A novel inhibitor of the jasmonic acid signaling pathway represses herbivore resistance in tea plants

Abstract

The jasmonic acid (JA) signaling pathway plays a vital role in mediating plant resistance to herbivores . The tea plant (Camellia sinensis) is one of the most important woody cash crops in the world. Due to the lack of genetic transformation systems for tea plants, how the JA signaling pathway works in tea plants has not yet been determined. Now, with the development of cross-disciplines, chemical biology provides new means for analyzing the JA signaling pathway. In the present study, the structure of the small-molecule isoquinoline compound ZINC71820901 (lyn3) was obtained from the ZINC molecular library through virtual screening based on the structure of the crystal COI1-JAZ1 co-receptor and was found to act as an inhibitor of the JA signaling pathway in both Arabidopsis and tea plants. Our results revealed that lyn3 repressed tea plant resistance to Ectropis grisescens mainly by decreasing the accumulation of (−)-epicatechin and (−)-epigallocatechin via repression of the JA signaling pathway, which functioned in a modulation manner different from that of the already known inhibitor salicylhydroxamic acid (SHAM). As a novel inhibitor of the JA signaling pathway, lyn3 provides a specific option for further research on the JA pathway.

References

[1] Howe GA, Jander G . Plant immunity to insect herbivores. Annu Rev Plant Biol. 2008; 59: 41-66.

[2] Wang JJ, Wu DW, Wang YP et al. Jasmonate action in plant defense against insects. J Exp Bot. 2019; 70: 3391-400.

[3] Wu JQ, Baldwin IT . New insights into plant responses to the attack from insect herbivores. Annu Rev Genet. 2010; 44: 1-24.

[4] Aljbory Z, Chen MS . Indirect plant defense against insect herbivores: a review. Insect Sci. 2018; 25: 2-23.

[5] Erb M, Reymond P . Molecular interactions between plants and insect herbivores. Annu Rev Plant Biol. 2019; 70: 527-57.

[6] Wasternack C, Song SS . Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot. 2017; 68: 1303-21.

[7] Ueda M, Kaji T, Kozaki W . Recent advances in plant chemical biology of jasmonates. Int J Mol Sci. 2020; 21: 1124.

[8] Andreou A, Feussner I . Lipoxygenases - structure and reaction mechanism. Phytochemistry. 2009; 70: 1504-10.

[9] Lee DS, Nioche P, Hamberg M et al. Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature. 2008; 455: 363-8.

[10] Hofmann E, Zerbe P, Schaller F . The crystal structure of Arabidopsis thaliana allene oxide cyclase: insights into the oxylipin cyclization reaction. Plant Cell. 2006; 18: 3201-17.

[11] Stintzi A, Browse J . The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA. 2000; 97: 10625-30.

[12] Staswick PE, Tiryaki I . The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis . Plant Cell. 2004; 16: 2117-27.

[13] Fonseca S, Chini A, Hamberg M et al. (+)-7-Iso-jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol. 2009; 5: 344-50.

[14] Zhang F, Yao J, Ke J et al. Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature. 2015; 525: 269-73.

[15] Dubos C, Stracke R, Grotewold E et al. MYB transcription factors in Arabidopsis . Trends Plant Sci. 2010; 15: 573-81.

[16] Pauw B, Memelink J . Jasmonate-responsive gene expression. J Plant Growth Regul. 2004; 23: 200-10.

[17] Chini A, Gimenez-Ibanez S, Goossens A et al. Redundancy and specificity in jasmonate signalling. Curr Opin Plant Biol 2016; 33: 147-56.

[18] Zhou M, Wang W . Recent advances in synthetic chemical inducers of plant immunity. Front Plant Sci. 2018; 9: 1613.

[19] Littleson MM, Baker CM, Dalencon AJ et al. Scalable total synthesis and comprehensive structure-activity relationship studies of the phytotoxin coronatine. Nat Commun. 2018; 9: 1105.

[20] Schuler G, Gorls H, Boland W . 6-Substituted indanoyl isoleucine conjugates mimic the biological activity of coronatine. Eur J Org Chem. 2001; 2001: 1663-8.

[21] Svoboda J, Boland W . Plant defense elicitors: analogues of jasmonoyl-isoleucine conjugate. Phytochemistry. 2010; 71: 1445-9.

[22] Yan JB, Li S, Gu M et al. Endogenous bioactive jasmonate is composed of a set of (+)-7-iso-JA-amino acid conjugates. Plant Physiol. 2016; 172: 2154-64.

[23] Sheard LB, Tan X, Mao H et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature. 2010; 468: 400-5.

[24] Monte I, Hamberg M, Chini A et al. Rational design of a ligand-based antagonist of jasmonate perception. Nat Chem Biol. 2014; 10: 671-6.

[25] Takaoka Y, Iwahashi M, Chini A et al. A rationally designed JAZ subtype-selective agonist of jasmonate perception. Nat Commun. 2018; 9: 3654.

[26] Pathak RK, Baunthiyal M, Shukla R et al. In silico identification of mimicking molecules as defense inducers triggering jasmonic acid mediated immunity against Alternaria blight disease in Brassica species . Front Plant Sci. 2017; 8: 609.

