Rice responds to Spodoptera frugiperda infestation via epigenetic regulation of H3K9ac in the jasmonic acid signaling and phenylpropanoid biosynthesis pathways.

Publisher: Springer Country of Publication: Germany NLM ID: 9880970 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-203X (Electronic) Linking ISSN: 07217714 NLM ISO Abbreviation: Plant Cell Rep Subsets: MEDLINE

Original Publication: Berlin ; New York : Springer, 1981-

Oryza*/metabolism ; Cyclopentanes* ; Oxylipins*; Animals ; Spodoptera/genetics ; Histones/metabolism ; Epigenesis, Genetic ; Larva/genetics

Key Message: This study provided important insights into the complex epigenetic regulatory of H3K9ac-modified genes involved in the jasmonic acid signaling and phenylpropanoid biosynthesis pathways of rice in response to Spodoptera frugiperda infestation. Physiological and molecular mechanisms underlying plant responses to insect herbivores have been well studied, while epigenetic modifications such as histone acetylation and their potential regulation at the genomic level of hidden genes remain largely unknown. Histone 3 lysine 9 acetylation (H3K9ac) is an epigenetic marker widely distributed in plants that can activate gene transcription. In this study, we provided the genome-wide profiles of H3K9ac in rice (Oryza sativa) infested by fall armyworm (Spodoptera frugiperda, FAW) using CUT&Tag-seq and RNA-seq. There were 3269 and 4609 up-regulated genes identified in plants infested by FAW larvae for 3 h and 12 h, respectively, which were mainly enriched in alpha-linolenic acid and phenylpropanoid pathways according to transcriptomic analysis. In addition, CUT&Tag-seq analysis revealed increased H3K9ac in FAW-infested plants, and there were 422 and 543 up-regulated genes enriched with H3K9ac observed at 3 h and 12 h after FAW feeding, respectively. Genes with increased H3K9ac were mainly enriched in the transcription start site (TSS), suggesting that H3K9ac is related to gene transcription. Integrative analysis of both RNA-seq and CUT&Tag-seq data showed that up-expressed genes with H3K9ac enrichment were mainly involved in the jasmonic acid (JA) and phenylpropanoid pathways. Particularly, two spermidine hydroxycinnamoyl transferase genes SHT1 and SHT2 involved in phenolamide biosynthesis were highly modified by H3K9ac in FAW-infested plants. Furthermore, the Ossht1 and Ossht2 transgenic lines exhibited decreased resistance against FAW larvae. Our findings suggest that rice responds to insect herbivory via H3K9ac epigenetic regulation in the JA signaling and phenolamide biosynthesis pathways.
(© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Allis CD, Jenuwein T (2016) The molecular hallmarks of epigenetic control. Nat Rev Genet 17:487–500. https://doi.org/10.1038/nrg.2016.59. (PMID: 10.1038/nrg.2016.5927346641)
Asensi-Fabado MA, Amtmann A, Perrella G (2017) Plant responses to abiotic stress: the chromatin context of transcriptional regulation. Biochim Biophys Acta Gene Regul Mech 1860:106–122. https://doi.org/10.1016/j.bbagrm.2016.07.015. (PMID: 10.1016/j.bbagrm.2016.07.01527487458)
Atighi MR, Verstraeten B, De Meyer T, Kyndt T (2021) Genome-wide shifts in histone modifications at early stage of rice infection with Meloidogyne graminicola. Mol Plant Pathol 22:440–455. https://doi.org/10.1111/mpp.13037. (PMID: 10.1111/mpp.13037335806307938626)
Baerenfaller K, Shu H, Hirsch-Hoffmann M, Fütterer J, Opitz L, Rehrauer H et al (2016) Diurnal changes in the histone H3 signature H3K9ac|H3K27ac|H3S28p are associated with diurnal gene expression in Arabidopsis. Plant Cell Environ 39:2557–2569. https://doi.org/10.1111/pce.12811. (PMID: 10.1111/pce.1281127487196)
