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Proteomic analysis of Arabidopsis thaliana leaves infested by tobacco whitefly Bemisia tabaci (Gennadius) B biotype

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Abstract

Bemisia tabaci (Gennadius) B biotype, a destructive pest causing heavy damage to crop production, has become an important economic pest of agriculture worldwide. Here, the proteome change of Arabidopsis thaliana leaves infested by B. tabaci was studied with two-dimensional electrophoresis and mass spectrometry. Twenty proteins showed a significant change in expression after B. tabaci infestation, including ten up-regulated and ten down-regulated. Using the Gene Ontology annotation, all except one were classified into one of four major groups based on their molecular function and biological process. Six of the proteins were involved in protein folding and regulation (HSP90.7, HSP90.3, HSP90.2, ERD1, FKB70, and ROC1), five in redox regulation (PRX2B, GPX6, MDAR3, MDARP, and Y4967), five in primary metabolism (TBA6, SPP2, PDX11, RR5, and RuBisCO activase (RCA)), and three in secondary metabolism (PR5, MYRO, and NMT2). All proteins belonging to the same group shared the same direction of change; the only exception was RCA. The proteins involved in protein folding and regulation were down-regulated indicating the inhibition of a plant defense response. Those involved in redox regulation were up-regulated, which may lead to an increase in tolerance as a result of a reduction in oxidation. Proteins involved in primary metabolism (except RCA) were inhibited while those involved in secondary metabolism were induced suggesting reallocation of resources with the host plant. These proteins will form the basis for future studies aimed at further understanding the mechanism underlying the host-adaptation capacity of B. tabaci.

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References

  • Alfenas-Zerbini P, Maia IG, Favaro RD, Cascardo JCM, Brommonschenkel SH, Zerbini FM (2009) Genome-wide analysis of differentially expressed genes during the early stages of tomato infection by a potyvirus. Mol Plant-Microbe Interact 22:352–361

    Article  PubMed  CAS  Google Scholar 

  • Andersson D, Chakrabarty R, Bejai S, Zhang JM, Rask L, Meijer J (2009) Myrosinases from root and leaves of Arabidopsis thaliana have different catalytic properties. Phytochemistry 70:1345–1354

    Article  PubMed  CAS  Google Scholar 

  • Andreasson E, Jorgensen LB, Hoglund AS, Rask L, Meijer J (2001) Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus. Plant Physiol 127:1750–1763

    Article  PubMed  CAS  Google Scholar 

  • Barth C, Jander G (2006) Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant J 46:549–562

    Article  PubMed  CAS  Google Scholar 

  • Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory—primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530

    Article  CAS  Google Scholar 

  • Bi CL, Chen F, Jackson L, Gill BS, Li WL (2010) Expression of lignin biosynthetic genes in wheat during development and upon infection by fungal pathogens. Plant Mol Biol Rep 29:149–161

    Article  Google Scholar 

  • Brehelin C, Meyer EH, de Souris JP, Bonnard G, Meyer Y (2003) Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: similar sequences for divergent gene expression, protein localization, and activity. Plant Physiol 132:2045–2057

    Article  PubMed  CAS  Google Scholar 

  • Byrne DN, Bellows TS (1991) Whitefly biology. Annu Rev Entomol 36:431–457

    Article  Google Scholar 

  • Chu CC, Margosan DA, Buckner JS, Freeman TP, Henneberry TJ (2007) Bemisia tabaci (Hemiptera: Aleyrodidae) nymphal feeding in cotton (Gossypium hirsutum) leaves. Insect Sci 14:375–381

    Article  Google Scholar 

  • De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ 32:1548–1560

    Article  PubMed  Google Scholar 

  • De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Interact 18:923–937

    Article  PubMed  Google Scholar 

  • De Vos M, Kim JH, Jander G (2007) Biochemistry and molecular biology of Arabidopsis-aphid interactions. Bioessays 29:871–883

    Article  PubMed  Google Scholar 

  • Estrada-Hernandez MG, Valenzuela-Soto JH, Ibarra-Laclette E, Delano-Frier JP (2009) Differential gene expression in whitefly Bemisia tabaci-infested tomato (Solanum lycopersicum) plants at progressing developmental stages of the insect's life cycle. Physiol Plant 137:44–60

