水稻抗虫相关基因OsPLDa4/5和OsJMT1的功能解析
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摘要
茉莉酸(jasmonic acid, JA)在虫害诱导的植物防御反应中的作用已被广泛研究。害虫取食可以诱导植物JA合成相关基因的表达以及JA水平的升高,其可以进一步诱导相关防御化合物如胰蛋白酶抑制剂(trypsin protease inhibitors, TrypPIs)水平的升高,进而减轻害虫对植物的伤害。而针对可以调控JA合成的底物-亚麻酸(linolenicaicd, LeA)的磷脂酶D (Phospholipases D, PLD)和将JA甲基化生成茉莉酸甲酯(Methyl jasmonate, MeJA)的茉莉酸转甲基酶(jasmonic acid carboxyl methyltransferase, JMT)在水稻抗虫反应中的功能,至今无人报道。因此本文以OsPLDa4、OsPLDa5和OsJMT1为研究对象,对其在水稻诱导抗虫反应中的作用及调控机理进行了详细研究,主要结果如下：
1. OsPLDa4和OsPLDa5有相似的诱导表达谱：机械损伤、二化螟(Chilo suppressalis, rice striped stem borer, SSB)取食和JA处理能够迅速诱导OsPLDa4/5基因的表达,而褐飞虱(Nilaparvata lugens, rice brown planthopper, BPH)危害和水杨酸(salicylic aicd,SA)处理不诱导其表达。利用农杆菌介导的转化法,我们获得OsPLDa4/5反义抑制的水稻突变体植株,两个基因沉默效果均在50%左右。反义PLD水稻品系(as-pld)降低了虫害或者损伤诱导的LeA、JA、绿叶性气味(green leaf volatiles,GLVs)和乙烯的水平,同时也降低了虫害诱导的OsMPK3,OsHI-LOX,OsHPL3和OsACS2基因的表达。JA和乙烯水平的下降降低了虫害诱导的胰蛋白酶抑制剂和挥发物(Herbivore-Induced Plant Volatiles,HIPVs)的水平。生测结果表明：as-pld品系降低了水稻对二化螟的抗性,二化螟幼虫取食反义品系后生长较快,而反义品系植株在二化螟取食后受害更严重；同时as-pld品系也降低了水稻对褐飞虱的抗性,表现在BPH雌成虫喜欢在反义品系上取食和产卵,若虫也喜欢在反义品系上取食,并且若虫在反义品系上死亡率更低,同时反义品系植株在BPH雌成虫取食后死亡较早。HIPVs的降低进而导致了水稻对二化螟寄生蜂-二化螟绒茧蜂(Apanteles chilonis)的吸引的下降。回补实验表明：胰蛋白酶抑制剂水平的下降可以被JA部分回补,对SSB抗性的下降可以被外施GLVs回补,而对BPH抗性的下降是由于GLVs水平的降低造成的。综上所述,OsPLDa4/5在水稻中虫害诱导的直接和间接防御中起着重要作用。
2.通过农杆菌介导法将OsJMT1在水稻中过量表达后获得了转基因品系(oe-JMT)。oe-JMT品系在大田种植后其成熟期株高及水稻产量均较野生型下降。过量表达OsJMT1后水稻MeJA在本底和二化螟诱导后的水平均高于野生型水稻水稻,而水稻受二化螟诱导的JA和胰蛋白酶抑制剂水平下降。过量表达OsJMT1对乙烯的合成无影响。经二化螟危害诱导的几种水稻挥发物水平在oe-JMT品系水稻中较野生型高。OsJMTl正调控挥发物相关合成基因OsSMT, OsLIS和JA合成相关基因OsAOSl、OsHILOX以及OsMPK3基因的表达但不影响OsPLDa4及OsMPK6的表达。过量表达OsJMT1后水稻对二化螟抗性下降,表现在二化螟幼虫在取食oe-JMT品系水稻后体重增长较快,而oe-JMT品系水稻却增强了水稻对褐飞虱若虫的抗性,表现在褐飞虱初孵若虫在oe-JMT品系上死亡率较高,若虫不喜欢在oe-JMT品系上取食,但是却增强了对褐飞虱雌成虫的吸引作用。利用MeJA对野生型和oe-JMT品系水稻进行系列外施实验发现,oe-JMT品系水稻对BPH若虫抗性的增强是由增加的MeJA水平造成的。此外oe-JMT品系水稻对褐飞虱若虫的抗性的增强可能与oe-JMT品系水稻茎秆强度的增加有关,而其对雌成虫的吸引可能是由于BPH雌成虫诱导的过氧化氢水平的下降造成的。在田间试验中,oe-JMT品系水稻降低了褐飞虱和白背飞虱(Sogatella furcifera)的产卵量以及稻虱缨小蜂(Anagrus nilaparvatae)对褐飞虱和白背飞虱卵的寄生率,同时也降低了蚜虫(Sitobion avenae)的取食选择性。以上结果表明OsJMT1控着水稻虫害诱导的直接和间接防御反应。
The role of jasmonic acid (JA) in herbivore-induced plant defense response has been well studied. Herbivore infestation induced JA synthesis related genes' expression levels which in turn induced higher JA levels. Some defense relate compounds such as trypsin protease inhibitors (TrypPIs) levels are induced by high JA levels, in this case reduced the pests'damage to plants. Phospholipases D (PLD) controls the release of linolenic aicd (LeA), the substrate of JA biosynthesis, while jasmonic acid carboxyl methyltransferase (JMT) methylate JA to Methyl jasmonate (MeJA). Both PLD's and JMT's role in herbivore-induced rice defense response have never been reported so far. Hence we chose OsPLDa4, OsPLDa5and OsJMTl and characterized their biological functions in regulating herbivore-induced defense responses. The results are as follows:
