Abstract
Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Crambidae) is an economically important pest of rice, Oryza sativa L. (Poaceae), throughout Asia, where damage caused by larvae, particularly during grain-filling stages, significantly increases yield losses. There is, therefore, a pressing need to develop cultivars that are resistant to C. medinalis. In this study, we assessed growth and mortality of first and third instar C. medinalis larvae fed on six rice cultivars that had previously been identified as resistant to the pest, and we quantified production of defense enzymes in plants exposed to herbivory. We found that mortality rates were highest in larvae fed on the resistant cultivars Baiqiaowan, Sasanishiki, Qingliu, and Kasalasu, while relative growth rates were lower for larvae fed on Baiqiaowan and Qingliu. Higher levels of phenylalanine ammonia lyase were expressed in the resistant cultivars. Qingliu plants exposed to herbivory by C. medinalis produced higher levels of jasmonyl isoleucine and salicylic acid (SA) than plants of the susceptible cultivar TN1, and levels of SA in Qingliu plants were intrinsically higher prior to feeding by C. medinalis.
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References
Bhonwong A, Stout MJ, Attajarusit J, Tantasawat P (2009) Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). J Chem Ecol 35:28–38
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cass CL, Peraldi A, Dowd PF, Mottiar Y, Santoro N, Karlen SD, Bukhman YV, Foster CE, Thrower N, Bruno LC (2015) Effects of PHENYLALANINE AMMONIA LYASE (PAL) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium. J Exp Bot 66:4317–4335
Chen M-S (2008) Inducible direct plant defense against insect herbivores. A review. Insect Sci 15:101–114. https://doi.org/10.1111/j.1744-7917.2008.00190.x
Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. PNAS 102:19237–19242. https://doi.org/10.1073/pnas.0509026102
Chen Y-L, Lee C-Y, Cheng K-T, Chang W-H, Huang R-N, Nam HG, Chen Y-R (2014) Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. Plant Cell 26:4135–4148. https://doi.org/10.1105/tpc.114.131185
Cheng C, Wu S (1999) Population dynamics and forecasting of rice leaffolder. Cnaphalocrocis medinalis Guenee in Taiwan. Plant Protect Bull Taipei 41:199–214
Cheng X, Chang C, Dai SM (2010) Responses of striped stem borer, Chilo suppressalis (Lepidoptera: Pyralidae), from Taiwan to a range of insecticides. Pest Manag Sci 66:762–766. https://doi.org/10.1002/ps.1939
Cipollini DF, Redman AM (1999) Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J Chem Ecol 25:271–281
Constabel CP, Ryan CA (1998) A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47:507–511. https://doi.org/10.1016/S0031-9422(97)00539-6
Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: A review. Environ Exp Bot 115:49–57. https://doi.org/10.1016/j.envexpbot.2015.02.010
Diezel C, von Dahl CC, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586. https://doi.org/10.1104/pp.109.139550
Duan C, Yu J, Bai J, Zhu Z, Wang X (2014) Induced defense responses in rice plants against small brown planthopper infestation. Crop J 2:55–62. https://doi.org/10.1016/j.cj.2013.12.001
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259
FAO (2014) FAOSTAT online statistical service. FAO, Rome. http://faostat.fao.org
Farrar RR, Barbour JD, Kennedy GG (1989) Quantifying food consumption and growth in insects. Ann Entomol Soc Am 82:593–598. https://doi.org/10.1093/aesa/82.5.593
Felton GW (2005) Indigestion is a plant’s best defense. PNAS 102:18771–18772. https://doi.org/10.1073/pnas.0509895102
Fraenkel G, Fallil F, Kumarasinghe KS (1981) The feeding behaviour of the rice leaf folder Cnaphalocrocis Medinalis. Entomol Exp Appl 29:147–161. https://doi.org/10.1111/j.1570-7458.1981.tb03054.x
Furstenberg-Hagg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297. https://doi.org/10.3390/ijms140510242
