauch-Mani, B.; Vogelsang, R.; Cammue, B.P.; Broekaert, W.F. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 1998, 95, 15107–15111. [Google Scholar] [CrossRef] [PubMed]
- Kloek, A.P.; Verbsky, M.L.; Sharma, S.B.; Schoelz, J.E.; Vogel, J.; Klessig, D.F.; Kunkel, B.N. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J. 2001, 26, 509–522. [Google Scholar] [CrossRef]
- Major, I.T.; Yoshida, Y.; Campos, M.L.; Kapali, G.; Xin, X.F.; Sugimoto, K.; Ferreira, D.d.O.; He, S.Y.; Howe, G.A. Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module. New Phytol. 2017, 215, 1533–1547. [Google Scholar] [CrossRef]
- Qiu, J.H.; Xie, J.H.; Chen, Y.; Shen, Z.N.; Shi, H.B.; Naqvi, N.I.; Qian, Q.; Liang, Y.; Kou, Y.J. Warm temperature compromises JA-regulated basal resistance to enhance Magnaporthe oryzae infection in rice. Mol. Plant 2022, 15, 723–739. [Google Scholar] [CrossRef]
- Yang, J.Y.; Iwasaki, M.; Machida, C.; Machida, Y.; Zhou, X.P.; Chua, N.H. βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev. 2008, 22, 2564–2577. [Google Scholar] [CrossRef]
- Lozano-Durán, R.; Rosas-Díaz, T.; Gusmaroli, G.; Luna, A.P.; Taconnat, L.; Deng, X.W.; Bejarano, E.R. Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 2011, 23, 1014–1032. [Google Scholar] [CrossRef]
- Wu, D.W.; Qi, T.C.; Li, W.X.; Tian, H.X.; Gao, H.; Wang, J.J.; Ge, J.; Yao, R.F.; Ren, C.M.; Wang, X.B.; et al. Viral effector protein manipulates host hormone signaling to attract insect vectors. Cell Res. 2017, 27, 402–415. [Google Scholar] [CrossRef]
- Zhang, C.; Ding, Z.M.; Wu, K.C.; Yang, L.; Li, Y.; Yang, Z.; Shi, S.; Liu, X.J.; Zhao, S.S.; Yang, Z.R.; et al. Suppression of jasmonic acid-mediated defense by viral-inducible microRNA319 facilitates virus infection in rice. Mol. Plant 2016, 9, 1302–1314. [Google Scholar] [CrossRef] [PubMed]
- He, Y.Q.; Zhang, H.H.; Sun, Z.T.; Li, J.M.; Hong, G.J.; Zhu, Q.S.; Zhou, X.B.; MacFarlane, S.; Yan, F.; Chen, J.P. Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to Rice black streaked dwarf virus infection in rice. New Phytol. 2017, 214, 388–399. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.R.; Huang, Y.; Yang, J.L.; Yao, S.Z.; Zhao, K.; Wang, D.H.; Qin, Q.Q.; Bian, Z.; Li, Y.; Lan, Y.; et al. Jasmonate signaling enhances RNA silencing and antiviral defense in rice. Cell Host Microbe 2020, 28, 89–103. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.F.; Hoffman, N.E. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1984, 35, 155–189. [Google Scholar] [CrossRef]
- Kende, H. Ethylene biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1993, 44, 283–307. [Google Scholar] [CrossRef]
- Zarembinski, T.I.; Theologis, A. Ethylene biosynthesis and action: A case of conservation. Plant Mol. Biol. 1994, 26, 1579–1597. [Google Scholar] [CrossRef] [PubMed]
- Singh, M.P.; Lee, F.N.; Counce, P.A.; Gibbons, J.H. Mediation of partial resistance to rice blast through anaerobic induction of ethylene. Phytopathology 2004, 94, 819–825. [Google Scholar] [CrossRef]
- Yang, C.; Li, W.; Cao, J.D.; Meng, F.W.; Yu, Y.Q.; Huang, J.K.; Jiang, L.; Liu, M.X.; Zhang, Z.G.; Chen, X.W.; et al. Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice. Plant J. 2017, 89, 338–353. [Google Scholar] [CrossRef]
