Abstract
Sugarcane, the commercial sugar-yielding crop, frequently suffers serious damage by trunk borers. The neonicotinoid insecticide imidacloprid is often used for disturbing insect nervous system to defense pests, while the molecular regulation of plant response controlling the imidacloprid is still unclear. Here, using the RNA-seq method, we detected the transcription level of sugarcane roots under the imidacloprid treatment for 24 h and 48 h, respectively. Results showed that a total of 1544 and 966 differentially expressed genes (DEGs) were detected under 24 h (1045 up-regulated and 499 down-regulated) and 48 h imidacloprid treatment (539 up-regulated and 427 down-regulated), respectively. Then the accuracy of RNA-seq data was verified by qRT-PCR assay, and a significant positive correlation between RNA-seq data and qRT-PCR results was detected. Crucial genes encoding the peroxidase (Sspon.03G0025980-4P, Sspon.08G0008080-2B) and the ZIM TFs (Sspon.01G0017230-1A, Sspon.01G0042730-3D) were prominently up-regulated in the 24 h treatment, while genes encoding nitrite reductase (Sspon.04G0002730-1A, Sspon.04G0002730-3D) were significantly down-regulated in the 24 h stress. In all, our results not only provide a whole expression analysis of imidacloprid on sugarcane but also are helpful in exploring crucial genes related to plant response on imidacloprid.
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References
Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsch ER, Colin ME (2005) Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 53:5336–5341. https://doi.org/10.1021/jf0479362
Bowling RD, Brewer MJ, Kerns DL, Gordy J, Seiter N, Elliott NE, Buntin GD, Way MO, Royer TA, Biles S, Maxson E (2016) Sugarcane Aphid (Hemiptera: Aphididae): A new pest on sorghum in North America J Integr Pest Manag 7 https://doi.org/10.1093/jipm/pmw011
Castle SJ, Byrne FJ, Jian LB, Toscano NC (2005) Spatial and temporal distribution of imidacloprid and thiamethoxam in citrus and impact on Homalodisca coagulata populations. Pest Manag Sci 61:75–84
Cataneo AC, Ferreira LC, Carvalho JC, Andreo-Souza Y, Corniani N, Mischan MM, Nunes JC (2010) Improved germination of soybean seed treated with thiamethoxam under drought conditions. Seed Sci Technol 38:248–251. https://doi.org/10.15258/sst.2010.38.1.27
Chung HS, Howe GA (2009) A critical role for the TIFY Motif in repression of Jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-Domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145. https://doi.org/10.1105/tpc.108.064097
Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-Domain genes in response to wounding and herbivory. Plant Physiol 146:952–964. https://doi.org/10.1104/pp.107.115691
Cipollini D, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653. https://doi.org/10.1111/j.1365-294X.2004.02161.x
Ding P, Ding Y (2020) Stories of salicylic acid: A plant defense hormone. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2020.01.004
Ebel RC, Wallace B, Elkins C (2000) Phytotoxicity of the systemic insecticide imidacloprid on tomato and cucumber in the greenhouse. Hort Technology 10:144–146
Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105. https://doi.org/10.1002/ps.1616
Ford CR, Vose JM, Daley M et al (2007) Use of water by eastern hemlock: Implications for systemic insecticide application. Arboric Urban For 33(6):421–427
Ford KA, Casida JE, Chandran D, Gulevich AG, Okrent RA, Durkin KA, Sarpong R, Bunnelle EM, Wildermuth MC (2010) Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proc Natl Acad Sci USA 107:17527–17532. https://doi.org/10.1073/pnas.1013020107
Francini A, Giro A, Ferrante A (2019) Chapter 11 - Biochemical and molecular regulation of phenylpropanoids pathway under abiotic stresses. In: MIR Khan, PS Reddy, A Ferrante, NA Khan (eds) Plant Signaling Molecules. Wood head Publishing.
Francis MI, Redondo A, Burns JK, Graham JH (2009) Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker. Eur J Plant Pathol 124:283–292. https://doi.org/10.1007/s10658-008-9415-x
Fu J, Zhao H, An Y, Lu Y, Chen L, Dai S, Gong H, Sun D (2019) Spatial, temporal distribution and efficacy of immidacloprid via drip irrigation in sugarcane and soil applied in South China. Fresenius Environ Bull 28:8540–8547
Jeschke P, Nauen R, Beck ME (2013) Nicotinic acetylcholine receptor agonists: A milestone for modern crop protection. Angewandte Chemie-International Edition 52:9464–9485. https://doi.org/10.1002/anie.201302550
Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908. https://doi.org/10.1021/jf101303g
Kanehisa M, Araki M, Goto S et al (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484
Kaur N, Sohal BS, Singh K (2011) Biochemical and physiological changes on Bacillus thuringiensis cotton after imidacloprid foliar spray. Pestic Biochem Phys 99:280–284. https://doi.org/10.1016/j.pestbp.2011.01.007
Kostyn K, Czemplik M, Kulma A, Bortniczuk M, Skala J, Szopa J (2012) Genes of phenylpropanoid pathway are activated in early response to Fusarium attack in flax plants. Plant Sci 190:103–115. https://doi.org/10.1016/j.plantsci.2012.03.011
Larsen RJ, Falk DE (2013) Effects of a seed treatment with a neonicotinoid insecticide on germination and freezing tolerance of spring wheat seedlings. Can J Plant Sci 93:535–540. https://doi.org/10.4141/cjps2012-127
Laurent FM, Rathahao E (2003) Distribution of C-14 imidacloprid in sunflowers (Helianthus annuus L.) following seed treatment. J Agric Food Chem 51:8005–8010. https://doi.org/10.1021/jf034310n
Li WF, Yin J, Huang YK, Shen K, Luo ZM, Wang XY, Shan HL (2014) The dynamics of population structure and control strategies of sugarcane borers in Yunnan. J Agric 4(8):35–38
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402
Matimati I, Verboom GA, Cramer MD (2014) Nitrogen regulation of transpiration controls mass-flow acquisition of nutrients. J Exp Bot 65(1):159–168
Ngadze E, Icishahayo D, Coutinho T, Waals JE (2012) Role of polyphenol oxidase, peroxidase, phenylalanine ammonia lyase, chlorogenic acid, and ttotal soluble phenols in resistance of potatoes to soft rot. Plant Dis 96:186–192. https://doi.org/10.1094/PDIS-02-11-0149
Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M, Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van der Sluijs JP, Van Dyck H, Wiemers M (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102. https://doi.org/10.1007/s11356-014-3471-x
Raupp MJ (2004) Incidence, abundance, and severity of mites on hemlocks following applications of imidacloprid. J Arboric v. 30: pp. 108–100–2004 v.2030 no.2002.
Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biol Med 20:933–956. https://doi.org/10.1016/0891-5849(95)02227-9
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140
Ruckert A, Allen LN, Ramirez RA (2018) Combinations of plant water-stress and neonicotinoids can lead to secondary outbreaks of Banks grass mite (Oligonychus pratensis Banks) PLoS One 13 https://doi.org/10.1371/journal.pone.0191536
Sharma A, Kumar V, Kanwar MK, Thukral AK, Bhardwaj R (2017a) Ameliorating imidacloprid induced oxidative stress by 24-epibrassinolide in Brassica juncea L. Russ J Plant Physiol 64:509–517. https://doi.org/10.1134/s1021443717040124
Sharma A, Thakur S, Kumar V et al (2017b) 24-epibrassinolide stimulates imidacloprid detoxification by modulating the gene expression of Brassica juncea L. BMC Plant Biol 17(1):1–10
Singh J, Singh DK (2005) Available nitrogen and arginine deaminase activity in groundnut (Arachis hypogaea L.) fields after imidacloprid, diazinon, and lindane treatments. J Agric Food Chem 53:363–368. https://doi.org/10.1021/jf048476f
Singh J, Singh DK (2006) Ammonium, nitrate and nitrite nitrogen and nitrate reductase enzyme activity in groundnut (Arachis hypogaea L.) Fields after diazinon, imidacloprid and lindane treatments. J Environ Sci Health B 41:1305–1318. https://doi.org/10.1080/03601230600963938
Smith JF, Catchot AL, Musser FR, Gore J (2013) Effects of aldicarb and neonicotinoid seed treatments on twospotted spider mite on cotton. J Econ Entomol 2.
Stamm MD, Enders LS, Donze-Reiner TJ, Baxendale FP, Siegfried BD, Heng-Moss TM (2014) Transcriptional response of soybean to thiamethoxam seed treatment in the presence and absence of drought stress BMC Genomics 15 https://doi.org/10.1186/1471-2164-15-1055
Sun D, Fu J, Lu Y, Chen L, Gong H, Zhao H, Dai S, An Y, Xu H (2017) Absorption, transportation and distribution of imidacloprid in maize. Int J Environ Anal Chem 97:783–795. https://doi.org/10.1080/03067319.2017.1337110
Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD (2013) Neonicotinoid Insecticides Alter Induced Defenses and Increase Susceptibility to Spider Mites in Distantly Related Crop Plants PLoS One 8 https://doi.org/10.1371/journal.pone.0062620
Tanis SR, Cregg BM, Mota-Sanchez D, McCullough DG, Poland TM (2012) Spatial and temporal distribution of trunk-injected 14C-imidacloprid in Fraxinus trees. Pest Manag Sci 68:529–536. https://doi.org/10.1002/ps.2281
Turcotte RM, Lagalante A, Jones J, et al (2017) Spatial and temporal distribution of imidacloprid within the crown of eastern hemlock. J Insect Sci 17(1).
Vranová E, Atichartpongkul S, Villarroel R, Van Montagu M, Inzé D, Van Camp W (2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc Natl Acad Sci 99:10870–10875. https://doi.org/10.1073/pnas.152337999
Wang XY, Li WF, Huang YK et al (2010) Occurrence characteristics and control measures of sugarcane seed-borne disease [J]. Sugar Crops of China 2:45–48
Wulff JA, Kiani M, Regan K, Eubanks MD, Szczepaniec A (2019) Neonicotinoid insecticides alter the transcriptome of soybean and decrease plant resistance Int J Mol Sci 20 https://doi.org/10.3390/ijms20030783
Yu YS, Xue S, Wu JC et al (2014) Distribution of imidacloprid residues in different parts of rice plants and its effect on larvae and adult females of Chilo suppressalis (Lepidoptera: Pyralidae). J Econ Entomol 100(2):375–380
Zhang J, Zhang X, Tang H, Zhang Q et al (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet 50:1565–1573. https://doi.org/10.1038/s41588-018-0237-2
Zhang RY, Shan HL, Li WF, Cang XY, Wang XY, Yin J, Luo ZM, Huang YK (2017) First report of sugarcane leaf scald caused by Xandzomonas albilineans in the province of Guangxi, China. Plant Dis 101:1541–1542. https://doi.org/10.1094/pdis-12-16-1774-pdn
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This work was supported by the GDAS' Project of Science and Technology Development (2019GDASYL-0103032).
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Shi, F., Lu, Y., Sun, D. et al. Imidacloprid Triggers Transcriptomic Changes in Sugarcane (Saccharum officinarum). Tropical Plant Biol. 14, 203–212 (2021). https://doi.org/10.1007/s12042-021-09284-5
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DOI: https://doi.org/10.1007/s12042-021-09284-5