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Role of jasmonate signaling in rice resistance to the leaf folder Cnaphalocrocis medinalis

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Abstract

Key message

Jasmonate-induced accumulation of anti-herbivore compounds mediates rice resistance to the leaf folder Cnaphalocrocis medinalis.

Abstract

The rice leaf folder (LF), Cnaphalocrocis medinalis, is one of the most destructive insect pests in the paddy field. LF larvae induces leaf folding and scrapes the upper epidermis and mesophyll tissues reducing photosynthesis and yield in rice. Identifying plant defense pathways and genes involved in LF resistance is essential to understand better this plant–insect interaction and develop new control strategies for this pest. Jasmonate (JA) signaling controls a plethora of plant defenses against herbivores. Using RNA-seq time series analysis, we characterized changes in the transcriptome of wild-type (WT) leaves in response to LF damage and measured the dynamics of accumulation of JA phytohormone pools in time-course experiments. Genes related to JA signaling and responses, known to mediate resistance responses to herbivores, were induced by LF and were accompanied by an increment in the levels of JA pools in damaged leaves. The accumulation of defense compounds such as phenolamides and trypsin proteinase inhibitor (TPI) also increased after LF infestation in WT but not in JA mutant plants impaired in JA biosynthesis (aoc-2) and signaling (myc2-5). Consistent with all these responses, we found that LF larvae performed better in the JA mutant backgrounds than in the WT plants. Our results show that JA signaling regulates LF-induced accumulation of TPI and phenolamides and that these compounds are likely an essential part of the defense arsenal of rice plants against this insect pest.

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Data availability

The raw sequence data reported in this paper has been deposited in the Genome Sequence Archive at the BIG Data Center (http://bigd.big.ac.cn/gsa), Beijing Institute of Genomics (BIG), Chinese Academy of Sciences, under Accession No. CRA004405.

References

  • Alamgir KM, Hojo Y, Christeller JT, Fukumoto K, Isshiki R, Shinya T, Baldwin IT, Galis I (2016) Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory. Plant Cell Environ 39:453–466

    Article  CAS  PubMed  Google Scholar 

  • Arimura G-i (2021) Making sense of the way plants sense herbivores. Trends Plant Sci 26:288–298

    Article  CAS  PubMed  Google Scholar 

  • Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25:1091–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheah BH, Lin HH, Chien HJ, Liao CT, Liu LYD, Lai CC, Lin YF, Chuang WP (2020) SWATH-MS-based quantitative proteomics reveals a uniquely intricate defense response in Cnaphalocrocis medinalis-resistant rice. Sci Rep 10:6597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CY, Liu YQ, Song WM, Chen DY, Chen FY, Chen XY, Chen ZW, Ge SX, Wang CZ, Zhan S, Chen XY, Mao YB (2019) An effector from cotton bollworm oral secretion impairs host plant defense signaling. Proc Natl Acad Sci USA 116:14331–14338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chini A, Gimenez-Ibanez S, Goossens A, Solano R (2016) Redundancy and specificity in jasmonate signalling. Curr Opin Plant Biol 33:147–156

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Monte I, Zamarreno AM, Hamberg M, Lassueur S, Reymond P, Weiss S, Stintzi A, Schaller A, Porzel A, Garcia-Mina JM, Solano R (2018) An OPR3-independent pathway uses 4,5-didehydrojasmonate for jasmonate synthesis. Nat Chem Biol 14:171–178

    Article  CAS  PubMed  Google Scholar 

  • Deng Y, Lu S (2017) Biosynthesis and regulation of phenylpropanoids in plants. Crit Rev Plant Sci 36:257–290

    Article  Google Scholar 

  • Dong X, Gao Y, Chen W, Wang W, Gong L, Liu X, Luo J (2015) Spatiotemporal distribution of phenolamides and the genetics of natural variation of hydroxycinnamoyl spermidine in rice. Mol Plant 8:111–121

    Article  CAS  PubMed  Google Scholar 

  • Erb M, Kliebenstein DJ (2020) Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy. Plant Physiol 184:39–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erb M, Reymond P (2019) Molecular interactions between plants and insect herbivores. Annu Rev Plant Biol 70:527–557

    Article  CAS  PubMed  Google Scholar 

  • Figon F, Baldwin IT, Gaquerel E (2021) Ethylene is a local modulator of jasmonate-dependent phenolamide accumulation during Manduca sexta herbivory in Nicotiana attenuata. Plant Cell Environ 44:964–981

    Article  CAS  PubMed  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    Article  CAS  PubMed  Google Scholar 

  • Fu W, Jin G, Jiménez-Alemán GH, Wang X, Song J, Li S, Lou Y, Li R (2021) The jasmonic acid-amino acid conjugates JA-Val and JA-Leu are involved in rice resistance to herbivores. Plant Cell Environ. https://doi.org/10.1111/pce.14202

    Article  PubMed  Google Scholar 

  • Guo TW, Liao CT, Chuang WP (2019) Defensive responses of rice cultivars resistant to Cnaphalocrocis medinalis (Lepidoptera: Crambidae). Arthropod Plant Interact 13:611–620

    Article  Google Scholar 

  • Gurr GM, Read DMY, Catindig JLA, Cheng J, Liu J, La Pham L, Heong KL (2012) Parasitoids of the rice leaffolder Cnaphalocrocis medinalis and prospects for enhancing biological control with nectar plants. Agr Forest Entomol 14:1–12

