Arthropod-Plant Interactions

, Volume 13, Issue 4, pp 611–620 | Cite as

Defensive responses of rice cultivars resistant to Cnaphalocrocis medinalis (Lepidoptera: Crambidae)

  • Tzu-Wei Guo
  • Chung-Ta Liao
  • Wen-Po ChuangEmail author
Original Paper


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.


Larval mortality rate Insect resistant cultivar Qingliu Phytohormone Phenylalanine ammonia lyase 



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.


  1. 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 35:28–38CrossRefPubMedGoogle Scholar
  2. 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 72:248–254CrossRefPubMedGoogle Scholar
  3. 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 66:4317–4335CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chen M-S (2008) Inducible direct plant defense against insect herbivores. A review. Insect Sci 15:101–114. CrossRefGoogle Scholar
  5. 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. CrossRefPubMedGoogle Scholar
  6. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cheng C, Wu S (1999) Population dynamics and forecasting of rice leaffolder. Cnaphalocrocis medinalis Guenee in Taiwan. Plant Protect Bull Taipei 41:199–214Google Scholar
  8. 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. CrossRefPubMedGoogle Scholar
  9. 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 25:271–281CrossRefGoogle Scholar
  10. Constabel CP, Ryan CA (1998) A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47:507–511. CrossRefGoogle Scholar
  11. Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: A review. Environ Exp Bot 115:49–57. CrossRefGoogle Scholar
  12. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259CrossRefPubMedPubMedCentralGoogle Scholar
  15. FAO (2014) FAOSTAT online statistical service. FAO, Rome.
  16. Farrar RR, Barbour JD, Kennedy GG (1989) Quantifying food consumption and growth in insects. Ann Entomol Soc Am 82:593–598. CrossRefGoogle Scholar
  17. Felton GW (2005) Indigestion is a plant’s best defense. PNAS 102:18771–18772. CrossRefPubMedGoogle Scholar
  18. Fraenkel G, Fallil F, Kumarasinghe KS (1981) The feeding behaviour of the rice leaf folder Cnaphalocrocis Medinalis. Entomol Exp Appl 29:147–161. CrossRefGoogle Scholar
  19. Furstenberg-Hagg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 4:45–55CrossRefGoogle Scholar
  21. 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:e0153918CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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. CrossRefPubMedGoogle Scholar
  23. Heinrichs E, Camanag E, Romena A (1985) Evaluation of rice cultivars for resistance to Cnaphalocrocis medinalis Guenee (Lepidoptera: Pyralidae). J Econ Entomol 78:274–278CrossRefGoogle Scholar
  24. 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: 269–279Google Scholar
  25. 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. CrossRefPubMedGoogle Scholar
  26. 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 198:267–284CrossRefPubMedGoogle Scholar
  27. 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 41:350–359CrossRefPubMedPubMedCentralGoogle Scholar
  28. Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247. CrossRefPubMedGoogle Scholar
  29. 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:e47401CrossRefPubMedPubMedCentralGoogle Scholar
  30. Liao C-T, Chen C-L (2017) Oviposition preference and larval performance of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) on rice genotypes. J Econ Entomol 110:1291–1297CrossRefPubMedGoogle Scholar
  31. 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. CrossRefGoogle Scholar
  32. 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 73:2559–2568Google Scholar
  33. 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 63:166–171CrossRefGoogle Scholar
  34. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Punithavalli M, Muthukrishnan N, Rajkuma MB (2013) Defensive responses of rice genotypes for resistance against rice leaffolder Cnaphalocrocis medinalis. Rice Sci 20:363–370CrossRefGoogle Scholar
  36. 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. CrossRefPubMedGoogle Scholar
  37. Rani PU, Jyothsna Y (2010) Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiol Plant 32:695–701CrossRefGoogle Scholar
  38. Rekha lR, Singh R (2001) Sources and mechanisms of resistance in rice against rice leaffolder Cnaphalocrocis medinalis (Guenee)—a review. Agric Rev 22(1):1–12Google Scholar
  39. 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. CrossRefPubMedGoogle Scholar
  40. 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 36:179–191CrossRefPubMedGoogle Scholar
  41. 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. CrossRefGoogle Scholar
  42. 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 42:228–232PubMedGoogle Scholar
  43. Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer, BerlinCrossRefGoogle Scholar
  44. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 6:531–541CrossRefGoogle Scholar
  46. 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.
  47. 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. CrossRefPubMedGoogle Scholar
  48. 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 8:1023–1032CrossRefPubMedGoogle Scholar
  49. Vlot AC, Klessig DF, Park S-W (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442. CrossRefPubMedGoogle Scholar
  50. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20CrossRefPubMedGoogle Scholar
  51. 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. CrossRefGoogle Scholar
  52. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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. CrossRefGoogle Scholar
  54. Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. CrossRefPubMedGoogle Scholar
  55. Xu J, Wang Q-X, Wu J-C (2010) Resistance of cultivated rice varieties to Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). J Econ Entomol 103:1166–1171CrossRefPubMedGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. 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:e36214CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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–E3639CrossRefPubMedGoogle Scholar
  59. Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of AgronomyNational Taiwan UniversityTaipeiTaiwan, ROC
  2. 2.Taichung District Agricultural Research and Extension Station, COAChanghua CountyTaiwan, ROC

Personalised recommendations