Barah P, Bones AM (2015) Multidimensional approaches for studying plant defence against insects: from ecology to omics and synthetic biology. J Exp Bot 66:479–493. https://doi.org/10.1093/jxb/eru489. (PMID: 10.1093/jxb/eru48925538257)
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x. (PMID: 10.1111/j.2517-6161.1995.tb02031.x)
Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412. https://doi.org/10.1038/nature05915. (PMID: 10.1038/nature0591517522673)
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170. (PMID: 10.1093/bioinformatics/btu170246954044103590)
Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330:612–616. https://doi.org/10.1126/science.1191078. (PMID: 10.1126/science.1191078210306443772643)
Bossdorf O, Richards CL, Pigliucci M (2007) Epigenetics for ecologists. Ecol Lett 11:106–115. https://doi.org/10.1111/j.1461-0248.2007.01130.x. (PMID: 10.1111/j.1461-0248.2007.01130.x18021243)
Brusslan JA, Bonora G, Rus-Canterbury AM, Tariq F, Jaroszewicz A, Pellegrini M (2015) A genome-wide chronological study of gene expression and two histone modifications, H3K4me3 and H3K9ac, during developmental leaf senescence. Plant Physiol 168:1246–1261. https://doi.org/10.1104/pp.114.252999. (PMID: 10.1104/pp.114.252999258023674528724)
Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X et al (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant 6:1769–1780. https://doi.org/10.1093/mp/sst080. (PMID: 10.1093/mp/sst08023702596)
Chen S, Zhou Y, Chen Y, Gu J, Biotechnology H (2018) fastp: an ultrafast all-in-one FASTQ preprocessor. Bioinformatics 34:12. https://doi.org/10.1101/274100. (PMID: 10.1101/274100)
Cohen SP, Leach JE (2019) Abiotic and biotic stresses induce a core transcriptome response in rice. Sci Rep 9:6273. https://doi.org/10.1038/s41598-019-42731-8. (PMID: 10.1038/s41598-019-42731-8310007466472405)
Cui X, Zheng Y, Lu Y, Issakidis-Bourguet E, Zhou DX (2021) Metabolic control of histone demethylase activity involved in plant response to high temperature. Plant Physiol 185:1813–1828. https://doi.org/10.1093/plphys/kiab020. (PMID: 10.1093/plphys/kiab020337939498133595)
Douglas AE (2018) Strategies for enhanced crop resistance to insect pests. Annu Rev Plant Biol 69:637–660. https://doi.org/10.1146/annurev-arplant-042817-040248. (PMID: 10.1146/annurev-arplant-042817-04024829144774)
Du Z, Li H, Wei Q, Zhao X, Wang C, Zhu Q et al (2013) Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. J Mol Plant 6:1463–1472. https://doi.org/10.1093/mp/sst018. (PMID: 10.1093/mp/sst018)
Erb M, Reymond P (2019) Molecular interactions between plants and insect herbivores. Annu Rev Plant Biol 70:527–557. https://doi.org/10.1146/annurev-arplant-050718-095910. (PMID: 10.1146/annurev-arplant-050718-09591030786233)
Fang H, Liu X, Thorn G, Duan J, Tian L (2014) Expression analysis of histone acetyltransferases in rice under drought stress. Biochem Biophys Res Commun 443:400–405. https://doi.org/10.1016/j.bbrc.2013.11.102. (PMID: 10.1016/j.bbrc.2013.11.10224309107)
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. https://doi.org/10.1111/pce.13955. (PMID: 10.1111/pce.1395533215737)
Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185–208. https://doi.org/10.1146/annurev-genet-110711-155511. (PMID: 10.1146/annurev-genet-110711-15551122934640)
Grativol C, Hemerly AS, Ferreira PCG (2012) Genetic and epigenetic regulation of stress responses in natural plant populations. Biochim Biophys Acta Gene Regul Mech 1819:176–185. https://doi.org/10.1016/j.bbagrm.2011.08.010. (PMID: 10.1016/j.bbagrm.2011.08.010)