Gulsen O, Eickhoff T, Heng-Moss T, Shearman R, Baxendale F, Sarath G, Lee D (2010) Characterization of peroxidase changes in resistant and susceptible warm-season turfgrasses challenged by Blissus occiduus. Arthropod-Plant Interactions 4:45–55
Han Y, Li P, Gong S, Yang L, Wen L, Hou M (2016) Defense responses in rice induced by silicon amendment against infestation by the leaf folder Cnaphalocrocis medinalis. PLoS ONE 11:e0153918
He J, Chen F, Chen S, Lv G, Deng Y, Fang W, Liu Z, Guan Z, He C (2011) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. J Plant Physiol 168:687–693. https://doi.org/10.1016/j.jplph.2010.10.009
Heinrichs E, Camanag E, Romena A (1985) Evaluation of rice cultivars for resistance to Cnaphalocrocis medinalis Guenee (Lepidoptera: Pyralidae). J Econ Entomol 78:274–278
Huang S-H, Cheng C-H, Wu W-J (2010) Possible impacts of climate change on rice insect pests and management tactics in Taiwan Crop. Environ Bioinform 4: 269–279
Kroes A, Stam JM, David A, Boland W, van Loon JJA, Dicke M, Poelman EH (2016) Plant-mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage. Plant Biol 18:981–991. https://doi.org/10.1111/plb.12490
La Camera S, Gouzerh G, Dhondt S, Hoffmann L, Fritig B, Legrand M, Heitz T (2004) Metabolic reprogramming in plant innate immunity: the contributions of phenylpropanoid and oxylipin pathways. Immunol Rev 198:267–284
Lariviere A, Limeri LB, Meindl GA, Traw MB (2015) Herbivory and relative growth rates of Pieris rapae are correlated with host constitutive salicylic acid and flowering time. J Chem Ecol 41:350–359
Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247. https://doi.org/10.1007/s00425-002-0750-4
Li S-W, Yang H, Liu Y-F, Liao Q-R, Du J, Jin D-C (2012) Transcriptome and gene expression analysis of the rice leaf folder Cnaphalocrosis medinalis. PLoS ONE 7:e47401
Liao C-T, Chen C-L (2017) Oviposition preference and larval performance of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) on rice genotypes. J Econ Entomol 110:1291–1297
Litsinger JA, Bandong JP, Canapi BL, Dela Cruz CG, Pantua PC, Alviola AL, Batay-An EH (2006) Evaluation of action thresholds for chronic rice insect pests in the Philippines. III. Leaffolders. Int J Pest Manag 52:181–194. https://doi.org/10.1080/09670870600664490
Liu J, Du H, Ding X, Zhou Y, Xie P, Wu J (2017) Mechanisms of callose deposition in rice regulated by exogenous abscisic acid and its involvement in rice resistance to Nilaparvata lugens Stål (Hemiptera: Delphacidae) Pest Management. Science 73:2559–2568
Lv M, Kong H, Liu H, Lu Y, Zhang C, Liu J, Ji C, Zhu J, Su J, Gao X (2017) Induction of phenylalanine ammonia-lyase (PAL) in insect damaged and neighboring undamaged cotton and maize seedlings. Int J Pest Manag 63:166–171
Nguyen D, Rieu I, Mariani C, van Dam NM (2016) How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol Biol 91:727–740. https://doi.org/10.1007/s11103-016-0481-8
Punithavalli M, Muthukrishnan N, Rajkuma MB (2013) Defensive responses of rice genotypes for resistance against rice leaffolder Cnaphalocrocis medinalis. Rice Sci 20:363–370
Ramm C, Wachholtz M, Amundsen K, Donze T, Heng-Moss T, Twigg P, Palmer NA, Sarath G, Baxendale F (2015) Transcriptional profiling of resistant and susceptible buffalograsses in response to Blissus occiduus (Hemiptera: Blissidae) feeding. J Econ Entomol 108:1354–1362. https://doi.org/10.1093/jee/tov067
Rani PU, Jyothsna Y (2010) Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiol Plant 32:695–701
Rekha lR, Singh R (2001) Sources and mechanisms of resistance in rice against rice leaffolder Cnaphalocrocis medinalis (Guenee)—a review. Agric Rev 22(1):1–12
Savary S, Willocquet L, Elazegui FA, Castilla NP, Teng PS (2000) Rice pest constraints in tropical asia: quantification of yield losses due to rice pests in a range of production situations. Plant Dis 84:357–369. https://doi.org/10.1094/PDIS.2000.84.3.357
Shivaji R, Camas A, Ankala A, Engelberth J, Tumlinson JH, Williams WP, Wilkinson JR, Luthe DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191