    Article  CAS  Google Scholar 

  • Fridovich I (1978) Biology of oxygen radicals. Science 201:875–880

    Article  PubMed  CAS  Google Scholar 

  • Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type Ш effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284–289

    Article  PubMed  CAS  Google Scholar 

  • Garavaglia BS, Garofalo CG, Orellano EG, Ottado J (2009) HSP70 and HSP90 expression in citrus and pepper plants in response to Xanthomonas axonopodis pv. Citri. Eur J Plant Pathol 123:91–97

    Article  CAS  Google Scholar 

  • Giri AP, Wunsche H, Mitra S, Zavala JA, Muck A, Svatos A, Baldwin IT (2006) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VП. Changes in the plant's proteome. Plant Physiol 142:1621–1641

    Article  PubMed  CAS  Google Scholar 

  • Gorovits R, Akad F, Beery H, Vidavsky F, Mahadav A, Czosnek H (2007) Expression of stress-response proteins upon whitefly-mediated inoculation of tomato yellow leaf curl virus in susceptible and resistant tomato plants. Mol Plant-Microbe Interact 20:1376–1383

    Article  PubMed  CAS  Google Scholar 

  • Griffin TJ, Gygi SP, Ideker T, Rist B, Eng J, Hood L, Aebersold R (2002) Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol Cell Proteomics 1:323–333

    Article  PubMed  CAS  Google Scholar 

  • Halitschke R, Gase K, Hui DQ, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 131:1894–1902

    Article  PubMed  CAS  Google Scholar 

  • Haukioja E, Ruohomaki K, Suomela J, Vuorisalo T (1991) Nutritional quality as a defense against herbivores. For Ecol Manage 39:237–245

    Article  Google Scholar 

  • Heil M, Hilpert A, Kaiser W, Linsenmair KE (2000) Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? J Ecol 88:645–654

    Article  CAS  Google Scholar 

  • Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83

    Article  PubMed  CAS  Google Scholar 

  • Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, Shirasu K, Dangl JL (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 22:5679–5689

    Article  PubMed  CAS  Google Scholar 

  • Hui DQ, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131:1877–1893

    Article  PubMed  CAS  Google Scholar 

  • Imlay JA, Chin SM, Linn S (1988) Toxic DNA damage by hydrogen-peroxide through the fenton reaction in vivo and in vitro. Science 240:640–642

    Article  PubMed  CAS  Google Scholar 

  • Kempema LA, Cui XP, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143:849–865

    Article  PubMed  CAS  Google Scholar 

  • Kent C (1995) Eukaryotic phospholipid biosynthesis. Annu Rev Biochem 64:315–343

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019

    Article  PubMed  CAS  Google Scholar 

  • Krishna P, Gloor G (2001) The HSP90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246

    Article  PubMed  CAS  Google Scholar 

  • Kusnierczyk A, Winge P, Midelfart H, Armbruster WS, Rossiter JT, Bones AM (2007) Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. J Exp Bot 58:2537–2552

    Article  PubMed  CAS  Google Scholar 

  • Leitner M, Boland W, Mithofer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 167:597–606

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Xie QG, Smith-Becker J, Navarre DA, Kaloshian I (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol Plant-Microbe Interact 19:655–664

    Article  PubMed  CAS  Google Scholar 

  • Liu YH, Li HY, Shi YS, Song YC, Wang TY, Li Y (2009) A maize early responsive to dehydration gene, ZmERD4, provides enhanced drought and salt tolerance in Arabidopsis. Plant Mol Biol Rep 27:542–548

    Article  CAS  Google Scholar 

  • Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, Rathjen JP, Bendahmane A, Day L, Baulcombe DC (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22:5690–5699

    Article  PubMed  CAS  Google Scholar 

  • Luo C, Yao Y, Wang RJ, Yan FM, Hu DX, Zhang ZL (2002) The use of mitochondrial cytochrome oxidase I (mtCOI) gene sequences for the identification of biotypes of Bemisia tabaci (Gennadius) in China. Acta Entomologica Sinica 45:759–763