Grover S, Shinde S, Puri H, Palmer N, Sarath G, Sattler SE et al (2022) Dynamic regulation of phenylpropanoid pathway metabolites in modulating sorghum defense against fall armyworm. Front Plant Sci 13:1019266. https://doi.org/10.3389/fpls.2022.1019266. (PMID: 10.3389/fpls.2022.1019266365074379732255)
Hilker M, Schmülling T (2019) Stress priming, memory, and signaling in plants: stress priming, memory, and signaling in plants. Plant Cell Environ 42:753–761. https://doi.org/10.1111/pce.13526. (PMID: 10.1111/pce.1352630779228)
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. https://doi.org/10.1146/annurev.arplant.59.032607.092825. (PMID: 10.1146/annurev.arplant.59.032607.09282518031220)
Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K et al (2011) Trichostatin a selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS ONE 6:e22132. https://doi.org/10.1371/journal.pone.0022132. (PMID: 10.1371/journal.pone.0022132218115643141014)
Jiang Y, Liu J, Xie M, Li Y (2019) Observation on law of diffusion damage of Spodoptera frugiperda in China in 2019. Plant Prot 45:10–19. https://doi.org/10.16688/j.zwbh.2019539. (PMID: 10.16688/j.zwbh.2019539)
Karban R, Chen Y (2007) Induced resistance in rice against insects. Bull Entomol Res 97:327–335. https://doi.org/10.1017/S0007485307005056. (PMID: 10.1017/S000748530700505617645814)
Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, Minami E (2012) Simultaneous RNA-Seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS ONE 7:e49423. https://doi.org/10.1371/journal.pone.0049423. (PMID: 10.1371/journal.pone.0049423231398453490861)
Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S et al (2013) Improvement of the Oryza sativa nipponbare reference genome using next generation sequence and optical map data. Rice 6:4. https://doi.org/10.1186/1939-8433-6-4. (PMID: 10.1186/1939-8433-6-4242803745395016)
Kaya-Okur HS, Wu SJ, Codomo CA, Pledger ES, Bryson TD, Henikoff JG et al (2019) CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat Commun 10:1930. https://doi.org/10.1038/s41467-019-09982-5. (PMID: 10.1038/s41467-019-09982-5310368276488672)
Kouzarides T (2007) SnapShot: histone-modifying enzymes. Cell 131(4):822–822.e1. https://doi.org/10.1016/j.cell.2007.11.005. (PMID: 10.1016/j.cell.2007.11.00518022374)
Kumar V, Thakur JK, Prasad M (2021) Histone acetylation dynamics regulating plant development and stress responses. Cell Mol Life Sci 78:4467–4486. https://doi.org/10.1007/s00018-021-03794-x. (PMID: 10.1007/s00018-021-03794-x33638653)
Kundu P, Vadassery J (2021) Role of WRKY transcription factors in plant defense against lepidopteran insect herbivores: an overview. J Plant Biochem Biotechnol 30:698–707. https://doi.org/10.1007/s13562-021-00730-9. (PMID: 10.1007/s13562-021-00730-9)
Kurita K, Sakamoto T, Yagi N, Sakamoto Y, Ito A, Nishino N et al (2017) Live imaging of H3K9 acetylation in plant cells. Sci Rep 7:45894. https://doi.org/10.1038/srep45894. (PMID: 10.1038/srep45894284180195394682)
Laura B, Silvia P, Francesca F, Benedetta S, Carla C (2018) Epigenetic control of defense genes following MeJA-induced priming in rice (O. sativa). J Plant Physiol 228:166–177. https://doi.org/10.1016/j.jplph.2018.06.007. (PMID: 10.1016/j.jplph.2018.06.00729936261)
Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y et al (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243. https://doi.org/10.1371/journal.pgen.1002243. (PMID: 10.1371/journal.pgen.1002243218766823158056)
Li S, Yang H, Liu Y-F, Liao Q-R, Du J, Jin DC (2012) Transcriptome and gene expression analysis of the rice leaf folder, Cnaphalocrosis medinalis. PLoS ONE 7:e47401. https://doi.org/10.1371/journal.pone.0047401. (PMID: 10.1371/journal.pone.0047401231852383501527)
