Toward Understanding the Molecular Recognition of Fungal Chitin and Activation of the Plant Defense Mechanism in Horticultural Crops
Abstract
:1. Introduction
2. Molecular Mechanism of Plant Response to Pathogens
3. Cellular Recognition of Fungal Molecules: Chitin
4. Plant Membrane Receptors That Recognize Chitin and ChOs
5. Recognition of Chitin and Its Oligosaccharides in Horticultural Crops
6. Concluding Remarks and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Ala, F.T.; Askarne, L.; Boubaker, H.; Bo, E.H.; Ben Ao, A.A. Control of Gray Mold Disease of Tomato by Postharvest Application of Organic Acids and Salts. Plant Pathol. J. 2017, 16, 62–72. [Google Scholar] [CrossRef] [Green Version]
- Troncoso-Rojas, R.; Tiznado-Hernández, M. Alternaria alternata (black rot, black spot). In Postharvest Decay of Fruits and Vegetables: Control Strategies; Bautista-Baños, S., Ed.; Elsevier Inc.: Cambridge, MA, USA, 2014; pp. 147–187. [Google Scholar]
- Takao, K.; Akagi, Y.; Tsuge, T.; Kodama, M. Functional characterization of putative G protein-coupled receptors in the tomato pathotype of Alternaria alternata. J. Gen. Plant Pathol. 2016, 82, 82–88. [Google Scholar] [CrossRef]
- Yang, L.-N.; He, M.-H.; Ouyang, H.-B.; Zhu, W.; Pan, Z.-C.; Sui, Q.-J.; Shang, L.-P.; Zhan, J. Cross-resistance of the pathogenic fungus Alternaria alternata to fungicides with different modes of action. BMC Microbiol. 2019, 19, 205. [Google Scholar] [CrossRef] [Green Version]
- Sudheeran, P.K.; Sela, N.; Carmeli-Weissberg, M.; Ovadia, R.; Panda, S.; Feygenberg, O.; Maurer, D.; Oren-Shamir, M.; Aharoni, A.; Alkan, N. Induced defense response in red mango fruit against Colletotrichum gloeosporioides. Hortic. Res. 2021, 8, 1–11. [Google Scholar] [CrossRef]
- Alkan, N.; Friedlander, G.; Ment, D.; Prusky, D.; Fluhr, R. Simultaneous transcriptome analysis of Colletotrichum gloeosporioides and tomato fruit pathosystem reveals novel fungal pathogenicity and fruit defense strategies. New Phytol. 2015, 205, 801–815. [Google Scholar] [CrossRef]
- Delteil, A.; Gobbato, E.; Cayrol, B.; Estevan, J.; Michel-Romiti, C.; Dievart, A.; Kroj, T.; Morel, J.-B. Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol. 2016, 16, 17. [Google Scholar] [CrossRef]
- Costa-De-Oliveira, S.; Silva, A.P.; Miranda, I.M.; Salvador, A.; Azevedo, M.M.; Munro, C.A.; Rodrigues, A.G.; Pina-Vaz, C. Determination of chitin content in fungal cell wall: An alternative flow cytometric method. Cytom. Part. A 2013, 83A, 324–328. [Google Scholar] [CrossRef] [Green Version]
- Vallet, A.S.; Mesters, J.R.; Thomma, B.P. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol. Rev. 2015, 39, 171–183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pusztahelyi, T. Chitin and chitin-related compounds in plant–fungal interactions. Mycology 2018, 9, 189–201. [Google Scholar] [CrossRef]
- Asensio, J.L.; Cañada, F.J.; Siebert, H.-C.; Laynez, J.; Poveda, A.; Nieto, P.M.; Soedjanaamadja, U.; Gabius, H.-J.; Jiménez-Barbero, J. Structural basis for chitin recognition by defense proteins: GlcNAc residues are bound in a multivalent fashion by extended binding sites in hevein domains. Chem. Biol. 2000, 7, 529–543. [Google Scholar] [CrossRef] [Green Version]
- Iizasa, E.; Mitsutomi, M.; Nagano, Y. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 2010, 285, 2996–3004. [Google Scholar] [CrossRef] [Green Version]
