{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T10:49:02Z","timestamp":1778842142681,"version":"3.51.4"},"reference-count":97,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2021,10,2]],"date-time":"2021-10-02T00:00:00Z","timestamp":1633132800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"This work was supported by the Cooperative Research Program for Agriculture Science &amp; Technology Development:","award":["Project No. PJ01579401"],"award-info":[{"award-number":["Project No. PJ01579401"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The green rice leafhopper (GRH, Nephotettix cincticeps Uhler) is one of the most important insect pests causing serious damage to rice production and yield loss in East Asia. Prior to performing RNA-Seq analysis, we conducted an electrical penetration graph (EPG) test to investigate the feeding behavior of GRH on Ilpum (recurrent parent, GRH-susceptible cultivar), a near-isogenic line (NIL carrying Grh1) compared to the Grh1 donor parent (Shingwang). Then, we conducted a transcriptome-wide analysis of GRH-responsive genes in Ilpum and NIL, which was followed by the validation of RNA-Seq data by qPCR. On the one hand, EPG results showed differential feeding behaviors of GRH between Ilpum and NIL. The phloem-like feeding pattern was detected in Ilpum, whereas the EPG test indicated a xylem-like feeding habit of GRH on NIL. In addition, we observed a high death rate of GRH on NIL (92%) compared to Ilpum (28%) 72 h post infestation, attributed to GRH failure to suck the phloem sap of NIL. On the other hand, RNA-Seq data revealed that Ilpum and NIL GRH-treated plants generated 1,766,347 and 3,676,765 counts per million mapped (CPM) reads, respectively. The alignment of reads indicated that more than 75% of reads were mapped to the reference genome, and 8859 genes and 15,815,400 transcripts were obtained. Of this number, 3424 differentially expressed genes (DEGs, 1605 upregulated in Ilpum and downregulated in NIL; 1819 genes upregulated in NIL and downregulated in Ilpum) were identified. According to the quantile normalization of the fragments per kilobase of transcript per million mapped reads (FPKM) values, followed by the Student\u2019s t-test (p &lt; 0.05), we identified 3283 DEGs in Ilpum (1935 upregulated and 1348 downregulated) and 2599 DEGs in NIL (1621 upregulated and 978 downregulated) with at least a log2 (logarithm base 2) twofold change (Log2FC \u22652) in the expression level upon GRH infestation. Upregulated genes in NIL exceeded by 13.3% those recorded in Ilpum. The majority of genes associated with the metabolism of carbohydrates, amino acids, lipids, nucleotides, the activity of coenzymes, the action of phytohormones, protein modification, homeostasis, the transport of solutes, and the uptake of nutrients, among others, were abundantly upregulated in NIL (carrying Grh1). However, a high number of upregulated genes involved in photosynthesis, cellular respiration, secondary metabolism, redox homeostasis, protein biosynthesis, protein translocation, and external stimuli response related genes were found in Ilpum. Therefore, all data suggest that Grh1-mediated resistance against GRH in rice would involve a transcriptome-wide reprogramming, resulting in the activation of bZIP, MYB, NAC, bHLH, WRKY, and GRAS transcription factors, coupled with the induction of the pathogen-pattern triggered immunity (PTI), systemic acquired resistance (SAR), symbiotic signaling pathway, and the activation of genes associated with the response mechanisms against viruses. This comprehensive transcriptome profile of GRH-responsive genes gives new insights into the molecular response mechanisms underlying GRH (insect pest)\u2013rice (plant) interaction.<\/jats:p>","DOI":"10.3390\/ijms221910696","type":"journal-article","created":{"date-parts":[[2021,10,4]],"date-time":"2021-10-04T09:24:15Z","timestamp":1633339455000},"page":"10696","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["RNA-Seq and Electrical Penetration Graph Revealed the Role of Grh1-Mediated Activation of Defense Mechanisms towards Green Rice Leafhopper (Nephotettix cincticeps Uhler) Resistance in Rice (Oryza sativa L.)"