- Zhai, K.R.; Liang, D.; Li, H.L.; Jiao, F.Y.; Yan, B.X.; Liu, J.; Lei, Z.Y.; Huang, L.; Gong, X.Y.; Wang, X. NLRs guard metabolism to coordinate pattern- and effector-triggered immunity. Nature 2022, 601, 245–251. [Google Scholar] [CrossRef]
- Helliwell, E.E.; Wang, Q.; Yang, Y.N. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol. J. 2013, 11, 33–42. [Google Scholar] [CrossRef]
- Hoffman, T.; Schmidt, J.S.; Zheng, X.Y.; Bent, A.F. Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol. 1999, 119, 935–950. [Google Scholar] [CrossRef] [PubMed]
- Shibata, Y.; Kawakita, K.; Takemoto, D. Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid-mediated signaling pathways. Mol. Plant Microbe Interact. 2010, 23, 1130–1142. [Google Scholar] [CrossRef] [PubMed]
- Tintor, N.; Ross, A.; Kanehara, K.; Yamada, K.; Fan, L.; Kemmerling, B.; Nürnberger, T.; Tsuda, K.; Saijo, Y. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl. Acad. Sci. USA 2013, 110, 6211–6216. [Google Scholar] [CrossRef]
- He, P.; Warren, R.F.; Zhao, T.H.; Shan, L.B.; Zhu, L.H.; Tang, X.Y.; Zhou, J.M. Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Mol. Plant Microbe Interact. 2001, 14, 1453–1457. [Google Scholar] [CrossRef]
- Gu, Y.Q.; Wildermuth, M.C.; Chakravarthy, S.; Loh, Y.T.; Yang, C.M.; He, X.H.; Han, Y.; Martin, G.B. Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 2002, 14, 817–831. [Google Scholar] [CrossRef] [PubMed]
- Berrocal-Lobo, M.; Molina, A.; Solano, R. Constitutive expression of ETHYLENERESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 2002, 29, 23–32. [Google Scholar] [CrossRef]
- Berrocal-Lobo, M.; Molina, A. Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol. Plant Microbe Interact. 2004, 17, 763–770. [Google Scholar] [CrossRef]
- Fischer, U.; Dröge-Laser, W. Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol. Plant Microbe Interact. 2004, 17, 1162–1171. [Google Scholar] [CrossRef]
- McGrath, K.C.; Dombrecht, B.; Manners, J.M.; Schenk, P.M.; Edgar, C.I.; Maclean, D.J.; Scheible, W.R.; Udvardi, M.K.; Kazan, K. Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol. 2005, 139, 949–959. [Google Scholar] [CrossRef]
- Zhu, X.L.; Qi, L.; Liu, X.; Cai, S.B.; Xu, H.J.; Huang, R.F.; Li, J.R.; Wei, X.N.; Zhang, Z.Y. The wheat ethylene response factor transcription factor pathogen-induced ERF1 mediates host responses to both the necrotrophic pathogen Rhizoctonia cerealis and freezing stresses. Plant Physiol. 2014, 164, 1499–1514. [Google Scholar] [CrossRef]
- Dong, L.; Cheng, Y.; Wu, J.; Cheng, Q.; Li, W.; Fan, S.; Jiang, L.; Xu, Z.; Kong, F.; Zhang, D.; et al. Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean. J. Exp. Bot. 2015, 66, 2635–2647. [Google Scholar] [CrossRef] [PubMed]
- Xing, L.P.; Di, Z.C.; Yang, W.W.; Liu, J.Q.; Li, M.N.; Wang, X.J.; Cui, C.F.; Wang, X.Y.; Wang, X.E.; Zhang, R.Q.; et al. Overexpression of ERF1-V from Haynaldia villosa can enhance the resistance of wheat to powdery mildew and increase the tolerance to salt and drought stresses. Front. Plant Sci. 2017, 8, 1948. [Google Scholar] [CrossRef] [PubMed]