Li H, Yan S, Zhao L, Tan J, Zhang Q, Gao F et al (2014) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 14:105. https://doi.org/10.1186/1471-2229-14-105. (PMID: 10.1186/1471-2229-14-105247583734005470)
Li J, Zhu L, Hull JJ, Liang S, Daniell H, Jin S et al (2016) Transcriptome analysis reveals a comprehensive insect resistance response mechanism in cotton to infestation by the phloem feeding insect Bemisia tabaci (whitefly). Plant Biotechnol J 14:1956–1975. https://doi.org/10.1111/pbi.12554. (PMID: 10.1111/pbi.12554269233395042180)
Li S, Lin YCJ, Wang P, Zhang B, Li M, Chen S et al (2019) The AREB1 transcription factor influences histone acetylation to regulate drought responses and tolerance in Populus trichocarpa. Plant Cell 31:663–686. https://doi.org/10.1105/tpc.18.00437. (PMID: 10.1105/tpc.18.0043730538157)
Li S, He X, Gao Y, Zhou C, Chiang VL, Li W (2021) Histone acetylation changes in plant response to drought stress. Genes 12:1409. https://doi.org/10.3390/genes12091409. (PMID: 10.3390/genes12091409345733918468061)
Liu X, Luo M, Zhang W, Zhao J, Zhang J, Wu K et al (2012) Histone acetyltransferases in rice (Oryza sativa L.): phylogenetic analysis, subcellular localization and expression. BMC Plant Biol 12:145. https://doi.org/10.1186/1471-2229-12-145. (PMID: 10.1186/1471-2229-12-145228945653502346)
Liu Q, Wang X, Tzin V, Romeis J, Peng Y, Li Y (2016) Combined transcriptome and metabolome analyses to understand the dynamic responses of rice plants to attack by the rice stem borer Chilo suppressalis (lepidoptera: crambidae). BMC Plant Biol 16:259. https://doi.org/10.1186/s12870-016-0946-6. (PMID: 10.1186/s12870-016-0946-6279233455142284)
Liu H, Cheng Y, Wang X, Francis F, Wang Q, Liu X et al (2022) Biochemical and morphological mechanisms underlying the performance and preference of fall armyworm (Spodoptera frugiperda) on wheat and faba bean plants. InSects 13:317. https://doi.org/10.3390/insects13040317. (PMID: 10.3390/insects13040317354477589028518)
Lopes FB, Sant’Ana J (2019) Responses of spodoptera frugiperda and trichogramma pretiosum to rice plants exposed to herbivory and phytohormones. Neotrop Entomol 48:381–390. https://doi.org/10.1007/s13744-018-0661-0. (PMID: 10.1007/s13744-018-0661-030569388)
Ma C, Li R, Sun Y, Zhang M, Li S, Xu Y et al (2022) ZmMYC2s play important roles in maize responses to simulated herbivory and jasmonate. J Integr Plant Biol 65:1041–1058. https://doi.org/10.1111/jipb.13404. (PMID: 10.1111/jipb.1340436349965)
Malook S, Xu Y, Qi J, Li J, Wang L, Wu J (2021) Mythimna separata herbivory primes maize resistance in systemic leaves. J Exp Bot 72:3792–3805. https://doi.org/10.1093/jxb/erab083. (PMID: 10.1093/jxb/erab083336479318096606)
Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA et al (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149. https://doi.org/10.1093/pcp/pcn101. (PMID: 10.1093/pcp/pcn10118625610)
Matthias E (2018) Plant defenses against herbivory: closing the fitness gap. Trends Plant Sci 23:187–194. https://doi.org/10.1016/j.tplants.2017.11.005. (PMID: 10.1016/j.tplants.2017.11.005)
Onkokesung N, Gaquerel E, Kotkar H, Kaur H, Baldwin IT, Galis I (2012) MYB8 controls inducible phenolamide levels by activating three novel hydroxycinnamoyl-Coenzyme A: polyamine transferases in Nicotiana attenuata. Plant Physiol 158:389–407. https://doi.org/10.1104/pp.111.187229. (PMID: 10.1104/pp.111.18722922082505)