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1104-985X","authenticated-orcid":false,"given":"Youngho","family":"Kwon","sequence":"first","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4918-7369","authenticated-orcid":false,"given":"Nkulu Rolly","family":"Kabange","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ji-Yoon","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bo Yoon","family":"Seo","sequence":"additional","affiliation":[{"name":"Crop Protection Division, National Institute of Agricultural Science, RDA, Jeonju 55365, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2874-0575","authenticated-orcid":false,"given":"Dongjin","family":"Shin","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"So-Myeong","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jin-Kyung","family":"Cha","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jun-Hyeon","family":"Cho","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ju-Won","family":"Kang","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3386-5719","authenticated-orcid":false,"given":"Dong-Soo","family":"Park","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jong-Min","family":"Ko","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5750-112X","authenticated-orcid":false,"given":"Jong-Hee","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Southern Area Crop Science, National Institute of Crop Science, RDA, Miryang 50424, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Tang, Y., Bao, X., Zhi, Y., Wu, Q., Guo, Y., Yin, X., Zeng, L., Li, J., Zhang, J., and He, W. (2019). Overexpression of a MYB family gene, OsMYB6, increases drought and salinity stress tolerance in transgenic rice. Front. Plant Sci., 10.","DOI":"10.3389\/fpls.2019.00168"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1007\/s12298-017-0477-0","article-title":"Comprehensive physiological analyses and reactive oxygen species profiling in drought tolerant rice genotypes under salinity stress","volume":"23","author":"Basu","year":"2017","journal-title":"Physiol. Mol. Biol. Plants"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Alford, D.V. (2019). Beneficial Insects, CRC Press.","DOI":"10.1201\/9780429161940"},{"key":"ref_4","unstructured":"Van Huis, A., Van Itterbeeck, J., Klunder, H., Mertens, E., Halloran, A., Muir, G., and Vantomme, P. (2013). Edible Insects: Future Prospects for Food and Feed Security, Food and Agriculture Organization of the United Nations."},{"key":"ref_5","unstructured":"Pathak, M.D., and Khan, Z.R. (1994). Insect Pests of Rice, International Rice Research Institute."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms12986","article-title":"Massive yet grossly underestimated global costs of invasive insects","volume":"7","author":"Bradshaw","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_7","unstructured":"UN Department of Economic and Social Affairs (2019). World Population Projected to Reach 9.8 Billion in 2050, and 11.2 Billion in 2100, UN Department of Economic and Social Affairs."},{"key":"ref_8","unstructured":"Brar, D., Virk, P., Jena, K., and Khush, G. (2009). Breeding for Resistance to Planthoppers in Rice, International Rice Research Institute."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1017\/S0007485300040438","article-title":"Revision of the genus Nephotettix Matsumura (Homoptera: Cicadelloidea Euscelidae) based on the type material","volume":"60","author":"Ghauri","year":"1971","journal-title":"Bull. Entomol. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1303\/aez.13.264","article-title":"Zoology. Transmission efficiency of rice waika virus by the green rice leafhoppers, Nephotettix spp. (Hemiptera: Cicadellidae)","volume":"13","author":"Hirao","year":"1978","journal-title":"Appl. Entomol. Zool."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1303\/aez.14.123","article-title":"Zoology. Transmission Efficiency of Rice Transitory Yellowing Virus by teh Green Rice Leafhoppers, Nephotetlix spp. (Hemiptera: Cicadellidae)","volume":"14","author":"Inoue","year":"1979","journal-title":"Appl. Entomol. Zool."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3570","DOI":"10.1128\/aem.57.12.3570-3575.1991","article-title":"Cloning and detection of chromosomal and extrachromosomal DNA from mycoplasmalike organisms that cause yellow dwarf disease of rice","volume":"57","author":"Nakashima","year":"1991","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1007\/s00122-006-0270-x","article-title":"Molecular mapping of a novel gene, Grh5, conferring resistance to green rice leafhopper (Nephotettix cincticeps Uhler) in rice, Oryza sativa L.","volume":"113","author":"Fujita","year":"2006","journal-title":"Theor. Appl. Genet."