- Petutschnig, E.K.; Jones, A.M.; Serazetdinova, L.; Lipka, U.; Lipka, V. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 2010, 285, 28902–28911. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shinya, T.; Nakagawa, T.; Kaku, H.; Shibuya, N. Chitin-mediated plant–fungal interactions: Catching, hiding and handshaking. Curr. Opin. Plant Biol. 2015, 26, 64–71. [Google Scholar] [CrossRef]
- Huang, C.; Yan, Y.; Zhao, H.; Ye, Y.; Cao, Y. Arabidopsis CPK5 phosphorylates the chitin receptor LYK5 to regulate plant innate immunity. Front. Plant Sci. 2020, 11, 702. [Google Scholar] [CrossRef]
- Kaku, H.; Nishizawa, Y.; Ishii-Minami, N.; Akimoto-Tomiyama, C.; Dohmae, N.; Takio, K.; Minami, E.; Shibuya, N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 2006, 103, 11086–11091. [Google Scholar] [CrossRef] [Green Version]
- Buendia, L.; Girardin, A.; Wang, T.; Cottret, L.; Lefebvre, B. LysM receptor-like kinase and lysM receptor-like protein families: An update on phylogeny and functional characterization. Front. Plant Sci. 2018, 9, 1531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miya, A.; Albert, P.; Shinya, T.; Desaki, Y.; Ichimura, K.; Shirasu, K.; Narusaka, Y.; Kawakami, N.; Kaku, H.; Shibuya, N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 2007, 104, 19613–19618. [Google Scholar] [CrossRef] [Green Version]
- Weibing, W.; Zhou, Z.; Wang, W.; Li, L.; Rao, S.; Wu, Y.; Zhang, X.; Menke, F.L.; Chen, S.; Zhou, J.-M. Receptor-Like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis. Plant Cell 2018, 30, 1543–1561. [Google Scholar] [CrossRef] [Green Version]
- Cao, Y.; Liang, Y.; Tanaka, K.; Nguyen, C.; Jedrzejczak, R.P.; Joachimiak, A.; Stacey, G. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 2014, 3, e03766. [Google Scholar] [CrossRef]
- Desaki, Y.; Miyata, K.; Suzuki, M.; Shibuya, N.; Kaku, H. Plant immunity and symbiosis signaling mediated by LysM receptors. Innate Immun. 2017, 24, 92–100. [Google Scholar] [CrossRef] [PubMed]
- Gubaeva, E.; Gubaev, A.; Melcher, R.L.J.; Cord-Landwehr, S.; Singh, R.; El Gueddari, N.E.; Moerschbacher, B.M. ‘Slipped sandwich’ model for chitin and chitosan perception in Arabidopsis. Mol. Plant-Microbe Interact. 2018, 31, 1145–1153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alkan, N.; Fortes, A.M. Insights into molecular and metabolic events associated with fruit response to post-harvest fungal pathogens. Front. Plant Sci. 2015, 6, 889. [Google Scholar] [CrossRef] [Green Version]
- Xu, T.; Qin, D.; Din, G.M.U.; Liu, T.; Chen, W.; Gao, L. Characterization of histological changes at the tillering stage (Z21) in resistant and susceptible wheat plants infected by Tilletia controversa Kühn. BMC Plant Biol. 2021, 21, 49. [Google Scholar] [CrossRef]
- Kim, W.; Prokchorchik, M.; Tian, Y.; Kim, S.; Jeon, H.; Segonzac, C. Perception of unrelated microbe-associated molecular patterns triggers conserved yet variable physiological and transcriptional changes in Brassica rapa ssp. pekinensis. Hortic. Res. 2020, 7, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Hu, S.-P.; Li, J.-J.; Dhar, N.; Li, J.-P.; Chen, J.-Y.; Jian, W.; Dai, X.-F.; Yang, X.-Y. Lysin motif (LysM) proteins: Interlinking manipulation of plant immunity and fungi. Int. J. Mol. Sci. 2021, 22, 3114. [Google Scholar] [CrossRef] [PubMed]