- Lund, S.T.; Stall, R.E.; Klee, H.J. Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 1998, 10, 371–382. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.M.; Xue, L.; Chintamanani, S.; Germain, H.; Lin, H.Q.; Cui, H.T.; Cai, R.; Zuo, J.R.; Tang, X.Y.; Li, X.; et al. ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 2009, 21, 2527–2540. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Steed, A.; Travella, S.; Keller, B.; Nicholson, P. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol. 2009, 182, 975–983. [Google Scholar] [CrossRef] [PubMed]
- Shen, X.L.; Liu, H.B.; Yuan, B.; Li, X.H.; Xu, C.G.; Wang, S.P. OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant Cell Environ. 2011, 34, 179–191. [Google Scholar] [CrossRef]
- Liu, J.; Zhang, T.R.; Jia, J.Z.; Sun, J.Q. The wheat mediator subunit TaMED25 interacts with the transcription factor TaEIL1 to negatively regulate disease resistance against powdery mildew. Plant Physiol. 2016, 170, 1799–1816. [Google Scholar] [CrossRef] [PubMed]
- Pieterse, C.M.; Leon-Reyes, A.; Van der Ent, S.; Van Wees, S.C. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 2009, 5, 308–316. [Google Scholar] [CrossRef] [PubMed]
- Berens, M.L.; Berry, H.M.; Mine, A.; Argueso, C.T.; Tsuda, K. Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 2017, 55, 401–425. [Google Scholar] [CrossRef] [PubMed]
- Zhang, K.W.; Halitschke, R.; Yin, C.X.; Liu, C.J.; Gan, S.S. Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc. Natl. Acad. Sci. USA 2013, 110, 14807–14812. [Google Scholar] [CrossRef]
- Zhang, Y.; Zhao, L.; Zhao, J.; Li, Y.; Wang, J.; Guo, R.; Gan, S.; Liu, C.-J.; Zhang, K. S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiol. 2017, 175, 1082–1093. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.Y.; Liu, Y.D.; Thorne, E.T.; Yang, H.P.; Fukushige, H.; Gassmann, W.; Hildebrand, D.; Sharp, R.E.; Zhang, S.Q. Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 2003, 15, 2707–2718. [Google Scholar] [CrossRef] [PubMed]
- Yim, W.J.; Kim, K.Y.; Lee, Y.W.; Sundaram, S.P.; Lee, Y.; Sa, T.M. Real time expression of ACC oxidase and PR-protein genes mediated by Methylobacterium spp. in tomato plants challenged with Xanthomonas campestris pv. vesicatoria. J. Plant Physiol. 2014, 171, 1064–1075. [Google Scholar] [CrossRef] [PubMed]
- van Schie, C.C.; Takken, F.L. Susceptibility genes 101: How to be a good host. Annu. Rev. Phytopathol. 2014, 52, 551–581. [Google Scholar] [CrossRef] [PubMed]
- Zaidi, S.S.; Mukhtar, M.S.; Mansoor, S. Genome editing: Targeting susceptibility genes for plant disease resistance. Trends Biotechnol. 2018, 36, 898–906. [Google Scholar] [CrossRef] [PubMed]
- Gao, C.X. Genome engineering for crop improvement and future agriculture. Cell 2021, 184, 1621–1635. [Google Scholar] [CrossRef] [PubMed]
- Jørgensen, J.H. Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 1992, 63, 141–152. [Google Scholar] [CrossRef]
- Büschges, R.; Hollricher, K.; Panstruga, R.; Simons, G.; Wolter, M.; Frijters, A.; van Daelen, R.; van der Lee, T.; Diergaarde, P.; Groenendijk, J. The barley Mlo gene: A novel control element of plant pathogen resistance. Cell 1997, 88, 695–705. [Google Scholar] [CrossRef]
- Acevedo-Garcia, J.; Kusch, S.; Panstruga, R. Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytol. 2014, 204, 273–281. [Google Scholar] [CrossRef]