1. OsPLDa4and OsPLDa5has similar induced expression patterns, both of which were up-regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis, mechanical wounding, and treatment with jasmonic acid (JA), while brown planthopper (BPH) Nilaparvata lugens infestation and salicylic acid (SA) treatment couldn't induce OsPLDa4and a5's expression. Antisense expression of OsPLDa4and-a5(as-pld) by Agrobacterium-mediated transformation, which resulted in a50%reduction of the expression of the two genes, reduced elicited levels of LeA, JA, GLVs, and ethylene and attenuated the SSB-induced expression of a mitogen-activated protein kinase (OsMPK3), a lipoxygenase (OsHI-LOX), a hydroperoxide lyase (OsHPL3), as well as a1-aminocyclopropane-l-carboxylic acid synthase (OsACS2). The impaired oxylipin and ethylene signaling in as-pld plants decreased the levels of herbivore-induced trypsin protease inhibitors and plant volatiles. Bioassay results show that as-pld plant reduced resistance against SSB. SSB caterpillars gained more mass on as-pld lines than on wild-type plants, and as-pld plants were more severely damaged by SSB and survived less than wild-type plants did. At the same time as-pld plant reduced resistance against BPH. BPH female adults prefer to feed and oviposit on as-pld lines than on wild-type plants. BPH nyinphs also preferred to feed on as-pld lines over wild-type plants, and BPH nymphs that fed on as-pld lines had higher survival rates than those that fed on wild-type plants. The reduced herbivore induced volatiles also reduced the attractiveness of plants to a larval parasitoid of SSB, Apanteles chilonis. The production of trypsin protease inhibitors in as-pld plants could be partially restored by JA, while the resistance to rice brown planthopper and SSB was restored by GLVs application. Our results show that phospholipases function as important components of herbivore-induced direct and indirect defenses in rice.
2. We over-expressed OsJMTl in rice by Agrobacterium-medmted transformation and got the transgenic lines (oe-JMT). Over-expressing OsJMTl reduced plant height and seed production in the filed. Oe-JMT plants increased the basic and SSB-induced MeJA levels but decreased SSB induced JA and trypsin protease inhibitors (TrypPIs) levels. While oe-JMT plants show no influence on ethylene (ETH) levels. Several kinds of rice volatiles induced by SSB infestation were higher in oe-JMT lines than that of WT plants. OsJMTl positively regulated expression levels of a methyl salicylate synthase (OsSMT), a linalool synthase (OsLIS), OsMPK3and JA synthesis gene OsAOS1and OsHILOX but has no influence on the expression levels of OsPLDa4and OsMPK6.Bioassay results show that oe-JMT plants reduced resistance against SSB. SSB caterpillars gained more mass on oe-JMT lines than on wild-type plants. While oe-JMT plants increased resistance against BPH nymph. New hached BPH nymphs survived less on oe-JMT lines than on wild-type plants and BPH nymphs preferred to feed on WT plants. However, BPH female adults prefer to feed on oe-JMT plants. Application of MeJA by different concentration on WT and oe-JMT plants show that the enhanced resistance of oe-JMT lines to BPH nymph is owing to the increased MeJA levels and also may be related to their higher stem hardness compared to WT plants and the attractness of oe-JMT plants to BPH female adults may oveing to the lower H2O2levels induced by BPH female adults. The field experiment showed that oe-JMT plants reduced attractiveness to aphaid (Sitobion avenae) as well as eggs laid by BPH and Whitebacked planthopper (WBPH, Sogatella furciferd) and those eggs'attractiveness to an egg parasitoid of BPH and WBPH, Anagrus nilaparvatae. Those results show that OsJMTl regulated herbivore-induced direct and indirect defenses in rice.