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1023\/A:1009633816713","article-title":"Rice plant (Oryza sativa L.) containing rice tungro spherical virus (RTSV) coat protein transgenes are resistant to virus infection","volume":"5","author":"Sivamani","year":"1999","journal-title":"Mol. Breed."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.jinsphys.2014.10.010","article-title":"Transcriptome analysis of the salivary glands of Nephotettix cincticeps (Uhler)","volume":"71","author":"Matsumoto","year":"2014","journal-title":"J. Insect Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1303\/aez.2.195","article-title":"Studies on the salivary glands of rice plant leafhoppers: II. Origins of the structural precursors of the sheath material","volume":"2","author":"SoGAWA","year":"1967","journal-title":"Appl. Entomol. Zool."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/s13355-013-0210-6","article-title":"Purification of \u03b2-glucosidase from the salivary glands of the green rice leafhopper, Nephotettix cincticeps (Uhler) (Hemiptera: Cicadellidae), and its detection in the salivary sheath","volume":"48","author":"Nakamura","year":"2013","journal-title":"Appl. Entomol. Zool."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1303\/jjaez.11.50","article-title":"Studies on the feeding behavior of green rice leafhopper, Nephotettix cincticeps UHLER. I. Insertion of the stylets into host plant","volume":"11","author":"Naito","year":"1967","journal-title":"Jap. J. Appl. Ent. Zool"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev-genet-102209-163500","article-title":"New insights into plant responses to the attack from insect herbivores","volume":"44","author":"Wu","year":"2010","journal-title":"Annu. Rev. Genet."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1007\/s11738-009-0449-2","article-title":"Biochemical and enzymatic changes in rice plants as a mechanism of defense","volume":"32","author":"Rani","year":"2010","journal-title":"Acta Physiol. Plant."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12870-019-2116-0","article-title":"Rice defense responses are induced upon leaf rolling by an insect herbivore","volume":"19","author":"Shi","year":"2019","journal-title":"BMC Plant Biol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Wang, Y., Liu, Q., Du, L., Hallerman, E.M., and Li, Y. (2020). Transcriptomic and Metabolomic Responses of Rice Plants to Cnaphalocrocis medinalis Caterpillar Infestation. Insects, 11.","DOI":"10.3390\/insects11100705"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1270\/jsbbs.60.18","article-title":"Development of near-isogenic lines and pyramided lines carrying resistance genes to green rice leafhopper (Nephotettix cincticeps Uhler) with the Taichung 65 genetic background in rice (Oryza sativa L.)","volume":"60","author":"Fujita","year":"2010","journal-title":"Breed. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1016\/S2095-3119(15)61165-0","article-title":"Pyramiding blast, bacterial blight and brown planthopper resistance genes in rice restorer lines","volume":"15","author":"Ji","year":"2016","journal-title":"J. Integ. Agric."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1270\/jsbbs.49.11","article-title":"Mapping of the Grh1 locus for Green Rice Leahopper Resistance in Rice Using RFLP Markers","volume":"49","author":"Tamura","year":"1999","journal-title":"Breed. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1270\/jsbbs.60.336","article-title":"A major QTL for resistance to green rice leafhopper (Nephotettix cincticeps Uhler) derived from African rice (Oryza glaberrima Steud.)","volume":"60","author":"Fujita","year":"2010","journal-title":"Breed. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2069","DOI":"10.1104\/pp.15.01625","article-title":"RNA-Seq links the transcription factors AINTEGUMENTA and AINTEGUMENTA-LIKE6 to cell wall remodeling and plant defense pathways","volume":"171","author":"Krizek","year":"2016","journal-title":"Plant Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-15-972","article-title":"RNA-Seq reveals a xenobiotic stress response in the soybean aphid, Aphis glycines, when fed aphid-resistant soybean","volume":"15","author":"Bansal","year":"2014","journal-title":"BMC Genom."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2793","DOI":"10.1002\/ps.5066","article-title":"RNA-Seq identification of candidate defense genes targeted by endophytic Bacillus cereus-mediated induced systemic resistance against Meloidogyne incognita in tomato","volume":"74","author":"Hu","year":"2018","journal-title":"Pest Manag. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Li, Q., Sun, Z., Shi, Q., Wang, R., Xu, C., Wang, H., Song, Y., and Zeng, R. (2019). RNA-seq analyses of midgut and fat body tissues reveal the molecular mechanism underlying Spodoptera litura resistance to tomatine. Front. Physiol., 10.","DOI":"10.3389\/fphys.2019.00008"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-14-340","article-title":"Insights into organ-specific pathogen defense responses in plants: RNA-seq analysis of potato tuber-Phytophthora infestans interactions","volume":"14","author":"Gao","year":"2013","journal-title":"BMC Genom."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Menuz, K., Larter, N.K., Park, J., and Carlson, J.R. (2014). An RNA-seq screen of the Drosophila antenna identifies a transporter necessary for ammonia detection. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004810"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1007\/s11032-013-9896-y","article-title":"Fine mapping of Grh1, a major gene associated with antibiosis to green rice leafhopper in rice","volume":"32","author":"Park","year":"2013","journal-title":"Mol. Breed."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Mustafa, T., Horton, D.R., Cooper, W.R., Swisher, K.D., Zack, R.S., Pappu, H.R., and Munyaneza, J.E. (2015). Use of electrical penetration graph technology to examine transmission of \u2018Candidatus Liberibacter solanacearum\u2019to potato by three haplotypes of potato psyllid (Bactericera cockerelli; Hemiptera: Triozidae). PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0138946"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1002\/ps.2098","article-title":"Electrical penetration graph evidence that pymetrozine toxicity to the rice brown planthopper is by inhibition of phloem feeding","volume":"67","author":"He","year":"2011","journal-title":"Pest Manag. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Rafalski, J.A., Vogel, J.M., Morgante, M., Powell, W., Andre, C., and Tingey, S.V. (1996). Generating and using DNA markers in plants. Nonmammalian Genomic Analysis, Elsevier.","DOI":"10.1016\/B978-012101285-4\/50005-9"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1104\/pp.20.00433","article-title":"Plant secondary metabolites as defenses, regulators, and primary metabolites: The blurred functional trichotomy","volume":"184","author":"Erb","year":"2020","journal-title":"Plant Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Nishad, R., Ahmed, T., Rahman, V.J., and Kareem, A. (2020). Modulation of Plant Defense System in Response to Microbial Interactions. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.01298"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3178","DOI":"10.3390\/ijms14023178","article-title":"Activation of defense mechanisms against pathogens in mosses and flowering plants","volume":"14","author":"Montesano","year":"2013","journal-title":"Int. J. Mol. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1093\/jxb\/eru480","article-title":"Role of early signalling events in plant\u2013insect interactions","volume":"66","author":"Zebelo","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1111\/j.1467-7652.2007.00243.x","article-title":"Functional analysis of rice NPR1-like genes reveals that OsNPR1\/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility","volume":"5","author":"Yuan","year":"2007","journal-title":"Plant Biotechnol. J."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1094\/MPMI-18-0511","article-title":"Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light","volume":"18","author":"Chern","year":"2005","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-15-461","article-title":"Interaction specificity and coexpression of rice NPR1 homologs 1 and 3 (NH1 and NH3), TGA transcription factors and Negative Regulator of Resistance (NRR) proteins","volume":"15","author":"Chern","year":"2014","journal-title":"BMC Genom."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Rolly, N.K., Imran, Q.M., Lee, I.-J., and Yun, B.-W.J. (2020). Salinity stress-mediated suppression of expression of salt overly sensitive signaling pathway genes suggests negative regulation by AtbZIP62 transcription factor in Arabidopsis thaliana. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21051726"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Rolly, N.K., Mun, B.-G., and Yun, B.