Biotic stress-induced expression of mulberry cystatins and identification of cystatin exhibiting stability to silkworm gut proteinases

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• 作者：Jiubo Liang ; Yupeng Wang ; Guangyu Ding ; Wensheng Li ; Guangwei Yang ; Ningjia He
• 关键词：Antidigestive stability ; Cystatin ; Induced gene expression ; Insect herbivory ; Mulberry
• 刊名：Planta
• 出版年：2015
• 出版时间：November 2015
• 年：2015
• 卷：242
• 期：5
• 页码：1139-1151
• 全文大小：1,143 KB
• 参考文献：Arai S, Matsumoto I, Emori Y, Abe K (2002) Plant seed cystatins and their target enzymes of endogenous and exogenous origin. J Agric Food Chem 50:6612鈥?617CrossRef PubMed
  Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91鈥?11CrossRef PubMed
  Atkinson HJ, Grimwood S, Johnston K, Green J (2004) Prototype demonstration of transgenic resistance to the nematode Radopholus similis conferred on banana by a cystatin. Transgenic Res 13:135鈥?42CrossRef PubMed
  Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249鈥?57CrossRef PubMed
  Belenghi B, Acconcia F, Trovato M, Perazzolli M, Bocedi A, Polticelli F, Ascenzi P, Delledonne M (2003) AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. Eur J Biochem 270:2593鈥?604CrossRef PubMed
  Benchabane M, Schluter U, Vorster J, Goulet MC, Michaud D (2010) Plant cystatins. Biochimie 92:1657鈥?666CrossRef PubMed
  Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: signalP 3.0. J Mol Biol 340:783鈥?95CrossRef PubMed
  Bolter CJ (1993) Methyl jasmonate induces papain inhibitor(s) in tomato leaves. Plant Physiol 103:1347鈥?353PubMed Central PubMed
  Bonaventure G, VanDoorn A, Baldwin IT (2011) Herbivore-associated elicitors: fAC signaling and metabolism. Trends Plant Sci 16:294鈥?99CrossRef PubMed
  Botella MA, Xu Y, Prabha TN, Zhao Y, Narasimhan ML, Wilson KA, Nielsen SS, Bressan RA, Hasegawa PM (1996) Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol 112:1201鈥?210PubMed Central CrossRef PubMed
  Bricchi I, Leitner M, Foti M, Mithofer A, Boland W, Maffei ME (2010) Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: early signaling and volatile emission in Lima bean (Phaseolus lunatus L.). Planta 232:719鈥?29CrossRef PubMed
  Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237鈥?9242PubMed Central CrossRef PubMed
  Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol 143:1954鈥?967PubMed Central CrossRef PubMed
  Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666鈥?71CrossRef PubMed
  Corr-Menguy F, Cejudo FJ, Mazubert C, Vidal J, Lelandais-Briere C, Torres G, Rode A, Hartmann C (2002) Characterization of the expression of a wheat cystatin gene during caryopsis development. Plant Mol Biol 50:687鈥?98CrossRef PubMed
  DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, Palo Alto
  Duan XL, Li XG, Xue QZ, AboElSaad M, Xu DP, Wu R (1996) Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat Biotechnol 14:494鈥?98CrossRef PubMed
  Duceppe MO, Cloutier C, Michaud D (2012) Wounding, insect chewing and phloem sap feeding differentially alter the leaf proteome of potato. Solanum tuberosum L. Proteome Sci 10:73CrossRef PubMed
  Edgar RC (2004a) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113PubMed Central CrossRef PubMed
  Edgar RC (2004b) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792鈥?797PubMed Central CrossRef PubMed
  Felton GW, Tumlinson JH (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11:457鈥?63CrossRef PubMed
  Girard C, Rivard D, Kiggundu A, Kunert K, Gleddie SC, Cloutier C, Michaud D (2007) A multicomponent, elicitor-inducible cystatin complex in tomato, Solanum lycopersicum. New Phytol 173:841鈥?51CrossRef PubMed
  Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776鈥?77CrossRef PubMed
  Green AR, Nissen MS, Kumar GN, Knowles NR, Kang C (2013) Characterization of Solanum tuberosum multicystatin and the significance of core domains. Plant Cell 25:5043鈥?052PubMed Central CrossRef PubMed
  He N, Zhang C, Qi X, Zhao S, Tao Y, Yang G, Lee TH, Wang X, Cai Q, Li D, Lu M, Liao S, Luo G, He R, Tan X, Xu Y, Li T, Zhao A, Jia L, Fu Q, Zeng Q, Gao C, Ma B, Liang J, Wang X, Shang J, Song P, Wu H, Fan L, Wang Q, Shuai Q, Zhu J, Wei C, Zhu-Salzman K, Jin D, Wang J, Liu T, Yu M, Tang C, Wang Z, Dai F, Chen J, Liu Y, Zhao S, Lin T, Zhang S, Wang J, Wang J, Yang H, Yang G, Wang J, Paterson AH, Xia Q, Ji D, Xiang Z (2013) Draft genome sequence of the mulberry tree Morus notabilis. Nat Commun 4:2445PubMed Central CrossRef PubMed
  Hettenhausen C, Baldwin IT, Wu J (2013) Nicotiana attenuata MPK4 suppresses a novel jasmonic acid (JA) signaling-independent defense pathway against the specialist insect Manduca sexta, but is not required for the resistance to the generalist Spodoptera littoralis. New Phytol 199:787鈥?99CrossRef PubMed
  Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160鈥?63CrossRef
  Jacinto T, Fernandes KVS, Machado OLT, Siqueira-Junior CL (1998) Leaves of transgenic tomato plants overexpressing prosystemin accumulate high levels of cystatin. Plant Sci 138:35鈥?2CrossRef
  Johnson R, Narvaez J, An G, Ryan C (1989) Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 86:9871鈥?875PubMed Central CrossRef PubMed
  Katsir L, Chung HS, Koo AJ, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428鈥?35PubMed Central CrossRef PubMed
  Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459鈥?468PubMed Central CrossRef PubMed