1. OsPLDa4和OsPLDa5有相似的诱导表达谱：机械损伤、二化螟(Chilo suppressalis, rice striped stem borer, SSB)取食和JA处理能够迅速诱导OsPLDa4/5基因的表达,而褐飞虱(Nilaparvata lugens, rice brown planthopper, BPH)危害和水杨酸(salicylic aicd,SA)处理不诱导其表达。利用农杆菌介导的转化法,我们获得OsPLDa4/5反义抑制的水稻突变体植株,两个基因沉默效果均在50%左右。反义PLD水稻品系(as-pld)降低了虫害或者损伤诱导的LeA、JA、绿叶性气味(green leaf volatiles,GLVs)和乙烯的水平,同时也降低了虫害诱导的OsMPK3,OsHI-LOX,OsHPL3和OsACS2基因的表达。JA和乙烯水平的下降降低了虫害诱导的胰蛋白酶抑制剂和挥发物(Herbivore-Induced Plant Volatiles,HIPVs)的水平。生测结果表明：as-pld品系降低了水稻对二化螟的抗性,二化螟幼虫取食反义品系后生长较快,而反义品系植株在二化螟取食后受害更严重；同时as-pld品系也降低了水稻对褐飞虱的抗性,表现在BPH雌成虫喜欢在反义品系上取食和产卵,若虫也喜欢在反义品系上取食,并且若虫在反义品系上死亡率更低,同时反义品系植株在BPH雌成虫取食后死亡较早。HIPVs的降低进而导致了水稻对二化螟寄生蜂-二化螟绒茧蜂(Apanteles chilonis)的吸引的下降。回补实验表明：胰蛋白酶抑制剂水平的下降可以被JA部分回补,对SSB抗性的下降可以被外施GLVs回补,而对BPH抗性的下降是由于GLVs水平的降低造成的。综上所述,OsPLDa4/5在水稻中虫害诱导的直接和间接防御中起着重要作用。
2.通过农杆菌介导法将OsJMT1在水稻中过量表达后获得了转基因品系(oe-JMT)。oe-JMT品系在大田种植后其成熟期株高及水稻产量均较野生型下降。过量表达OsJMT1后水稻MeJA在本底和二化螟诱导后的水平均高于野生型水稻水稻,而水稻受二化螟诱导的JA和胰蛋白酶抑制剂水平下降。过量表达OsJMT1对乙烯的合成无影响。经二化螟危害诱导的几种水稻挥发物水平在oe-JMT品系水稻中较野生型高。OsJMTl正调控挥发物相关合成基因OsSMT, OsLIS和JA合成相关基因OsAOSl、OsHILOX以及OsMPK3基因的表达但不影响OsPLDa4及OsMPK6的表达。过量表达OsJMT1后水稻对二化螟抗性下降,表现在二化螟幼虫在取食oe-JMT品系水稻后体重增长较快,而oe-JMT品系水稻却增强了水稻对褐飞虱若虫的抗性,表现在褐飞虱初孵若虫在oe-JMT品系上死亡率较高,若虫不喜欢在oe-JMT品系上取食,但是却增强了对褐飞虱雌成虫的吸引作用。利用MeJA对野生型和oe-JMT品系水稻进行系列外施实验发现,oe-JMT品系水稻对BPH若虫抗性的增强是由增加的MeJA水平造成的。此外oe-JMT品系水稻对褐飞虱若虫的抗性的增强可能与oe-JMT品系水稻茎秆强度的增加有关,而其对雌成虫的吸引可能是由于BPH雌成虫诱导的过氧化氢水平的下降造成的。在田间试验中,oe-JMT品系水稻降低了褐飞虱和白背飞虱(Sogatella furcifera)的产卵量以及稻虱缨小蜂(Anagrus nilaparvatae)对褐飞虱和白背飞虱卵的寄生率,同时也降低了蚜虫(Sitobion avenae)的取食选择性。以上结果表明OsJMT1控着水稻虫害诱导的直接和间接防御反应。
The role of jasmonic acid (JA) in herbivore-induced plant defense response has been well studied. Herbivore infestation induced JA synthesis related genes' expression levels which in turn induced higher JA levels. Some defense relate compounds such as trypsin protease inhibitors (TrypPIs) levels are induced by high JA levels, in this case reduced the pests'damage to plants. Phospholipases D (PLD) controls the release of linolenic aicd (LeA), the substrate of JA biosynthesis, while jasmonic acid carboxyl methyltransferase (JMT) methylate JA to Methyl jasmonate (MeJA). Both PLD's and JMT's role in herbivore-induced rice defense response have never been reported so far. Hence we chose OsPLDa4, OsPLDa5and OsJMTl and characterized their biological functions in regulating herbivore-induced defense responses. The results are as follows:
1. OsPLDa4and OsPLDa5has similar induced expression patterns, both of which were up-regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis, mechanical wounding, and treatment with jasmonic acid (JA), while brown planthopper (BPH) Nilaparvata lugens infestation and salicylic acid (SA) treatment couldn't induce OsPLDa4and a5's expression. Antisense expression of OsPLDa4and-a5(as-pld) by Agrobacterium-mediated transformation, which resulted in a50%reduction of the expression of the two genes, reduced elicited levels of LeA, JA, GLVs, and ethylene and attenuated the SSB-induced expression of a mitogen-activated protein kinase (OsMPK3), a lipoxygenase (OsHI-LOX), a hydroperoxide lyase (OsHPL3), as well as