    CAS  Google Scholar 

  • Matyssek R, Agerer R, Ernst D, Munch JC, Osswald W, Pretzsch H, Priesack E, Schnyder H, Treutter D (2005) The plant's capacity an regulating resource demand. Plant Biol 7:560–580

    Article  PubMed  CAS  Google Scholar 

  • Mayer RT, McCollum TG, McDonald RE, Polston JE, Doostdar H (1995) Bemisia feeding induces pathogenesis-related proteins in tomato. In: Gerling D, Mayer RT (eds) Bemisia: 1995. Taxonomy, biology, damage, control and management. Andover Intercept Ltd, Hampshire, pp 179–188

    Google Scholar 

  • Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399

    Article  PubMed  CAS  Google Scholar 

  • Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162

    Article  PubMed  CAS  Google Scholar 

  • Mittapalli O, Neal JJ, Shukle RH (2007) Antioxidant defense response in a galling insect. Proc Natl Acad Sci USA 104:1889–1894

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

    Article  PubMed  CAS  Google Scholar 

  • Mou ZL, Wang XQ, Fu ZM, Dai Y, Han C, Ouyang J, Bao F, Hu YX, Li JY (2002) Silencing of phosphoethanolamine n-methyltransferase results in temperature-sensitive male sterility and salt hypersensitivity in Arabidopsis. Plant Cell 14:2031–2043

    Article  PubMed  CAS  Google Scholar 

  • Nair RA, Kiran AG, Sivakumar KC, Thomas G (2010) Molecular characterization of an oomycete-responsive PR-5 protein gene from Zingiber zerumbet. Plant Mol Biol Rep 28:128–135

    Article  CAS  Google Scholar 

  • Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Routhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379

    Article  PubMed  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (pr) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507

    CAS  Google Scholar 

  • Ohta M, Sugita M, Sugiura M (1995) 3 types of nuclear genes encoding chloroplast RNA-binding proteins (CP29, CP31 and CP33) are present in Arabidopsis thaliana - presence of CP31 in chloroplasts and its homolog in nuclei/cytoplasms. Plant MolBiol 27:529–539

    CAS  Google Scholar 

  • Portis AR (2003) RuBisCO activase—RuBisCO's catalytic chaperone. Photosynth Res 75:11–27

    Article  PubMed  CAS  Google Scholar 

  • Puthoff DP, Holzer FM, Perring TM, Walling LL (2010) Tomato pathogenesis-related protein genes are expressed in response to Trialeurodes vaporariorum and Bemisia tabaci biotype B feeding. J Chem Ecol 36:1271–1285

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88

    Article  PubMed  CAS  Google Scholar 

  • Shi R, Kumar C, Zougman A, Zhang Y, Podtelejnikov A, Cox J, Wisniewski JR, Mann M (2007) Analysis of the mouse liver proteome using advanced mass spectrometry. J Proteome Res 6:2963–2972

    Article  PubMed  CAS  Google Scholar 

  • Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270

    Article  PubMed  CAS  Google Scholar 

  • Takahashi A, Casais C, Ichimura K, Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100:11777–11782

    Article  PubMed  CAS  Google Scholar 

  • Thao NP, Chen L, Nakashima A, Hara SI, Umemura K, Takahashi A, Shirasu K, Kawasaki T, Shimamoto K (2007) RAR1 and HSP90 form a complex with rac/rop gtpase and function in innate-immune responses in rice. Plant Cell 19:4035–4045

    Article  PubMed  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genet 37:1130–1134

    Article  PubMed  CAS  Google Scholar 

  • Uknes S, Mauchmani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired-resistance in Arabidopsis. Plant Cell 4:645–656

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela-Soto JH, Estrada-Hernandez MG, Ibarra-Laclette E, Delano-Frier JP (2010) Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development. Planta 231:397–410

    Article  PubMed  CAS  Google Scholar 

  • van de Ven WTG, LeVesque CS, Perring TM, Walling LL (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12:1409–1423

    PubMed  Google Scholar 

  • Vigers AJ, Wiedemann S, Roberts WK, Legrand M, Selitrennikoff CP, Fritig B (1992) Thaumatin-like pathogenesis-related proteins are antifungal. Plant Sci 83:155–161

