Abstract
The roles of signaling pathways in the production of trypsin proteinase inhibitors (TrypPIs) in rice infested by the leaf folder (LF) Cnaphalocrocis medinalis were studied. Infestation by LF increased TrypPI levels in the leaves of rice plants at the tillering, booting and flowering stages but decreased TrypPI levels at the ripening stage; TrypPI levels in rice stems did not increase at any developmental stage. Infestation by LF at the tillering stage systemically increased TrypPI levels in leaves but not in stems; it also enhanced salicylic acid (SA) levels in leaves and stems, and the ethylene level released from plants. However, LF infestation did not increase JA concentrations. Exogenous application of SA or ethylene enhanced TrypPI levels in the leaves and stems of plants at the tillering stage, whereas treatment with both SA and ethylene induced lower levels of TrypPIs than treatment with SA or ethylene alone, suggesting an antagonistic effect of SA and ethylene on TrypPIs induction. The results suggest that both SA and ethylene signaling pathways are involved in the production of TrypPIs in rice induced by LF; moreover, the antagonistic effect of SA and ethylene may explain the changes in TrypPI levels seen at different plant developmental stages and in different organs.
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Macedo M L R, Mello G C, Freire M D G, et al. Effect of a trypsin inhibitor from Dimorphandra mollis seeds on the development of Callosobruchus maculatus. Plant Physiol Biochem, 2002, 40: 891–898
Tamhane V A, Chougule N P, Giri A P, et al. In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim Biophys Acta, 2005, 1722: 156–167
Franco O L, Dias S C, Magalhaes C P, et al. Effects of sovbean Kunitz trypsin inhibitor on the cotton boll weevil (Anthonomus grandis). Phytochemistry, 2004, 65: 81–89
Bhattacharyya A, Leighton S M, Babu C R. Bioinsecticidal activity of Archidendron ellipticum trypsin inhibitor on growth and serine digestive enzymes during larval development of Spodoptera litura. Comp Bioch Phys C, 2007, 145: 669–677
Zhu Y C, Abel C A, Chen M S. Interaction of Cry1Ac toxin (Bacillus thuringiensis) and proteinase inhibitors on the growth, development, and midgut proteinase activities of the bollworm, Helicoverpa zea. Pestic Biochem Phys, 2007, 87: 39–46
Geoffroy P, Legrand M, Fritig B. Isolation and characterization of a proteinaceous inhibitor of microbial proteinases induced during the hypersensitive reaction of tobacco to tobacco mosaic virus. Mol Plant Microbe Interact, 1990, 3: 327–333
Balandin T, Vanderdoes C, Albert J M B, et al. Structure and induction pattern of a novel proteinase inhibitor class II gene of tobacco. Plant Mol Biol, 1995, 27: 1197–1204
Qu L J, Chen J, Liu M H, et al. Molecular cloning and functional analysis of a novel type of Bowman-Birk inhibitor gene family in rice. Plant Physiol, 2003, 133: 560–570
Hermosa M R, Turrà D, Fogliano V, et al. Identification and characterization of potato protease inhibitors able to inhibit pathogenicity and growth of Botrytis cinerea. Physiol Mol Plant Pathol, 2006, 68: 138–148
Oliveira A S, Migliolo L, Aquino R O, et al. Purification and characterization of a trypsin-papain inhibitor from Pithecelobium dumosum seeds and its in vitro effects towards digestive enzymes from insect pests. Plant Physiol Biochem, 2007, 45: 858–865
Cordero M J, Raventos D, Sansegundo B. Expression of a maize proteinase-inhibitor gene is induced in response to wounding and fungal infection: Systemic wound-response of a monocot gene. Plant J, 1994, 6: 141–150
Rakwal R, Agrawal G K, Jwa N S. Characterization of a rice (Oryza sativa L.) Bowman-Birk proteinase inhibitor: Tightly light regulated induction in response to cut, jasmonic acid, ethylene and protein phosphatase 2A inhibitors. Gene, 2001, 263: 189–198
Van Dam N M, Horn M, Mares M, et al. Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol, 2001, 27: 547–568
Casaretto J A, Zuniga G E, Corcuera L J. Abscisic acid and jasmonic acid affect proteinase inhibitor activities in barley leaves. J Plant Physiol, 2004, 161: 389–396