a1-aminocyclopropane-l-carboxylic acid synthase (OsACS2). The impaired oxylipin and ethylene signaling in as-pld plants decreased the levels of herbivore-induced trypsin protease inhibitors and plant volatiles. Bioassay results show that as-pld plant reduced resistance against SSB. SSB caterpillars gained more mass on as-pld lines than on wild-type plants, and as-pld plants were more severely damaged by SSB and survived less than wild-type plants did. At the same time as-pld plant reduced resistance against BPH. BPH female adults prefer to feed and oviposit on as-pld lines than on wild-type plants. BPH nyinphs also preferred to feed on as-pld lines over wild-type plants, and BPH nymphs that fed on as-pld lines had higher survival rates than those that fed on wild-type plants. The reduced herbivore induced volatiles also reduced the attractiveness of plants to a larval parasitoid of SSB, Apanteles chilonis. The production of trypsin protease inhibitors in as-pld plants could be partially restored by JA, while the resistance to rice brown planthopper and SSB was restored by GLVs application. Our results show that phospholipases function as important components of herbivore-induced direct and indirect defenses in rice.
2. We over-expressed OsJMTl in rice by Agrobacterium-medmted transformation and got the transgenic lines (oe-JMT). Over-expressing OsJMTl reduced plant height and seed production in the filed. Oe-JMT plants increased the basic and SSB-induced MeJA levels but decreased SSB induced JA and trypsin protease inhibitors (TrypPIs) levels. While oe-JMT plants show no influence on ethylene (ETH) levels. Several kinds of rice volatiles induced by SSB infestation were higher in oe-JMT lines than that of WT plants. OsJMTl positively regulated expression levels of a methyl salicylate synthase (OsSMT), a linalool synthase (OsLIS), OsMPK3and JA synthesis gene OsAOS1and OsHILOX but has no influence on the expression levels of OsPLDa4and OsMPK6.Bioassay results show that oe-JMT plants reduced resistance against SSB. SSB caterpillars gained more mass on oe-JMT lines than on wild-type plants. While oe-JMT plants increased resistance against BPH nymph. New hached BPH nymphs survived less on oe-JMT lines than on wild-type plants and BPH nymphs preferred to feed on WT plants. However, BPH female adults prefer to feed on oe-JMT plants. Application of MeJA by different concentration on WT and oe-JMT plants show that the enhanced resistance of oe-JMT lines to BPH nymph is owing to the increased MeJA levels and also may be related to their higher stem hardness compared to WT plants and the attractness of oe-JMT plants to BPH female adults may oveing to the lower H2O2levels induced by BPH female adults. The field experiment showed that oe-JMT plants reduced attractiveness to aphaid (Sitobion avenae) as well as eggs laid by BPH and Whitebacked planthopper (WBPH, Sogatella furciferd) and those eggs'attractiveness to an egg parasitoid of BPH and WBPH, Anagrus nilaparvatae. Those results show that OsJMTl regulated herbivore-induced direct and indirect defenses in rice.