Onosato H, Fujimoto G, Higami T, Sakamoto T, Yamada A, Suzuki T et al (2022) Sustained defense response via volatile signaling and its epigenetic transcriptional regulation. Plant Physiol 189:922–933. https://doi.org/10.1093/plphys/kiac077. (PMID: 10.1093/plphys/kiac077352013469157098)
Onufriev AV, Schiessel H (2019) The nucleosome: from structure to function through physics. Curr Opin Struct Biol 56:119–130. https://doi.org/10.1016/j.sbi.2018.11.003. (PMID: 10.1016/j.sbi.2018.11.00330710748)
Qi J, ul Malook S, Shen G, Gao L, Zhang C, Li J et al (2018) Current understanding of maize and rice defense against insect herbivores. Plant Divers 40:189–195. https://doi.org/10.1016/j.pld.2018.06.006. (PMID: 10.1016/j.pld.2018.06.006307405646137261)
Qiu C, Zeng J, Tang Y, Gao Q, Xiao W, Lou Y (2023) The fall armyworm, Spodoptera frugiperda (lepidoptera: Noctuidae), influences Nilaparvata lugens population growth directly, by preying on its eggs, and indirectly, by inducing defenses in rice. Int J Mol Sci 24:8754. https://doi.org/10.3390/ijms24108754. (PMID: 10.3390/ijms241087543724010210217797)
Ramaroson ML, Koutouan C, Helesbeux JJ, Le Clerc V, Hamama L, Geoffriau E et al (2022) Role of phenylpropanoids and flavonoids in plant resistance to pests and diseases. Molecules 27:8371. https://doi.org/10.3390/molecules27238371. (PMID: 10.3390/molecules27238371365004599735708)
Rando OJ (2012) Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr Opin Genet Dev 22:148–155. https://doi.org/10.1016/j.gde.2012.02.013. (PMID: 10.1016/j.gde.2012.02.013224404803345062)
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616. (PMID: 10.1093/bioinformatics/btp61619910308)
Roumani M, Le Bot J, Boisbrun M, Magot F, Péré A, Robin C et al (2022) Transcriptomics and metabolomics analyses reveal high induction of the phenolamide pathway in tomato plants attacked by the leafminer Tuta absoluta. Metabolites 12:484. https://doi.org/10.3390/metabo12060484. (PMID: 10.3390/metabo12060484357364169230075)
Schuman MC, Baldwin IT (2016) The layers of plant responses to insect herbivores. Annu Rev Entomol 61:373–394. https://doi.org/10.1146/annurev-ento-010715-023851. (PMID: 10.1146/annurev-ento-010715-02385126651543)
Schweizer F, Bodenhausen N, Lassueur S, Masclaux FG, Reymond P (2013a) Differential contribution of transcription factors to Arabidopsis thaliana defense against Spodoptera littoralis. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00013. (PMID: 10.3389/fpls.2013.00013233827343563046)
Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G et al (2013b) Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25:3117–3132. https://doi.org/10.1105/tpc.113.115139. (PMID: 10.1105/tpc.113.115139239438623784603)
Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75–100. https://doi.org/10.1146/annurev.biochem.76.052705.162114. (PMID: 10.1146/annurev.biochem.76.052705.16211417362198)
Sharma C, Kumar S, Saripalli G, Jain N, Raghuvanshi S, Sharma JB et al (2019) H3K4/K9 acetylation and Lr28-mediated expression of six leaf rust responsive genes in wheat (Triticum aestivum). Mol Genet Genomics 294:227–241. https://doi.org/10.1007/s00438-018-1500-z. (PMID: 10.1007/s00438-018-1500-z30298213)
Song J, Henry H, Tian L (2020) Drought-inducible changes in the histone modification H3K9ac are associated with drought-responsive gene expression in Brachypodium distachyon. Plant Biol J 22:433–440. https://doi.org/10.1111/plb.13057. (PMID: 10.1111/plb.13057)
Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62:82–86. https://doi.org/10.2307/3494083. (PMID: 10.2307/3494083)
Stout MJ, Riggio MR, Yang Y (2009) Direct induced resistance in Oryza sativa to Spodoptera frugiperda. Environ Entomol 38:1174–1181. https://doi.org/10.1603/022.038.0426. (PMID: 10.1603/022.038.042619689897)