Shono Y, Hirano M (1989) Improved mass-rearing of the rice leaffolder, Cnaphalocrocis medinalis (Guenee) (Lepidoptera: Pyralidae) using corn seedlings. Appl Entomol Zool 24:258–263. https://doi.org/10.1303/aez.24.258
Sinha S, Balasaraswathi R, Selvaraju K, Shanmugasundaram P (2005) Molecular and biochemical markers associated with leaffolder (Cnaphalocrocis medinalis G.) resistance in rice (Oryza sativa L.). Indian J Biochem Biophys 42:228–232
Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer, Berlin
Soffan A, Alghamdi SS, Aldawood AS (2014) Peroxidase and polyphenol oxidase activity in moderate resistant and susceptible Vicia faba induced by Aphis craccivora (Hemiptera: Aphididae) infestation. J Insect Sci 14:285–285. https://doi.org/10.1093/jisesa/ieu147
Tan C-W, Chiang S-Y, Ravuiwasa KT, Yadav J, Hwang S-Y (2012) Jasmonate-induced defenses in tomato against Helicoverpa armigera depend in part on nutrient availability, but artificial induction via methyl jasmonate does not. Arthropod Plant Interactions 6:531–541
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665. http://www.nature.com/nature/journal/v448/n7154/suppinfo/nature05960_S1.html
Tonnessen BW, Manosalva P, Lang JM, Baraoidan M, Bordeos A, Mauleon R, Oard J, Hulbert S, Leung H, Leach JE (2015) Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol Biol 87:273–286. https://doi.org/10.1007/s11103-014-0275-9
Van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FB, Botha AM, Lapitan NL (2010) Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnol J 8:1023–1032
Vlot AC, Klessig DF, Park S-W (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442. https://doi.org/10.1016/j.pbi.2008.05.003
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20
Waldbauer GP (1968) The consumption and utilization of food by insects. In: Beament JWL, Treherne JE, Wigglesworth VB (eds) Advances in insect physiology, vol 5. Academic Press, New York, pp 229–288. https://doi.org/10.1016/S0065-2806(08)60230-1
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
War AR, Paulraj MG, Ignacimuthu S, Sharma HC (2013) Defensive responses in groundnut against chewing and sap-sucking insects. J Plant Growth Regul 32:259–272. https://doi.org/10.1007/s00344-012-9294-4
Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. https://doi.org/10.1146/annurev-genet-102209-163500
Xu J, Wang Q-X, Wu J-C (2010) Resistance of cultivated rice varieties to Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). J Econ Entomol 103:1166–1171
Xu H-X, Zheng X-S, Yang Y-J, Tian J-C, Lu Y-H, Tan K-H, Heong K-L, Lu Z-X (2015) Methyl eugenol bioactivities as a new potential botanical insecticide against major insect pests and their natural enemies on rice (Oriza sativa). Crop Protect 72:144–149. https://doi.org/10.1016/j.cropro.2015.03.017
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
Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, Zhu-Salzman K, Xie J, Cai K, Luo S (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci 110:E3631–E3639
Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858. https://doi.org/10.1104/pp.107.112177
Acknowledgements
We thank the Ministry of Science and Technology, Taiwan, for funding this work (104-2313-B-002-001-MY2, 106-2313-B-002-001, 106-2311-B-002-025 and 107-2311-B-002-018-MY3). We thank Dr. Shu-Jen Wang for providing TN1 seeds, Dr. Chi-Te Liu for providing vacuum equipment, and Dr. Yet-Ran Chen for supporting phytohormone analysis in the Metabolomics Core Facility, Academia Sinica, Taiwan. We are grateful to Dr. Charles Michael Smith for suggestions on how to improve the manuscript and Dr. Shin-Fu Tsai for statistical consultation.
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Guo, TW., Liao, CT. & Chuang, WP. Defensive responses of rice cultivars resistant to Cnaphalocrocis medinalis (Lepidoptera: Crambidae). Arthropod-Plant Interactions 13, 611–620 (2019). https://doi.org/10.1007/s11829-019-09673-4
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DOI: https://doi.org/10.1007/s11829-019-09673-4