引文
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Kim EH, Kim YS, Park SH, Koo YJ, Do Choi Y, Chung YY, Lee IJ, Kim JK (2009) Methyl Jasmonate Reduces Grain Yield by Mediating Stress Signals to Alter Spikelet Development in Rice. Plant Physiology 149:1751-1760
Kobayashi H, Yanaka M, Ikeda TM (2010) Exogenous Methyl Jasmonate Alters Trichome Density on Leaf Surfaces of Rhodes Grass (Chloris gayana Kunth). Journal of Plant Growth Regulation 29:506-511
Kollner TG, Lenk C, Zhao N, Seidl-Adams I, Gershenzon J, Chen F, Degenhardt J (2010) Herbivore-Induced SABATH Methyltransferases of Maize That Methylate Anthranilic Acid Using S-Adenosyl-L-Methionine. Plant Physiology 153:1795-1807
Koo YJ, Kim MA, Kim EH, Song JT, Jung C, Moon JK, Kim JH, Seo HS, Song SI, Kim JK, Lee JS, Cheong JJ, Do Choi Y (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Molecular Biology 64:1-15
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Lee S, Hirt H, Lee Y (2001) Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant Journal 26:479-486
Li MY, Hong YY, Wang XM (2009) Phospholipase D-and phosphatidic acid-mediated signaling in plants. Biochimica Et Biophysica Acta-Molecular and Cell Biology of Lipids 1791:927-935
Lou YG, Du MH, Turlings TCJ, Cheng JA, Shan WF (2005) Exogenous application of jasmonic acid induces volatile emissions in rice and enhances parasitism of Nilaparvata lugens eggs by theParasitoid Anagrus nilaparvatae. Journal of Chemical Ecology 31: 1985-2002
Lu J, Ju HP, Zhou GX, Zhu CS, Erb M, Wang XP, Wang P, Lou YG (2011) An EAR-motif-containing ERF transcription factor affects herbivore-induced signaling, defense and resistance in rice. Plant Journal 68:583-596
Lu YJ, Wang X, Lou YG, Cheng JA (2006) Role of ethylene signaling in the production of rice volatiles induced by the rice brown planthopper Nilaparvata lugens. Chinese Science Bulletin 51:2457-2465
McGee JD, Roe JL, Sweat TA, Wang XM, Guikema JA, Leach JE (2003) Rice phospholipase D isoforms show differential cellular location and gene induction. Plant and Cell Physiology 44:1013-1026
Mosblech A, Feussner I, Heilmann I (2009) Oxylipins:Structurally diverse metabolites from fatty acid oxidation. Plant Physiology and Biochemistry 47:511-517
Murfitt LM, Kolosova N, Mann CJ, Dudareva N (2000) Purification and characterization of S-adenosyl-L-methionine:Benzoic acid carboxyl methyltransferase, the enzyme responsible for biosynthesis of the volatile ester methyl benzoate in flowers of Antirrhinum majus. Archives of Biochemistry and Biophysics 382:145-151
Negre F, Kolosova N, Knoll J, Kish CM, Dudareva N (2002) Novel S-adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme responsible for biosynthesis of methyl salicylate and methyl benzoate, is not involved in floral scent production in snapdragon flowers. Archives of Biochemistry and Biophysics 406:261-270
Pinhero RG, Almquist KC, Novotna Z, Paliyath G (2003) Developmental regulation of phospholipase D in tomato fruits. Plant Physiology and Biochemistry 41:223-240
Qu CH, Huang F, Huang YF, Tao L, Shi WP (2006) Determination of a-Linolenic acid in Gingko leaf tablets by GC-MS. Chinese Journal of Hospital Pharmacy 26:1099-1101
Rajashekar CB, Zhou HE, Zhang YW, Li WQ, Wang XM (2006) Suppression of phospholipase D alpha 1 induces freezing tolerance in Arabidopsis:Response of coldresponsive genes and osmolyte accumulation. Journal of Plant Physiology 163: 916-926
Redman AM, Cipollini DF, Schultz JC (2001) Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum. Oecologia 126:380-385