Sun X, Hu C, Jia H, Wu Q, Shen X, Zhao S et al (2021) Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China. J Integr Agric 20:664–672. https://doi.org/10.1016/S2095-3119(19)62839-X. (PMID: 10.1016/S2095-3119(19)62839-X)
Tao X, Feng S, Zhao T, Guan X (2020) Efficient chromatin profiling of H3K4me3 modification in cotton using CUT&Tag. Plant Methods 16:120. https://doi.org/10.1186/s13007-020-00664-8. (PMID: 10.1186/s13007-020-00664-8328845777460760)
Tzin V, Hojo Y, Strickler SR, Bartsch LJ, Archer CM, Ahern KR et al (2017) Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding. J Exp Bot 68:4709–4723. https://doi.org/10.1093/jxb/erx274. (PMID: 10.1093/jxb/erx274289817815853842)
Van Dam NM, Horn M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568. https://doi.org/10.1023/A:1010341022761. (PMID: 10.1023/A:101034102276111441445)
Wang W, Yu Z, Meng J et al (2020a) Rice phenolamindes reduce the survival of female adults of the white-backed planthopper Sogatella furcifera. Sci Rep 10:5778. https://doi.org/10.1038/s41598-020-62752-y. (PMID: 10.1038/s41598-020-62752-y322388507113316)
Wang Y, Liu Q, Du L, Hallerman EM, Li Y (2020b) Transcriptomic and metabolomic responses of rice plants to Cnaphalocrocis medinalis caterpillar infestation. InSects 11:705. https://doi.org/10.3390/insects11100705. (PMID: 10.3390/insects11100705330764197602657)
Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of nicotiana attenuata. Plant Cell 19:1096–1122. https://doi.org/10.1105/tpc.106.049353. (PMID: 10.1105/tpc.106.049353174008941867352)
Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B et al (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327. https://doi.org/10.1186/s12870-014-0327-y. (PMID: 10.1186/s12870-014-0327-y254325174262988)
Xu J, Wang X, Zu H, Zeng X, Baldwin IT, Lou Y et al (2021) Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore. New Phytol 230:1639–1652. https://doi.org/10.1111/nph.17251. (PMID: 10.1111/nph.1725133533489)
Xu D, Fang H, Liu J, Chen Y, Gu Y, Sun G et al (2022) ChIP-seq assay revealed histone modification H3K9ac involved in heat shock response of the sea cucumber Apostichopus japonicus. Sci Total Environ 820:153168. https://doi.org/10.1016/j.scitotenv.2022.153168. (PMID: 10.1016/j.scitotenv.2022.15316835051475)
Xue R, Li Q, Guo R, Yan H, Ju X, Liao L et al (2023) Rice defense responses orchestrated by oral bacteria of the rice striped stem borer, Chilo suppressalis. Rice 16:1. https://doi.org/10.1186/s12284-022-00617-w. (PMID: 10.1186/s12284-022-00617-w366225039829949)
Yan L, Fan G, Li X (2019) Genome-wide analysis of three histone marks and gene expression in Paulownia fortunei with phytoplasma infection. BMC Genomics 20:234. https://doi.org/10.1186/s12864-019-5609-1. (PMID: 10.1186/s12864-019-5609-1308981126429711)
Yan L, Zhai X, Zhao Z, Fan G (2020) Whole-genome landscape of H3K4me3, H3K36me3 and H3K9ac and their association with gene expression during Paulownia witches’ broom disease infection and recovery processes. 3 Biotech 10:336. https://doi.org/10.1007/s13205-020-02331-0. (PMID: 10.1007/s13205-020-02331-0326707367340717)
Ye W, Bustos-Segura C, Degen T, Erb M, Turlings TCJ (2022) Belowground and aboveground herbivory differentially affect the transcriptome in roots and shoots of maize. Plant Direct. https://doi.org/10.1002/pld3.426. (PMID: 10.1002/pld3.426358985579307387)
Yoshida S (1976) Routine procedure for growing rice plants in culture solution in Laboratory manual for physiological studies of Rice. In: Yoshida S, Forno DA, Cock JH (eds) Los Baños. Philippines, International rice research institute, pp 61–66.
Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R Package for comparing biological themes among gene clusters. OMICS 16:284–287. https://doi.org/10.1089/omi.2011.0118. (PMID: 10.1089/omi.2011.0118224554633339379)
Yu G, Wang LG, He QY (2015) ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31:2382–2383. https://doi.org/10.1093/bioinformatics/btv145. (PMID: 10.1093/bioinformatics/btv14525765347)
Yung W, Wang Q, Huang M, Wong F, Liu A, Ng M et al (2022) Priming-induced alterations in histone modifications modulate transcriptional responses in soybean under salt stress. Plant J 109:1575–1590. https://doi.org/10.1111/tpj.15652. (PMID: 10.1111/tpj.1565234961994)
Zentner GE, Henikoff S (2013) Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20:259–266. https://doi.org/10.1038/nsmb.2470. (PMID: 10.1038/nsmb.247023463310)
Zhan EL, Wang Y, Jiang J, Jia Z-Q, Tang T, Song Z-J et al (2021) Influence of three insecticides targeting GABA receptor on fall armyworm Spodoptera frugiperda: analyses from individual, biochemical and molecular levels. Pestic Biochem Physiol 179:104973. https://doi.org/10.1016/j.pestbp.2021.104973. (PMID: 10.1016/j.pestbp.2021.10497334802523)
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE et al (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137. https://doi.org/10.1186/gb-2008-9-9-r137. (PMID: 10.1186/gb-2008-9-9-r137187989822592715)
Zhang L, Qiu Z, Hu Y, Yang F, Yan S, Zhao L et al (2011) ABA treatment of germinating maize seeds induces VP1 gene expression and selective promoter-associated histone acetylation. Physiol Plant 143:287–296. https://doi.org/10.1111/j.1399-3054.2011.01496.x. (PMID: 10.1111/j.1399-3054.2011.01496.x21679193)
Zhang L, Liu B, Jiang Y, Liu J, Wu K, Xiao Y (2019) Molecular characterization analysis of fall armyworm populations in China. Plant Prot 45:20–27. https://doi.org/10.16688/j.zwbh.2019296. (PMID: 10.16688/j.zwbh.2019296)
Zhang J, Zhang X, Chen R, Yang L, Fan K, Liu Y et al (2020a) Generation of transgene-Free semidwarf maize plants by gene editing of gibberellin-oxidase20-3 using CRISPR/Cas9. Front Plant Sci 11:1048. https://doi.org/10.3389/fpls.2020.01048. (PMID: 10.3389/fpls.2020.01048327422697365143)
Zhang K, Liu Q, Kang H, Liu X, Chen P, Peng Y, Li Y (2020b) Herbivore-induced rice resistance against rice blast mediated by salicylic acid. Insect Sci 27:49–57. https://doi.org/10.1111/1744-7917.12630. (PMID: 10.1111/1744-7917.1263029999564)
Zhang Y, Li Y, Zhang Y, Zhang Z, Zhang D, Wang X et al (2022) Genome-wide H3K9 acetylation level increases with age-dependent senescence of flag leaf in rice. J Exp Bot 73:4696–4715. https://doi.org/10.1093/jxb/erac155. (PMID: 10.1093/jxb/erac15535429161)
Zheng Y, Zhang X, Liu X, Qin N, Xu K, Zeng R et al (2021) Nitrogen supply alters rice defense against the striped stem borer Chilo suppressalis. Front Plant Sci 12:691292. https://doi.org/10.3389/fpls.2021.691292. (PMID: 10.3389/fpls.2021.691292343814798351598)
Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B et al (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648. https://doi.org/10.1111/j.1365-313X.2009.03988.x. (PMID: 10.1111/j.1365-313X.2009.03988.x19656341)
Zhou J, Wang X, He K, Charron JBF, Elling AA, Deng XW (2010) Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression. Plant Mol Biol 72:585–595. https://doi.org/10.1007/s11103-009-9594-7. (PMID: 10.1007/s11103-009-9594-720054610)
Zhou G, Wang X, Yan F, Wang X, Li R, Cheng J et al (2011) Genome-wide transcriptional changes and defence-related chemical profiling of rice in response to infestation by the rice striped stem borer Chilo suppressalis. Physiol Plant 143:21–40. https://doi.org/10.1111/j.1399-3054.2011.01483.x. (PMID: 10.1111/j.1399-3054.2011.01483.x21534978)
Zhuang Y, Wang X, Llorca LC, Lu J, Lou Y, Li R (2022) Role of jasmonate signaling in rice resistance to the leaf folder Cnaphalocrocis medinalis. Plant Mol Biol 109:627–637. https://doi.org/10.1007/s11103-021-01208-x. (PMID: 10.1007/s11103-021-01208-x34709485)

32171512 National Natural Science Foundation of China; 31701855 National Natural Science Foundation of China; 2022J01130 Natural Science Foundation of Fujian Province; 2020J02030 Natural Science Foundation of Fujian Province; 2019M652237 China Postdoctoral Science Foundation Fellowship; 2020T130099 China Postdoctoral Science Foundation Fellowship; KFb22004XA the Science and Technology Innovation Special foundation of Fujian Agriculture and Forestry University

Keywords: CUT&Tag; H3K9ac; JA signaling; Phenolamide; RNA-seq; Rice; Spodoptera frugiperda

6RI5N05OWW (jasmonic acid)
0 (Histones)
0 (Cyclopentanes)
0 (Oxylipins)

Date Created: 20240223 Date Completed: 20240226 Latest Revision: 20240312

20240312

10.1007/s00299-024-03160-8

38393406