- Kim, M.C.; Panstruga, R.; Elliott, C.; Müller, J.; Devoto, A.; Yoon, H.W.; Park, H.C.; Cho, M.J.; Schulze-Lefert, P. Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 2002, 416, 447–451. [Google Scholar] [CrossRef]
- Aist, J.R.; Gold, R.E.; Bayles, C.J. Evidence for the involvement of molecular components of papillae in ml-o resistance to barley powdery mildew. Phytopathology 1987, 77, 17–32. [Google Scholar]
- Nekrasov, V.; Wang, C.M.; Win, J.; Lanz, C.; Weigel, D.; Kamoun, S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci. Rep. 2017, 7, 482. [Google Scholar] [CrossRef]
- Wan, D.Y.; Guo, Y.; Cheng, Y.; Hu, Y.; Xiao, S.Y.; Wang, Y.J.; Wen, Y.Q. CRISPR/Cas9-mediated mutagenesis of VvMLO3 results in enhanced resistance to powdery mildew in grapevine (Vitis vinifera). Hortic. Res. 2020, 7, 116. [Google Scholar] [CrossRef]
- Pramanik, D.; Shelake, R.M.; Park, J.; Kim, M.J.; Hwang, I.; Park, Y.; Kim, J.Y. CRISPR/Cas9-mediated generation of pathogen-resistant tomato against tomato yellow leaf curl virus and powdery mildew. Int. J. Mol. Sci. 2021, 22, 1878. [Google Scholar] [CrossRef] [PubMed]
- Li, S.N.; Lin, D.X.; Zhang, Y.W.; Deng, M.; Chen, Y.X.; Lv, B.; Li, B.S.; Lei, Y.; Wang, Y.P.; Zhao, L.; et al. Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 2022, 602, 455–460. [Google Scholar] [CrossRef]
- Bui, T.P.; Le, H.; Ta, D.T.; Nguyen, C.X.; Le, N.T.; Tran, T.T.; Van Nguyen, P.; Stacey, G.; Stacey, M.G.; Pham, N.B.; et al. Enhancing powdery mildew resistance in soybean by targeted mutation of MLO genes using the CRISPR/Cas9 system. BMC Plant Biol. 2023, 23, 533. [Google Scholar] [CrossRef]
- Lin, W.C.; Lu, C.F.; Wu, J.W.; Cheng, M.L.; Lin, Y.M.; Yang, N.S.; Black, L.; Green, S.K.; Wang, J.F.; Cheng, C.P. Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res. 2004, 13, 567–581. [Google Scholar] [CrossRef]
- Wally, O.; Jayaraj, J.; Punja, Z.K. Broad-spectrum disease resistance to necrotrophic and biotrophic pathogens in transgenic carrots (Daucus carota L.) expressing an Arabidopsis NPR1 gene. Planta 2009, 231, 131–141. [Google Scholar] [CrossRef] [PubMed]
- Parkhi, V.; Kumar, V.; Campbell, L.M.; Bell, A.A.; Shah, J.; Rathore, K.S. Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Transgenic Res. 2010, 19, 959–975. [Google Scholar] [CrossRef] [PubMed]
- Kumar, V.; Joshi, S.G.; Bell, A.A.; Rathore, K.S. Enhanced resistance against Thielaviopsis basicola in transgenic cotton plants expressing Arabidopsis NPR1 gene. Transgenic Res. 2013, 22, 359–368. [Google Scholar] [CrossRef]
- Narváez, I.; Pliego Prieto, C.; Palomo-Ríos, E.; Fresta, L.; Jiménez-Díaz, R.M.; Trapero-Casas, J.L.; Lopez-Herrera, C.; Arjona-Lopez, J.M.; Mercado, J.A.; Pliego-Alfaro, F. Heterologous expression of the AtNPR1 gene in olive and its effects on fungal tolerance. Front. Plant Sci. 2020, 11, 308. [Google Scholar] [CrossRef] [PubMed]
- Qiu, W.M.; Soares, J.; Pang, Z.Q.; Huang, Y.X.; Sun, Z.H.; Wang, N.; Grosser, J.; Dutt, M. Potential mechanisms of AtNPR1 mediated resistance against Huanglongbing (HLB) in citrus. Int. J. Mol. Sci. 2020, 21, 2009. [Google Scholar] [CrossRef] [PubMed]
- Silva, K.J.; Brunings, A.; Peres, N.A.; Mou, Z.L.; Folta, K.M. The Arabidopsis NPR1 gene confers broad-spectrum disease resistance in strawberry. Transgenic Res. 2015, 24, 693–704. [Google Scholar] [CrossRef] [PubMed]