[27] Wang YN, Tang L, Hou Y et al. Differential transcriptome analysis of leaves of tea plant (Camellia sinensis) provides comprehensive insights into the defense responses to Ectropis oblique attack using RNA-Seq. Funct Integr Genomics. 2016; 16: 383-98.

[28] Xin ZJ, Zhang ZQ, Chen ZM et al. Salicylhydroxamic acid (SHAM) negatively mediates tea herbivore-induced direct and indirect defense against the tea geometrid Ectropis obliqua . J Plant Res. 2014; 127: 565-72.

[29] Zhang J, Zhang X, Ye M et al. The jasmonic acid pathway positively regulates the polyphenol oxidase-based defense against tea geometrid caterpillars in the tea plant (Camellia sinensis) . J Chem Ecol. 2020; 46: 308-16.

[30] Xin ZJ, Chen SL, Ge LG et al. The involvement of a herbivore-induced acyl-CoA oxidase gene, CsACX1, in the synthesis of jasmonic acid and its expression in flower opening in tea plant (Camellia sinensis) . Plant Physiol Biochem. 2019; 135: 132-40.

[31] Xin ZJ, Zhang J, Ge L et al. A putative 12-oxophytodienoate reductase gene CsOPR3 from Camellia sinensis, is involved in wound and herbivore infestation responses . Gene. 2017; 615: 18-24.

[32] Liu SA, Han BY . Differential expression pattern of an acidic 9/13-lipoxygenase in flower opening and senescence and in leaf response to phloem feeders in the tea plant. BMC Plant Biol. 2010; 10: 228.

[33] Jaghoori MM, Bleijlevens B, Olabarriaga SD . 1001 ways to run AutoDock Vina for virtual screening. J Comput Aided Mol Des. 2016; 30: 237-49.

[34] Li XW, Zhang J et al. (+)-Catechin, epicatechin and epigallocatechin are important inducible defensive compounds against Ectropis grisescens in tea plants. Plant Cell Environ. 2022; 45: 496-511.

[35] Howe GA, Major IT, Koo AJ . Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol. 2018; 69: 387-415.

[36] Jiang K, Asami T . Chemical regulators of plant hormones and their applications in basic research and agriculture. Biosci Biotechnol Biochem 2018; 82: 1265-300.

[37] Katsir L, Schilmiller AL, Staswick PE et al. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA. 2008; 105: 7100-5.

[38] Liao YY, Yu Z, Liu X et al. Effect of major tea insect attack on formation of quality-related nonvolatile specialized metabolites in tea (Camellia sinensis) leaves . J Agric Food Chem. 2019; 67: 6716-24.

[39] Yang ZW, Duan XN, Jin S et al. Regurgitant derived from the tea geometrid Ectropis obliqua suppresses wound-induced polyphenol oxidases activity in tea plants. J Chem Ecol. 2013; 39: 744-51.

[40] Xin ZJ, Li XW, Li JC et al. Application of chemical elicitor (Z)-3-hexenol enhances direct and indirect plant defenses against tea geometrid Ectropis obliqua . BioControl. 2016; 61: 1-12.

[41] Lin SB, Dong Y, Li X et al. JA-Ile-macrolactone 5b induces tea plant (Camellia sinensis) resistance to both herbivore Ectropis obliqua and pathogen Colletotrichum camelliae . Int J Mol Sci 2020; 21; 1828.

[42] Ye M, Liu M, Erb M et al. Indole primes defence signalling and increases herbivore resistance in tea plants. Plant Cell Environ. 2021; 44: 1165-77.

[43] Treutter D . Significance of flavonoids in plant resistance: a review. Environ Chem Lett 2006; 4: 147-57.

[44] Wang WW, Zheng C, Hao WJ et al. Transcriptome and metabolome analysis reveal candidate genes and biochemicals involved in tea geometrid defense in Camellia sinensis . PLoS One. 2018; 13: e0201670.

[45] Wang YC, Qian WJ, Li NN et al. Metabolic changes of caffeine in tea plant (Camellia sinensis (L.) O. Kuntze) as defense response to Colletotrichum fructicola . J Agric Food Chem. 2016; 64: 6685-93.

[46] Forli S, Huey R, Pique ME et al. Computational protein-ligand docking and virtual drug screening with the AutoDock suite. Nat Protoc 2016; 11: 905-19.

[47] Ghasemi JB, Shiri F, Pirhadi S et al. Discovery of new potential antimalarial compounds using virtual screening of ZINC database. Comb Chem High Throughput Screen. 2015;18:227-34.

[48] Huang C, Zhang J, Zhang X et al. Two new polyphenol oxidase genes of tea plant (Camellia sinensis) respond differentially to the regurgitant of tea geometrid, Ectropis obliqua . Int J Mol Sci 2018; 19: 2414.

[49] Wang WW, Zhou P, Mo X et al. Induction of defense in cereals by 4-fluorophenoxyacetic acid suppresses insect pest populations and increases crop yields in the field. Proc Natl Acad Sci USA. 2020; 117: 12017-28.