-W. (2021). Insights into the Transcriptional Regulation of Branching Hormonal Signaling Pathways Genes under Drought Stress in Arabidopsis. Genes, 12.","DOI":"10.3390\/genes12020298"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Xu, Z., Jiang, Y., and Zhou, G. (2015). Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front. Plant Sci., 6.","DOI":"10.3389\/fpls.2015.00701"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Lu, Y., and Yao, J. (2018). Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19123900"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1094\/MPMI-22-5-0487","article-title":"Primary metabolism and plant defense\u2014Fuel for the fire","volume":"22","author":"Bolton","year":"2009","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_49","first-page":"791","article-title":"Connecting photosynthesis and cellular respiration: Preservice teachers\u2019 conceptions","volume":"46","author":"Brown","year":"2009","journal-title":"J. Res. Sci. Teach. Off. J. Natl. Assoc. Res. Sci. Teach."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1111\/j.1469-8137.1994.tb02968.x","article-title":"Secondary metabolites in plant defence mechanisms","volume":"127","author":"Bennett","year":"1994","journal-title":"New Phytol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/nph.15597","article-title":"DNA damage and reactive oxygen species cause cell death in the rice local lesions 1 mutant under high light and high temperature","volume":"222","author":"Qiu","year":"2019","journal-title":"New Phytol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1104\/pp.114.255737","article-title":"MRG702, a reader protein of H3K4me3 and H3K36me3, is involved in brassinosteroid-regulated growth and flowering time control in rice","volume":"168","author":"Jin","year":"2015","journal-title":"Plant Physiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1563","DOI":"10.1007\/s00709-015-0791-8","article-title":"Stress-induced Oryza sativa BAT1 dual helicase exhibits unique bipolar translocation","volume":"252","author":"Tuteja","year":"2015","journal-title":"Protoplasma"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Wang, F., Liu, J., Chen, M., Zhou, L., Li, Z., Zhao, Q., Pan, G., Zaidi, S.-H.-R., and Cheng, F. (2016). Involvement of abscisic acid in PSII photodamage and D1 protein turnover for light-induced premature senescence of rice flag leaves. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0161203"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2673","DOI":"10.1093\/jxb\/eri260","article-title":"Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses","volume":"56","author":"Luo","year":"2005","journal-title":"J. Exp. Bot."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1055\/s-2005-865851","article-title":"Up-regulation of OsBIHD1, a rice gene encoding BELL homeodomain transcriptional factor, in disease resistance responses","volume":"7","author":"Luo","year":"2005","journal-title":"Plant Biol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Liu, H., Dong, S., Gu, F., Liu, W., Yang, G., Huang, M., Xiao, W., Liu, Y., Guo, T., and Wang, H. (2017). NBS-LRR protein Pik-H4 interacts with OsBIHD1 to balance rice blast resistance and growth by coordinating ethylene-brassinosteroid pathway. Front. Plant Sci., 8.","DOI":"10.3389\/fpls.2017.00127"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1080\/1085566031000141162","article-title":"cDNA cloning and expression analysis of the rice (Oryza sativa L.) RNase L inhibitor","volume":"14","author":"Du","year":"2003","journal-title":"DNA Seq."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/0005-2728(95)00032-E","article-title":"The genomic organization of the gene encoding a nitrate-inducible ferredoxin-NADP+ oxidoreductase from rice roots","volume":"1229","author":"Aoki","year":"1995","journal-title":"Biochim. Biophys. Acta Bioenerg."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1002\/ps.1906","article-title":"Jasmonic acid induces resistance to economically important insect pests in winter wheat","volume":"66","author":"Volkmar","year":"2010","journal-title":"Pest Manag. Sci. Former. Pestic. Sci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.pestbp.2009.07.001","article-title":"Effects of jasmonic acid-induced resistance in rice on the plant brownhopper, Nilaparvata lugens St\u00e5l (Homoptera: Delphacidae)","volume":"95","author":"Kalaivani","year":"2009","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1406","DOI":"10.1094\/MPMI-20-11-1406","article-title":"Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis","volume":"20","author":"Bodenhausen","year":"2007","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_63","unstructured":"Dicke, M., and Van Poecke, R. (2002). Signalling in plant-insect interactions: Signal transduction in direct and indirect plant defence. Plant Signal Transduction, Oxford University Press."