Ritsema T, van Zanten M, Leon-Reyes A, Voesenek LACJ, Millenaar FF, Pieterse CMJ, Peeters AJM (2010) Kinome Profiling Reveals an Interaction Between Jasmonate, Salicylate and Light Control of Hyponastic Petiole Growth in Arabidopsis thaliana. Plos One 5
Rohwer CL, Erwin JE (2010) Spider mites (Tetranychus urticae) perform poorly on and disperse from plants exposed to methyl jasmonate. Entomologia Experimentalis Et Applicata 137:143-152
Ross JR, Nam KH, D'Auria JC, Pichersky E (1999) S-adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Archives of Biochemistry and Biophysics 367:9-16
Ryu SB, Wang XM (1998) Increase in free linolenic and linoleic acids associated with phospholipase D-mediated hydrolysis of phospholipids in wounded castor bean leaves. Biochim. Biophys. Acta 1393:193-202
Sampedro L, Moreira X, Zas R (2011) Resistance and response of Pinus pinaster seedlings to Hylobius abietis after induction with methyl jasmonate. Plant Ecology 212:397-401
Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase:A key enzyme for jasmonate-regulated plant responses. Proceedings of the National Academy of Sciences of the United States of America 98: 4788-4793
Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants:An approach for improving plant resistance against both herbivores and pathogens. Proc. Natl. Acad. Sci. USA 103:16672-16676
Song MS, Kim DG, Lee SH (2005) Isolation and characterization of a jasmonic acid carboxyl methyltransferase gene from hot pepper (Capsicum annuum L.). Journal of Plant Biology 48:292-297
Stitz M, Baldwin IT, Gaquerel E (2011) Diverting the Flux of the JA Pathway in Nicotiana attenuata Compromises the Plant's Defense Metabolism and Fitness in Nature and Glasshouse. Plos One 6
Stitz M, Gase K, Baldwin IT, Gaquerel E (2011) Ectopic Expression of AtJMT in Nicotiana attenuata: Creating a Metabolic Sink Has Tissue-Specific Consequences for the Jasmonate Metabolic Network and Silences Downstream Gene Expression. Plant Physiology 157:341-354
Testerink C, Larsen PB, van der Does D, van Himbergen JAJ, Munnik T (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. Journal of Experimental Botany 58:3905-3914
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu GH, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448:661-U662
Tierranegra-Garcia N, Salinas-Soto P, Torres-Pacheco I, Ocampo-Velazquez RV, Rico-Garcia E, Mendoza-Diaz SO, Feregrino-Perez AA, Mercado-Luna A, Vargas-Hernandez M, Soto-Zarazua GM, Guevara-Gonzalez RG (2011) Effect of foliar salicylic acid and methyl jasmonate applications on protection against pill-bugs in lettuce plants (Lactuca sativa). Phytoparasitica 39:137-144
Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc. Natl. Acad. Sci. USA 98:8139-8144
von Merey GE, Veyrat N, de Lange E, Degen T, Mahuku G, Valdez RL, Turlings TCJ, D'Alessandro M (2012) Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields. Biological Control 60:7-15
Wan SB, Tian L, Tian RR, Pan QH, Zhan JC, Wen PF, Chen JY, Zhang P, Wang W, Huang WD (2009) Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiology and Biochemistry 47:504-510
Wang CX, Zien CA, Afitlhile M, Welti R, Hildebrand DF, Wang XM (2000) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12:2237-2246
Wang L, Allmann S, Wu JS, Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiology 146:904-915
Wang X, Hu LC, Zhou GX, Chen JA, Lou YG (2011) Salicylic acid and ethylene signaling pathways are involved in production of rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenee). Chinese Science Bulletin (in press).
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