    Article  CAS  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

  • Waltherlarsen H, Brandt J, Collinge DB, Thordalchristensen H (1993) A pathogen-induced gene of barley encodes a HSP90 homolog showing striking similarity to vertebrate forms resident in the endoplasmic-reticulum. Plant Mol Biol 21:1097–1108

    Article  CAS  Google Scholar 

  • Wang BC, Pan YH, Meng DZ, Zhu YX (2006) Identification and quantitative analysis of significantly accumulated proteins during the Arabidopsis seedling de-etiolation process. J Integr Plant Biol 48:104–113

    Article  CAS  Google Scholar 

  • Weaver LM, Gan SS, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469

    Article  PubMed  CAS  Google Scholar 

  • Weaver LM, Froehlich JE, Amasino RM (1999) Chloroplast-targeted ERD1 protein declines but its mRNA increases during senescence in Arabidopsis. Plant Physiol 119:1209–1216

    Article  PubMed  CAS  Google Scholar 

  • Xue JP, Jorgensen M, Pihlgren U, Rask L (1995) The myrosinase gene family in Arabidopsis-thaliana—gene organization, expression and evolution. Plant Mol Biol 27:911–922

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Liu P, Liu YS, Wang QS, Tong YP, Ji JG (2006) Proteomic analysis of rat pheochromocytoma pc12 cells. Proteomics 6:2982–2990

    Article  PubMed  CAS  Google Scholar 

  • Yang B, Rahman MH, Liang Y, Shah S, Kav NNV (2010) Characterization of defense signaling pathways of Brassica napus and Brassica carinata in response to Sclerotinia sclerotiorum challenge. Plant Mol Biol Rep 28:253–263

    Article  CAS  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  PubMed  CAS  Google Scholar 

  • Zhang PJ, Zheng SJ, van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in lima bean. Proc Natl Acad Sci USA 106:21202–21207

    Article  PubMed  CAS  Google Scholar 

  • Zhang JH, Sun LW, Liu LL, Lian J, An SL, Wang X, Zhang J, Jin JL, Li SY, Xi JH (2010) Proteomic analysis of interactions between the generalist herbivore Spodoptera exigua (Lepidoptera: Noctuidae) and Arabidopsis thaliana. Plant Mol Biol Rep 28:324–333

    Article  CAS  Google Scholar 

  • Zhang H, Hu YA, Wang CY, Ji WQ (2011) Gene expression in wheat induced by inoculation with Puccinia striiformis West. Plant Mol Biol Rep 29:458–465

    Article  Google Scholar 

  • Zhao RM, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J, Boone C, Emili A, Houry WA (2005) Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the HSP90 chaperone. Cell 120:715–727

    Article  PubMed  CAS  Google Scholar 

  • Zhu S, Saski CA, Boerma HR, Tomkins JP, All JN, Parrott WA (2009) Construction of a BAC library for a defoliating insect-resistant soybean and identification of candidate clones using a novel approach. Plant Mol Biol Rep 27:229–235

    Article  CAS  Google Scholar 

  • Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of Sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the project of National Natural Science Foundation of China (no. 30771381 and 30571219), the project of Ministry of Education (no. 20050001038), and the grant from the National Program of Development of Transgenic New Species of China (no. 2008ZX08012-005 and 2008ZX08011-006 and 2009ZX08012-007B). We especially thank Prof. Paul De Barro from CSIRO Entomology of Australia and Prof. Linda Walling from University of California, Riverside for revising the manuscript.

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  1. College of Life Sciences, Peking University, Beijing, 100871, China

    Haidi Yin, Fengming Yan, Jianguo Ji, Rongjiang Wang & Chongren Xu

  2. Institute of Chemical Ecology, Henan Agricultural University, Zhengzhou, Henan, 450002, China

    Fengming Yan

  3. Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Yinxin Li

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  1. Haidi Yin
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Correspondence to Rongjiang Wang or Chongren Xu.

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Yin, H., Yan, F., Ji, J. et al. Proteomic analysis of Arabidopsis thaliana leaves infested by tobacco whitefly Bemisia tabaci (Gennadius) B biotype. Plant Mol Biol Rep 30, 379–390 (2012). https://doi.org/10.1007/s11105-011-0351-0

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