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1046\/j.1364-3703.2000.00009.x","article-title":"Plant signalling and induced defence in insect attack","volume":"1","author":"Chamberlain","year":"2000","journal-title":"Mol. Plant Pathol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1111\/nph.17251","article-title":"Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore","volume":"230","author":"Xu","year":"2021","journal-title":"New Phytol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11032-020-1103-3","article-title":"Current understanding of the genomic, genetic, and molecular control of insect resistance in rice","volume":"40","author":"Du","year":"2020","journal-title":"Mol. Breed."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"2827","DOI":"10.1093\/jxb\/erv099","article-title":"ROS and RNS in plant physiology: An overview","volume":"66","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Bardaweel, S.K., Gul, M., Alzweiri, M., Ishaqat, A., ALSalamat, H.A., and Bashatwah, R.M. (2018). Reactive oxygen species: The dual role in physiological and pathological conditions of the human body. Eurasian J. Med., 50.","DOI":"10.5152\/eurasianjmed.2018.17397"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.1016\/j.tplants.2020.08.001","article-title":"Fine-Tuning of RBOH-Mediated ROS Signaling in Plant Immunity","volume":"25","author":"Wang","year":"2020","journal-title":"Trends Plant Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1093\/jxb\/erv558","article-title":"The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity","volume":"67","author":"Morales","year":"2016","journal-title":"J. Exp. Bot."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.niox.2010.12.008","article-title":"Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity","volume":"25","author":"Yoshioka","year":"2011","journal-title":"Nitric Oxide"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1105\/tpc.16.00976","article-title":"An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions","volume":"29","author":"Yamauchi","year":"2017","journal-title":"Plant Cell"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"4022","DOI":"10.1105\/tpc.107.055624","article-title":"Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension","volume":"19","author":"Wong","year":"2007","journal-title":"Plant Cell"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Das, K., and Roychoudhury, A. (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci., 2.","DOI":"10.3389\/fenvs.2014.00053"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Sharma, P., Jha, A.B., Dubey, R.S., and Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot., 2012.","DOI":"10.1155\/2012\/217037"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.1016\/j.bbagen.2008.06.003","article-title":"Glutaredoxin systems","volume":"1780","author":"Lillig","year":"2008","journal-title":"Biochim. Biophys. Acta Gen. Subj."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1089\/ars.2000.2.4-811","article-title":"Antioxidant function of thioredoxin and glutaredoxin systems","volume":"2","author":"Holmgren","year":"2000","journal-title":"Antioxid. Redox Signal."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1089\/ars.2005.7.919","article-title":"Identification of plant glutaredoxin targets","volume":"7","author":"Rouhier","year":"2005","journal-title":"Antioxid. Redox Signal."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/BF02857783","article-title":"The role of superoxide dismutase in combating oxidative stress in higher plants","volume":"66","author":"Raychaudhuri","year":"2000","journal-title":"Bot. Rev."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1146\/annurev.pp.43.060192.000503","article-title":"Superoxide dismutase and stress tolerance","volume":"43","author":"Bowler","year":"1992","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_81","first-page":"17","article-title":"Larval development of the green rice leafhopper, Nephotettix cincticeps Uhler, and the white back planthopper, Sogatella furcifera Horvath, on japonica and indica rice varieties","volume":"8","author":"Inoue","year":"1966","journal-title":"Jpn. J. Appl. Entomol. Zool. Chugoku Branch"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1303\/jjaez.22.3_169","article-title":"Zoology. Insect resistance of the rice plant to the green rice leafhopper Nephotettix cincticeps Uhler, 1: Laboratory technique for testing the antibiosis","volume":"22","author":"Ando","year":"1978","journal-title":"Jpn. J. Appl. Entomol. Zool."