Lou Y G, Baldwin I T. Nitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses to Nicotiana attenuata. Plant Physiol, 2004, 135: 496–506
Lou Y G, Baldwin I T. Silencing of a germin-like gene in Nicotiana attenuata improves performance of native herbivores. Plant Physiol, 2006, 140: 1126–1136
Jongsma M A, Bakker P L, Visser B, et al. Trypsin inhibitor activity in mature tobacco and tomato plants is mainly induced locally in response to insect attack, wounding and virus infection. Planta, 1994, 195: 29–35
Pearce G, Johnson S, Ryan C A. Purification and characterization from tobacco (Nicotiana tabacum) leaves of six small, wound-inducible, proteinase isoinhibitors of the potato inhibitor II family. Plant Physiol, 1993, 102: 639–644
Ohto M, Nakamurakito K, Nakamura K. Induction of expression of genes coding for sporamin and beta-amylase by polygalacturonic acid in leaf-petiole cuttings of sweet potato. Plant Physiol, 1992, 99: 422–427
Orians C M, Pomerleau J, Ricco R. Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J Chem Ecol, 2000, 26: 471–485
Wang S J, Lan Y C, Chen S F, et al. Wound-response regulation of the sweet potato sporamin gene promoter region. Plant Mol Biol, 2002, 48: 223–231
Botella M A, Xu Y, Prabha T N, et al. Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol, 1996, 112: 1201–1210
O’Donnell P J, Calvert C, Atzorn R, et al. Ethylene as a signal mediating the wound response of tomato plants. Science, 1996, 274: 1914–1917
Botelho-Júnior S, Siqueira-Júnior C L, Jardim B C, et al. Trypsin inhibitors in passion fruit (Passiflora f. edulis flavicarpa) leaves: Accumulation in response to methyl jasmonate, mechanical wounding, and herbivory. J Agric Food Chem, 2008, 56: 9404–9409
Agrawal G K, Rakwal R, Jwa N S, et al. Oryza sativa proteinase inhibitor gene, OsPIN, whose mRNA specifically accumulates in a compatible host-blast pathogen interaction. Plant Physiol Biochem, 2002, 40: 175–182
Ding J H. Agricultural Emtomology (in Chinese). Nanjing: Jiangsu Scientific and Technological Press, 1991
Wang X, Lu Y H, Wang X, et al. Influence of infestation by rice leaf folder Cnaphalocrocis medinalis on levels of defense chemicals and signal moleculars. J Zhejiang Univ, 2008, 34: 532–539
Zhou G X, Qi J F, Ren N, et al. Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J, 2009, 60: 638–648
Lou Y, Baldwin I T. Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc Natl Acad Sci USA, 2003, 100: 14581–14586
Howe G A, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol, 2008, 59: 41–66
Wu J Q, Hettenhausen C, Meldau S, et al. Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell, 2007, 19: 1096–1122
Bostock R M. Signal crosstalk and induced resistance: Straddling the line between cost and benefit. Annu Rev Phytopath, 2005, 43: 545–580
Lee A, Cho K, Jang S, et al. Inverse correlation between jasmonic acid and salicylic acid during early wound response in rice. Biochem Biophys Res Comm, 2004, 318: 734–738
Wu J Q, Baldwin I T. Herbivory-induced signalling in plants: Perception and action. Plant Cell Environ, 2009, 32: 1161–1174
Ausloos G R J, Proost P, Vandamme J, et al. Proteinase inhibitor II is developmentally regulated in Nicotiana flowers. Physiol Plantarum, 1995, 94: 701–707
Matyssek R, Agerer R, Ernst D, et al. The plant’s capacity in regulating resource demand. Plant Biol, 2005, 7: 560–580
Herbers K, Meuwly P, Metraux J P, et al. Salicylic acid-independent induction of pathogenesis-related protein transcripts by sugars is dependent on leaf developmental stage. FEBS Lett, 1996, 397: 239–244
Ohnmeiss T E, Baldwin I T. Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology, 2000, 81: 1765–1783
Alexander L, Grierson D. Ethylene biosynthesis and action in tomato: A model for climacteric fruit ripening. J Exp Bot, 2002, 53: 2039–2055
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Wang, X., Hu, L., Zhou, G. et al. Salicylic acid and ethylene signaling pathways are involved in production of rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenée). Chin. Sci. Bull. 56, 2351–2358 (2011). https://doi.org/10.1007/s11434-011-4568-y
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DOI: https://doi.org/10.1007/s11434-011-4568-y