  Kiyosaki T, Matsumoto I, Asakura T, Funaki J, Kuroda M, Misaka T, Arai S, Abe K (2007) Gliadain, a gibberellin-inducible cysteine proteinase occurring in germinating seeds of wheat, Triticum aestivum L., specifically digests gliadin and is regulated by intrinsic cystatins. FEBS J 274:1908鈥?917CrossRef PubMed
  Margis R, Reis EM, Villeret V (1998) Structural and phylogenetic relationships among plant and animal cystatins. Arch Biochem Biophys 359:24鈥?0CrossRef PubMed
  Martinez M, Abraham Z, Carbonero P, Diaz I (2005) Comparative phylogenetic analysis of cystatin gene families from Arabidopsis, rice and barley. Mol Genet Genomics 273:423鈥?32CrossRef PubMed
  Martinez M, Diaz-Mendoza M, Carrillo L, Diaz I (2007) Carboxy terminal extended phytocystatins are bifunctional inhibitors of papain and legumain cysteine proteinases. FEBS Lett 581:2914鈥?918CrossRef PubMed
  Martinez M, Cambra I, Carrillo L, Diaz-Mendoza M, Diaz I (2009) Characterization of the entire cystatin gene family in barley and their target cathepsin L-like cysteine-proteases, partners in the hordein mobilization during seed germination. Plant Physiol 151:1531鈥?545PubMed Central CrossRef PubMed
  Mcmanus MT, White DWR, Mcgregor PG (1994) Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests. Transgenic Res 3:50鈥?8CrossRef
  Michaud D, Cantin L, Bonade-Bottino M, Jouanin L, Vrain TC (1996) Identification of stable plant cystatin/nematode proteinase complexes using mildly denaturing gelatin/polyacrylamide gel electrophoresis. Electrophoresis 17:1373鈥?379CrossRef PubMed
  Mithofer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160鈥?168PubMed Central CrossRef PubMed
  Nagaraju J, Abraham EG (1995) Purification and characterization of digestive amylase from the tasar Silkworm, Antheraea mylitta (Lepidoptera, Saturniidae). Comp Biochem Physiol B: Biochem Mol Biol 110:201鈥?09CrossRef
  Nagata K, Kudo N, Abe K, Arai S, Tanokura M (2000) Three-dimensional solution structure of oryzacystatin-I, a cysteine proteinase inhibitor of the rice, Oryza sativa L. japonica. Biochemistry 39:14753鈥?4760CrossRef PubMed
  Nissen MS, Kumar GN, Youn B, Knowles DB, Lam KS, Ballinger WJ, Knowles NR, Kang C (2009) Characterization of Solanum tuberosum multicystatin and its structural comparison with other cystatins. Plant Cell 21:861鈥?75PubMed Central CrossRef PubMed
  Peitsch MC (1996) ProMod and Swiss-Model: internet-based tools for automated comparative protein modelling. Biochem Soc Trans 24:274鈥?79CrossRef PubMed
  Pernas M, Sanchez-Monge R, Gomez L, Salcedo G (1998) A chestnut seed cystatin differentially effective against cysteine proteinases from closely related pests. Plant Mol Biol 38:1235鈥?242CrossRef PubMed
  Pernas M, Sanchez-Mong R, Salcedo G (2000) Biotic and abiotic stress can induce cystatin expression in chestnut. FEBS Lett 467:206鈥?10CrossRef PubMed
  Rawlings ND, Waller M, Barrett AJ, Bateman A (2014) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 42:D503鈥揇509PubMed Central CrossRef PubMed
  Ribeiro APO, Pereira EJG, Galvan TL, Picanco MC, Picoli EAT, da Silva DJH, Fari MG, Otoni WC (2006) Effect of eggplant transformed with oryzacystatin gene on Myzus persicae and Macrosiphum euphorbiae. J Appl Entomol 130:84鈥?0CrossRef
  Santamaria ME, Diaz-Mendoza M, Diaz I, Martinez M (2014) Plant protein peptidase inhibitors: an evolutionary overview based on comparative genomics. BMC Genom 15:812CrossRef
  Schafer M, Fischer C, Meldau S, Seebald E, Oelmuller R, Baldwin IT (2011) Lipase activity in insect oral secretions mediates defense responses in Arabidopsis. Plant Physiol 156:1520鈥?534PubMed Central CrossRef PubMed
  Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH 3rd, Teal PE (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci USA 106:653鈥?57PubMed Central CrossRef PubMed
  Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381鈥?385PubMed Central CrossRef PubMed
  Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:431鈥?44PubMed Central CrossRef PubMed
  Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol Lett 10:499鈥?11CrossRef PubMed
  Stubbs MT, Laber B, Bode W, Huber R, Jerala R, Lenarcic B, Turk V (1990) The refined 2.4 A X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction. EMBO J 9:1939鈥?947PubMed Central PubMed
  Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731鈥?739PubMed Central CrossRef PubMed
  Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153鈥揝164PubMed Central PubMed
  van der Hoorn RA (2008) Plant proteases: from phenotypes to molecular mechanisms. Annu Rev Plant Biol 59:191鈥?23CrossRef PubMed
  Waldron C, Wegrich LM, Merlo PA, Walsh TA (1993) Characterization of a genomic sequence coding for potato multicystatin, an eight-domain cysteine proteinase inhibitor. Plant Mol Biol 23:801鈥?12CrossRef PubMed
  Weeda SM, Mohan Kumar GN, Richard Knowles N (2009) Developmentally linked changes in proteases and protease inhibitors suggest a role for potato multicystatin in regulating protein content of potato tubers. Planta 230:73鈥?4CrossRef PubMed
  Wu J, Haard NF (2000) Purification and characterization of a cystatin from the leaves of methyl jasmonate treated tomato plants. Comp Biochem Physiol C: Toxicol Pharmacol 127:209鈥?20
  Zavala JA, Patankar AG, Gase K, Hui DQ, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181鈥?190PubMed Central CrossRef PubMed
  