},{"key":"ref_83","first-page":"175","article-title":"Antixenosis\u2014A new term proposed to define Painter\u2019s \u201cnonpreference\u201d modality of resistance","volume":"24","author":"Kogan","year":"1978","journal-title":"Bull. ESA"},{"key":"ref_84","first-page":"221","article-title":"Resistance of rice varieties against green rice leafhopper, Nephotettix cincticeps Uhler","volume":"5","author":"Koshihara","year":"1971","journal-title":"Trop. Agric. Res. Ser."},{"key":"ref_85","first-page":"115","article-title":"Mechanism of varietal resistance to the rice green leafhopper (Nephotettix cincticeps Uhler)","volume":"19","author":"Abe","year":"1985","journal-title":"Jpn. Agric. Res. Q."},{"key":"ref_86","first-page":"79","article-title":"Biochemical basis of resistance in rice cultivars to brown plant hopper Nilaparvata lugens (Stal.)","volume":"28","author":"Reddy","year":"2004","journal-title":"J. Entomol. Res."},{"key":"ref_87","unstructured":"Heong, K.L., and Hardy, B. (2009). Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia, International Rice Research Institute."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Kabange, N.R., Park, S.-Y., Lee, J.-Y., Shin, D., Lee, S.-M., Kwon, Y., Cha, J.-K., Cho, J.-H., Duyen, D.V., and Ko, J.-M. (2021). New Insights into the Transcriptional Regulation of Genes Involved in the Nitrogen Use Efficiency under Potassium Chlorate in Rice (Oryza sativa L.). Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22042192"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1111\/eea.12621","article-title":"Analysis of tea plant resistance to tea green leafhopper, Empoasca onukii, by detecting stylet-probing behavior with DC electropenetrography","volume":"165","author":"Yorozuya","year":"2017","journal-title":"Entomol. Exp. Appl."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1111\/j.1570-7458.1980.tb02948.x","article-title":"Electronic measurement of probing activities of the green leafhopper of rice","volume":"27","author":"Kawabe","year":"1980","journal-title":"Entomol. Exp. Appl."},{"key":"ref_91","doi-asserted-by":"crossref","unstructured":"Wingett, S.W., and Andrews, S. (2018). FastQ Screen: A tool for multi-genome mapping and quality control. F1000Research, 7.","DOI":"10.12688\/f1000research.15931.2"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1658","DOI":"10.1093\/bioinformatics\/btl158","article-title":"Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences","volume":"22","author":"Li","year":"2006","journal-title":"Bioinformatics"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1093\/bioinformatics\/17.3.282","article-title":"Clustering of highly homologous sequences to reduce the size of large protein databases","volume":"17","author":"Li","year":"2001","journal-title":"Bioinformatics"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"374","DOI":"10.2144\/03342mt01","article-title":"TM4: A free, open-source system for microarray data management and analysis","volume":"34","author":"Saeed","year":"2003","journal-title":"Biotechniques"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Zeeberg, B.R., Feng, W., Wang, G., Wang, M.D., Fojo, A.T., Sunshine, M., Narasimhan, S., Kane, D.W., Reinhold, W.C., and Lababidi, S. (2003). GoMiner: A resource for biological interpretation of genomic and proteomic data. Genome Biol., 4.","DOI":"10.1186\/gb-2003-4-4-r28"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1071\/FP17249","article-title":"S-nitrosocysteine-responsive genes modulate diverse regulatory pathways in Oryza sativa: A transcriptome profiling study","volume":"45","author":"Mun","year":"2018","journal-title":"Funct. Plant Biol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/19\/10696\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:08:48Z","timestamp":1760166528000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/19\/10696"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,2]]},"references-count":97,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2021,10]]}},"alternative-id":["ijms221910696"],"URL":"https:\/\/doi.org\/10.3390\/ijms221910696","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,2]]}}}