- Fitzgerald, H.A.; Chern, M.S.; Navarre, R.; Ronald, P.C. Overexpression of (At)NPR1 in rice leads to a BTH- and environment-induced lesion-mimic/cell death phenotype. Mol. Plant Microbe Interact. 2004, 17, 140–151. [Google Scholar] [CrossRef] [PubMed]
- Quilis, J.; Peñas, G.; Messeguer, J.; Brugidou, C.; San Segundo, B. The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol. Plant Microbe Interact. 2008, 21, 1215–1231. [Google Scholar] [CrossRef]
- Xu, G.Y.; Yuan, M.; Ai, C.R.; Liu, L.J.; Zhuang, E.; Karapetyan, S.; Wang, S.P.; Dong, X.N. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 2017, 545, 491–494. [Google Scholar] [CrossRef]
Plant | Gene Name | Protein Function | Contribution to Plant Immunity | Pathogen | Reference |
---|---|---|---|---|---|
Arabidopsis | AtDMR6 | Hydroxylating SA | Negative | Hyaloperonospora parasitica | [54,56] |
Phytophthora capsici | |||||
Pseudomonas syringae | |||||
Hyaloperonospora arabidopsidis | |||||
Potato | StDMR6 | Hydroxylating SA | Negative | Botrytis cinerea | [57,58] |
Phytophthora infestans | |||||
Tomato | SlDMR6-1 | Hydroxylating SA | Negative | Pseudoidium neolycopersici | [59] |
Phytophthora capsici | |||||
Pseudomonas syringae pv. tomato | |||||
Xanthomonas gardneri | |||||
Xanthomonas perforans | |||||
Sweet basil | ObDMR6 | Hydroxylating SA | Negative | Peronospora belbahrii | [60] |
Peanut | AhS5H1 | Hydroxylating SA | Negative | Pseudomonas syringae pv. tomato DC3000 | [61] |
Peanut | AhS5H2 | Hydroxylating SA | Negative | Pseudomonas syringae pv. tomato DC3000 | [61] |
Barley | Hv2OGO | Hydroxylating SA | Negative | Fusarium graminearum | [62] |
Banana | MusaDMR6 | Hydroxylating SA | Negative | Xanthomonas campestris pv. musacearum | [63] |
Rice | OsSAH2 | Hydroxylating SA | Negative | Magnaporthe oryzae | [64,65,66] |
Xanthomonas oryzae pv. oryzae | |||||
Bipolaris oryzae | |||||
Rhizoctonia solani | |||||
Rice | OsSAH3 | Hydroxylating SA | Negative | Magnaporthe oryzae | [64,65,66] |
Xanthomonas oryzae pv. oryzae | |||||
Bipolaris oryzae | |||||
Rhizoctonia solani | |||||
Tobacco | NbACO1 | Biosynthesizing ethylene | Positive | Colletotrichum orbiculare | [67] |
Wheat | TuACO3 | Biosynthesizing ethylene | Positive | Blumeria graminis f. sp. tritici | [70] |
Arabidopsis | AtJAO1 | Hydroxylating JA | Negative | Botrytis cinerea | [71,72] |
Arabidopsis | AtJAO2 | Hydroxylating JA | Negative | Botrytis cinerea | [71,72] |
Arabidopsis | AtJAO3 | Hydroxylating JA | Negative | Botrytis cinerea | [71,72] |
Arabidopsis | AtJAO4 | Hydroxylating JA | Negative | Botrytis cinerea | [71,72] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, H.; Chen, Q.; Feng, W. The Emerging Role of 2OGDs as Candidate Targets for Engineering Crops with Broad-Spectrum Disease Resistance. Plants 2024, 13, 1129. https://doi.org/10.3390/plants13081129
Wang H, Chen Q, Feng W. The Emerging Role of 2OGDs as Candidate Targets for Engineering Crops with Broad-Spectrum Disease Resistance. Plants. 2024; 13(8):1129. https://doi.org/10.3390/plants13081129
Chicago/Turabian StyleWang, Han, Qinghe Chen, and Wanzhen Feng. 2024. "The Emerging Role of 2OGDs as Candidate Targets for Engineering Crops with Broad-Spectrum Disease Resistance" Plants 13, no. 8: 1129. https://doi.org/10.3390/plants13081129