• 作者单位：Jiubo Liang (1)
  Yupeng Wang (1)
  Guangyu Ding (1)
  Wensheng Li (1)
  Guangwei Yang (1)
  Ningjia He (1)
  
  1. State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing, 400715, China
  
• 刊物主题：Plant Sciences; Agriculture; Ecology; Forestry;
• 出版者：Springer Berlin Heidelberg
• ISSN：1432-2048

文摘

Main conclusion Biotic stresses induce the expression of mulberry cystatins. MaCPI-4 protein is stable in silkworm digestive fluid and accumulates in gut food debris and frass. Plant cystatins are considered to be involved in defense responses to insect herbivores though little is known about how cystatins from the natural host respond to a specialist herbivory and the following postingestive interaction is also poorly understood. Here, we studied the biotic stress-mediated inductions of cystatins from mulberry tree, and examined the stability of mulberry cystatin proteins in the gut of silkworm, Bombyx mori, a specialist insect feeding on mulberry leaf. First, we cloned and characterized six cystatin genes from a mulberry cultivar, Morus atropurpurea Roxb., named as MaCPI-1 to MaCPI-6. The recombinant MaCPI-1, MaCPI-3 and MaCPI-4 proteins, which showed inhibitory effects against papain in vitro, were produced. Silkworm herbivory as well as methyl jasmonate (MeJA) treatment induced the expression of five mulberry cystatin genes, and the highest inductions were observed from MaCPI-1 and MaCPI-6. Mechanical wounding led to the inductions of four cystatin genes. The differential induction occurred in MaCPI-2. The induced protein changes were detected from three mulberry cystatins comprising MaCPI-1, MaCPI-3 and MaCPI-4. In vivo and in vitro assays showed that MaCPI-1 and MaCPI-3 proteins were susceptible to silkworm digestive fluid and MaCPI-4 had an antidigestive stability, and was detected in silkworm gut and frass. Collectively, our data indicated that biotic stresses resulted in the transcriptional inductions and protein changes of mulberry cystatins (MaCPIs), and identified MaCPI-4 with stability in the gut of its specialist herbivore.