- Shinya, T.; Motoyama, N.; Ikeda, A.; Wada, M.; Kamiya, K.; Hayafune, M.; Kaku, H.; Shibuya, N. Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol. 2012, 53, 1696–1706. [Google Scholar] [CrossRef] [Green Version]
- Egusa, M.; Matsui, H.; Urakami, T.; Okuda, S.; Ifuku, S.; Nakagami, H.; Kaminaka, H. Chitin Nanofiber Elucidates the Elicitor Activity of Polymeric Chitin in Plants. Front. Plant Sci. 2015, 6, 1098. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abdul Malik, N.A.; Kumar, I.S.; Nadarajah, K. Elicitor and Receptor Molecules: Orchestrators of Plant Defense and Immunity. Int. J. Mol. Sci. 2020, 21, 963. [Google Scholar] [CrossRef] [Green Version]
- Yuan, M.; Huang, Y.; Ge, W.; Jia, Z.; Song, S.; Zhang, L.; Huang, Y. Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber. BMC Genom. 2019, 20, 144. [Google Scholar] [CrossRef] [Green Version]
- Chen, C.-L.; Yuan, F.; Li, X.-Y.; Ma, R.-C.; Xie, H. Jasmonic acid and ethylene signaling pathways participate in the defense response of Chinese cabbage to Pectobacterium carotovorum infection. J. Integr. Agric. 2021, 20, 1314–1326. [Google Scholar] [CrossRef]
- Skelly, M.J.; Furniss, J.J.; Grey, H.; Wong, K.-W.; Spoel, S.H. Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1. eLife 2019, 8, 8. [Google Scholar] [CrossRef]
- Gao, S.; Wang, F.; Niran, J.; Li, N.; Yin, Y.; Yu, C.; Jiao, C.; Yao, M. Transcriptome analysis reveals defense-related genes and pathways against Xanthomonas campestris pv. vesicatoria in pepper (Capsicum annuum L.). PLoS ONE 2021, 16, e0240279. [Google Scholar] [CrossRef]
- Sánchez-Estrada, A.; Tiznado-Hernández, M.E.; Ojeda-Contreras, A.J.; Valenzuela-Quintanar, A.I.; Troncoso-Rojas, R. Induction of enzymes and phenolic compounds related to the natural defence response of netted melon fruit by a bio-elicitor. J. Phytopathol. 2009, 157, 24–32. [Google Scholar] [CrossRef]
- Troncoso-Rojas, R.; Sanchez-Estrada, A.; Carvallo, T.; González-León, A.; Ojeda-Contreras, J.; Aguilar-Valenzuela, A.; Tiznado-Hernández, M.-E. A fungal elicitor enhances the resistance of tomato fruit to Fusarium oxysporum infection by activating the phenylpropanoid metabolic pathway. Phytoparasitica 2012, 41, 133–142. [Google Scholar] [CrossRef]
- Kishimoto, K.; Kouzai, Y.; Kaku, H.; Shibuya, N.; Minami, E.; Nishizawa, Y. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J. 2010, 64, 343–354. [Google Scholar] [CrossRef]
- Malinovsky, F.G.; Fangel, J.U.; Willats, W.G.T. The role of the cell wall in plant immunity. Front. Plant Sci. 2014, 5, 178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matilla, M.A. Metabolic responses of plants upon different plant–pathogen interactions. In Plant Metabolites and Regulation under Environmental Stress; Ahmad, P., Ahanger, M.A., Singh, V.P., Tripathi, D.K., Alam, P., Alyemeni, M.N., Eds.; Academic Press: Cambridge, MA, USA, 2018; pp. 195–214, Chapter 10. [Google Scholar]
- El Knidri, H.; Belaabed, R.; Addaou, A.; Laajeb, A.; Lahsini, A. Extraction, chemical modification and characterization of chitin and chitosan. Int. J. Biol. Macromol. 2018, 120, 1181–1189. [Google Scholar] [CrossRef] [PubMed]
- Malerba, M.; Cerana, R. Recent applications of chitin- and chitosan-based polymers in plants. Polymers 2019, 11, 839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pillai, C.K.S.; Paul, W.; Sharma, C.P. Chitin and chitosan polymers: Chemistry, solubility and fiber formation. Prog. Polym. Sci. 2009, 34, 641–678. [Google Scholar] [CrossRef]