    Article  Google Scholar 

  • Howe GA, Major IT, Koo AJ (2018) Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69:387–415

    Article  CAS  PubMed  Google Scholar 

  • Kaur H, Heinzel N, Schoettner M, Baldwin IT, Galis I (2010) R2R3-NaMYB8 Regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731–1747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar P, Pandit SS, Steppuhn A, Baldwin IT (2014) Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46’s role in a nicotine-mediated antipredator herbivore defense. Proc Natl Acad Sci USA 111:1245–1252

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Bhutani S, Singh R, Chauhan R, Chowdhury VK, Jain RK (2009) Enhanced resistance against the rice leaffolder (Cnaphalocrocis medinalis) in transgenic rice plants containing the potato proteinase inhibitor II gene. Entomol Gen 32:11–22

    Article  Google Scholar 

  • Li R, Llorca LC, Schuman MC, Wang Y, Wang L, Joo Y, Wang M, Vassao DG, Baldwin IT (2018) ZEITLUPE in the roots of wild tobacco regulates jasmonate-mediated nicotine biosynthesis and resistance to a generalist herbivore. Plant Physiol 177:833–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Weldegergis BT, Li J, Jung C, Qu J, Sun Y, Qian H, Tee C, van Loon JJA, Dicke M, Chua NH, Liu SS, Ye J (2014) Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26:4991–5008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Zhang J, Li J, Zhou G, Wang Q, Bian W, Erb M, Lou Y (2015) Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores. Elife 4:e04805

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin Y, Sun Z, Li Z, Xue R, Cui W, Sun S, Liu T, Zeng R, Song Y (2019) Deficiency in silicon transporter Lsi1 compromises inducibility of anti-herbivore defense in rice plants. Front Plant Sci 10:652

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu J, Robert CAM, Riemann M, Cosme M, Mène-Saffranè L, Massana J, Stout MJ, Lou YG, Gershenzon J, Erb M (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol 167:1100–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Padmavathi C, Katti G, Padmakumari AP, Voleti SR, Rao LVS (2013) The effect of leaffolder Cnaphalocrocis medinalis (Guenee) Lepidoptera: pyralidae injury on the plant physiology and yield loss in rice. J Appl Entomol 137:249–256

    Article  Google Scholar 

  • Peng M, Gao Y, Chen W, Wang W, Shen S, Shi J, Wang C, Zhang Y, Zou L, Wang S, Wan J, Liu X, Gong L, Luo J (2016) Evolutionarily distinct BAHD N-acyltransferases are responsible for natural variation of aromatic amine conjugates in rice. Plant Cell 28:1533–1550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi J, Zhou G, Yang L, Erb M, Lu Y, Sun X, Cheng J, Lou Y (2011) The chloroplast-localized phospholipases D alpha 4 and alpha 5 regulate herbivore-induced direct and indirect defenses in rice. Plant Physiol 157:1987–1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schweizer F, Fernandez-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P (2013) Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25:3117–3132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senthil-Nathan S (2019) Effect of methyl jasmonate (MeJA)-induced defenses in rice against the rice leaffolder Cnaphalocrocis medinalis (Guenee) (Lepidoptera: Pyralidae). Pest Manag Sci 75:460–465

    Article  CAS  PubMed  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Dam NM, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568

    Article  PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) 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 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L, Hu L, Li J, Han X, Zhang T, Lu J, Zhang G, Lou Y (2012) Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett 15:1130–1139

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Wang X, Zu H, Zeng X, Baldwin IT, Lou Y, Li R (2021) Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore. New Phytol 230:1639–1652

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Li N, Kitano T, Li P, Spindel JE, Wang L, Bai G, Xiao Y, McCouch SR, Ishihara A, Zhang J, Yang X, Chen Z, Wei J, Ge H, Jander G, Yan J (2021) Genetic mapping identifies a rice naringenin O-glucosyltransferase that influences insect resistance. Plant J. https://doi.org/10.1111/tpj.15244

    Article  PubMed  Google Scholar 

  • Ye M, Luo SM, Xie JF, Li YF, Xu T, Liu Y, Song YY, Zhu-Salzman K, Zeng RS (2012) Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. Plos One 7:e36214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, Zhu-Salzman K, Xie J, Cai K, Luo S, Zeng R (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA 110:E3631–E3639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Jingjing Jin, Xiaohan Zhang and Yingying Tang for technical assistance, and Genshen Xie for the assistance of leaf folder rearing. This work was supported by the Hundred-Talent Program of Zhejiang University (to R.L.), a grant from Max Planck Partner Group Program (to R.L.) and the earmarked fund for China Agriculture Research System (CARS-01-40, to Y. L.).

Funding

This work was supported by the Hundred-Talent Program of Zhejiang University (to R.L.), a grant from Max Planck Partner Group Program (to R.L.) and the earmarked fund for China Agriculture Research System (CARS-01-40, to Y. L.).

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RL designed the research. YZ and XW performed experiments. RL, LCL, JL and YL analyzed data. RL and LCLwrote the manuscript.

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Correspondence to Ran Li.

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Zhuang, Y., Wang, X., Llorca, L.C. et al. Role of jasmonate signaling in rice resistance to the leaf folder Cnaphalocrocis medinalis. Plant Mol Biol 109, 627–637 (2022). https://doi.org/10.1007/s11103-021-01208-x

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