- García, Y.H.; Troncoso-Rojas, R.; Tiznado-Hernández, M.E.; Báez-Flores, M.E.; Carvajal-Millan, E.; Rascon-Chu, A.; Lizardi-Mendoza, J.; Martínez-Robinson, K.G. Enzymatic treatments as alternative to produce chitin fragments of low molecular weight from Alternaria alternata. J. Appl. Polym. Sci. 2019, 136, 47339. [Google Scholar] [CrossRef]
- Zhan, J.; Qin, Y.; Gao, K.; Fan, Z.; Wang, L.; Xing, R.; Liu, S.; Li, P. Efficacy of a chitin-based water-soluble derivative in inducing Purpureocillium lilacinum against nematode disease (Meloidogyne incognita). Int. J. Mol. Sci. 2021, 22, 6870. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Yang, Q.; Ge, L.; Zhang, G.; Zhang, X.; Zhang, X. Chitin enhances biocontrol of Rhodotorula mucilaginosa to postharvest decay of peaches. Int. J. Biol. Macromol. 2016, 88, 465–475. [Google Scholar] [CrossRef] [PubMed]
- Sun, C.; Fu, D.; Jin, L.; Chen, M.; Zheng, X.; Yu, T. Chitin isolated from yeast cell wall induces the resistance of tomato fruit to Botrytis cinerea. Carbohydr. Polym. 2018, 199, 341–352. [Google Scholar] [CrossRef]
- Monaghan, J.; Zipfel, C. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 2012, 15, 349–357. [Google Scholar] [CrossRef] [PubMed]
- He, K.; Wu, Y. Receptor-like kinases and regulation of plant innate immunity. Enzymes 2016, 40, 105–142. [Google Scholar] [CrossRef]
- Liebrand, T.W.H.; Berg, G.C.M.V.D.; Zhang, Z.; Smit, P.; Cordewener, J.H.G.; America, A.; Sklenar, J.; Jones, A.; Tameling, W.I.L.; Robatzek, S.; et al. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl. Acad. Sci. USA 2013, 110, 10010–10015. [Google Scholar] [CrossRef] [Green Version]
- Richards, S.; Rose, L.E. The evolutionary history of LysM-RLKs (LYKs/LYRs) in wild tomatoes. BMC Evol. Biol. 2019, 19, 141. [Google Scholar] [CrossRef]
- Shimizu, T.; Nakano, T.; Takamizawa, D.; Desaki, Y.; Ishii-Minami, N.; Nishizawa, Y.; Minami, E.; Okada, K.; Yamane, H.; Kaku, H.; et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 2010, 64, 204–214. [Google Scholar] [CrossRef] [Green Version]
- Hayafune, M.; Berisio, R.; Marchetti, R.; Silipo, A.; Kayama, M.; Desaki, Y.; Arima, S.; Squeglia, F.; Ruggiero, A.; Tokuyasu, K.; et al. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl. Acad. Sci. USA 2014, 111, E404–E413. [Google Scholar] [CrossRef] [Green Version]
- Zhang, B.; Ramonell, K.; Somerville, S.; Stacey, G. Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 2002, 15, 963–970. [Google Scholar] [CrossRef] [Green Version]
- Liu, T.; Liu, Z.; Song, C.; Hu, Y.; Han, Z.; She, J.; Fan, F.; Wang, J.; Jin, C.; Chang, J.; et al. Chitin-induced dimerization activates a plant immune receptor. Science 2012, 336, 1160–1164. [Google Scholar] [CrossRef] [Green Version]
- Volk, H.; Marton, K.; Flajšman, M.; Radišek, S.; Tian, H.; Hein, I.; Podlipnik, Č.; Thomma, B.P.H.J.; Košmelj, K.; Javornik, B.; et al. Chitin-binding protein of Verticillium nonalfalfae disguises fungus from plant chitinases and suppresses chitin-triggered host immunity. Mol. Plant-Microbe Interact. 2019, 32, 1378–1390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Erwig, J.; Ghareeb, H.; Kopischke, M.; Hacke, R.; Matei, A.; Petutschnig, E.; Lipka, V. Chitin-induced and chitin elicitor receptor kinase1 (CERK1) phosphorylation-dependent endocytosis of Arabidopsis thaliana Lysin motif-containing receptor-like kinase5 (LYK5). New Phytol. 2017, 215, 382–396. [Google Scholar] [CrossRef] [Green Version]
- Yamada, K.; Yamaguchi, K.; Shirakawa, T.; Nakagami, H.; Mine, A.; Ishikawa, K.; Fujiwara, M.; Narusaka, M.; Narusaka, Y.; Ichimura, K.; et al. The Arabidopsis CERK 1-associated kinase PBL 27 connects chitin perception to MAPK activation. EMBO J. 2016, 35, 2468–2483. [Google Scholar] [CrossRef]
- Gong, B.-Q.; Wang, F.-Z.; Li, J.-F. Hide-and-Seek: Chitin-triggered plant immunity and fungal counterstrategies. Trends Plant Sci. 2020, 25, 805–816. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Yuan, L.; Staehelin, C.; Li, Y.; Ruan, J.; Liang, Z.; Xie, Z.; Wang, W.; Xie, J.; Huang, S. The lysin motif-containing receptor-like kinase 1 protein of banana is required for perception of pathogenic and symbiotic signals. New Phytol. 2019, 223, 1530–1546. [Google Scholar] [CrossRef]
- Zhou, Z.; Tian, Y.; Cong, P.; Zhu, Y. Functional characterization of an apple (Malus × domestica) LysM domain receptor encoding gene for its role in defense response. Plant Sci. 2018, 269, 56–65. [Google Scholar] [CrossRef]
- Chen, Q.; Dong, C.; Sun, X.; Zhang, Y.; Dai, H.; Bai, S. Overexpression of an apple LysM-containing protein gene, MdCERK1–2, confers improved resistance to the pathogenic fungus, Alternaria alternata, in Nicotiana benthamiana. BMC Plant Biol. 2020, 20, 146. [Google Scholar] [CrossRef]
- Zeng, L.; Velásquez, A.C.; Munkvold, K.R.; Zhang, J.; Martin, G.B. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J. 2012, 69, 92–103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liao, D.; Sun, X.; Wang, N.; Song, F.; Liang, Y. Tomato LysM receptor-like kinase SlLYK12 is involved in arbuscular mycorrhizal symbiosis. Front. Plant Sci. 2018, 9, 1004. [Google Scholar] [CrossRef] [Green Version]
- AbuQamar, S.; Chai, M.-F.; Luo, H.; Song, F.; Mengiste, T. Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell 2008, 20, 1964–1983. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, S.; Liao, C.-J.; Jaiswal, N.; Lee, S.; Yun, D.-J.; Lee, S.Y.; Garvey, M.; Kaplan, I.; Mengiste, T. Tomato PEPR1 ortholog receptor-like kinase1 regulates responses to systemin, necrotrophic fungi, and insect herbivory. Plant Cell 2018, 30, 2214–2229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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García, Y.H.; Zamora, O.R.; Troncoso-Rojas, R.; Tiznado-Hernández, M.E.; Báez-Flores, M.E.; Carvajal-Millan, E.; Rascón-Chu, A. Toward Understanding the Molecular Recognition of Fungal Chitin and Activation of the Plant Defense Mechanism in Horticultural Crops. Molecules 2021, 26, 6513. https://doi.org/10.3390/molecules26216513
García YH, Zamora OR, Troncoso-Rojas R, Tiznado-Hernández ME, Báez-Flores ME, Carvajal-Millan E, Rascón-Chu A. Toward Understanding the Molecular Recognition of Fungal Chitin and Activation of the Plant Defense Mechanism in Horticultural Crops. Molecules. 2021; 26(21):6513. https://doi.org/10.3390/molecules26216513
Chicago/Turabian StyleGarcía, Yaima Henry, Orlando Reyes Zamora, Rosalba Troncoso-Rojas, Martín Ernesto Tiznado-Hernández, María Elena Báez-Flores, Elizabeth Carvajal-Millan, and Agustín Rascón-Chu. 2021. "Toward Understanding the Molecular Recognition of Fungal Chitin and Activation of the Plant Defense Mechanism in Horticultural Crops" Molecules 26, no. 21: 6513. https://doi.org/10.3390/molecules26216513