iTRAQ-based proteomic analysis of resistant Nicotiana tabacum in response to Bemisia tabaci infestation

Abstract

Bemisia tabaci is a pest that poses a significant threat to the survival of Nicotiana tabacum and leads to decreased production and economic losses. However, it is still unknown whether proteomic changes occur in resistant N. tabacum in response to B. tabaci stresses. In the present study, iTRAQ was performed to unmask the regulating networks mediated by candidate proteins involved in resistance against B. tabaci. A total of 357 differentially accumulated proteins (DAPs) responsible for B. tabaci infestation were identified, including 178 upregulated and 179 downregulated proteins. The majority of DAPs were involved in the regulation of ROS production, cell expansion, citrate cycle (TCA cycle), photosynthesis, carbon fixation, and metabolic pathways. Moreover, the expression patterns of several genes encoding DAPs were validated by qRT-PCR. Our results indicate these proteins play a significant role in the resistance of N. tabacum against B. tabaci infestation. These findings also provide a valuable proteomic resource for the elucidation of the mechanism of resistance against B. tabaci.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370(6491):621–628

    CAS  PubMed  Article  Google Scholar 

  2. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8(1):15–19

    CAS  PubMed  Article  Google Scholar 

  3. Allison SD, Schultz JC (2004) Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in northern red oak (Quercus rubra L.). J Chem Ecol 30(7):1363–1379

    CAS  PubMed  Article  Google Scholar 

  4. Alon M, Malka O, Eakteiman G, Elbaz M, Moyal Ben Zvi M, Vainstein A, Morin S (2013) Activation of the Phenylpropanoid pathway in Nicotiana tabacum improves the performance of the whitefly Bemisia tabaci via reduced jasmonate signaling. PLoS ONE 8(10):e76619

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  6. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Belefant-Miller H, Porter DR, Pierce ML, Mort AJ (1994) An early indicator of resistance in barley to Russian wheat aphid. Plant Physiol 105(4):1289–1294

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580

    CAS  PubMed  Article  Google Scholar 

  9. Boyer PD (1997) The ATP synthase—a splendid molecular machine. Annu Rev Biochem 66:717–749

    CAS  PubMed  Article  Google Scholar 

  10. Boykin LM (2014) Bemisia tabaci nomenclature: lessons learned. Pest Manag Sci 70(10):1454–1459

    CAS  PubMed  Article  Google Scholar 

  11. Butlerjr GD, Henneberry TJ, Clayton TE (1983) Bemisia tabaci (Homoptera: Aleyrodidae): development, oviposition, and longevity in relation to temperature. Ann Entomol Soc Am 76(2):310–313

    Article  Google Scholar 

  12. Chu HA, Chiu YF (2015) The roles of cytochrome b 559 in assembly and photoprotection of Photosystem II revealed by site-directed mutagenesis studies. Front Plant Sci 6:1261

    PubMed  Article  Google Scholar 

  13. Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, Storme V, Clement L, Gonzalez N, Inze D (2015) Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol 167(3):800–816

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. Collinson IR, van Raaij MJ, Runswick MJ, Fearnley IM, Skehel JM, Orriss GL, Miroux B, Walker JE (1994) ATP synthase from bovine heart mitochondria. In vitro assembly of a stalk complex in the presence of F1-ATPase and in its absence. J Mol Biol 242(4):408–421

    CAS  PubMed  Google Scholar 

  15. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. De Barro PJ, Driver F, Trueman JW, Curran J (2000) Phylogenetic relationships of world populations of Bemisia tabaci (Gennadius) using ribosomal ITS1. Mol Phylogenet Evol 16(1):29–36

    PubMed  Article  CAS  Google Scholar 

  17. De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, Van Loon LC, Pieterse CM (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142(1):352–363

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  18. 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(3):1576–1586

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Ding A, Marowa P, Kong Y (2016) Genome-wide identification of the expansin gene family in tobacco (Nicotiana tabacum). Mol Genet Genomics 291(5):1891–1907

    CAS  PubMed  Article  Google Scholar 

  20. Ifuku K, Noguchi T (2016) Structural coupling of extrinsic proteins with the oxygen-evolving center in photosystem II. Front Plant Sci 7:84

    PubMed  PubMed Central  Article  Google Scholar 

  21. Ifuku K, Ido K, Sato F (2011) Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex. J Photochem Photobiol B 104(1–2):158–164

    CAS  PubMed  Article  Google Scholar 

  22. Junge W, Sielaff H, Engelbrecht S (2009) Torque generation and elastic power transmission in the rotary F(O)F(1)-ATPase. Nature 459(7245):364–370

    CAS  PubMed  Article  Google Scholar 

  23. Karatolos N, Denholm I, Williamson M, Nauen R, Gorman K (2010) Incidence and characterisation of resistance to neonicotinoid insecticides and pymetrozine in the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). Pest Manag Sci 66(12):1304–1307

    CAS  PubMed  Article  Google Scholar 

  24. Koiwa H, Kato H, Nakatsu T, Oda J, Yamada Y, Sato F (1997) Purification and characterization of tobacco pathogenesis-related protein PR-5d, an antifungal thaumatin-like protein. Plant Cell Physiol 38(7):783–791

    CAS  PubMed  Article  Google Scholar 

  25. Kuroda H, Kodama N, Sun XY, Ozawa S, Takahashi Y (2014) Requirement for Asn298 on D1 protein for oxygen evolution: analyses by exhaustive amino acid substitution in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol 55(7):1266–1275

    CAS  PubMed  Article  Google Scholar 

  26. Li N, Zhang SJ, Zhao Q, Long Y, Guo H, Jia HF, Yang YX, Zhang HY, Ye XF, Zhang ST (2018) Overexpression of tobacco GCN2 stimulates multiple physiological changes associated with stress tolerance. Front Plant Sci 9:725

    PubMed  PubMed Central  Article  Google Scholar 

  27. Liang P, Tian YA, Biondi A, Desneux N, Gao XW (2012) Short-term and transgenerational effects of the neonicotinoid nitenpyram on susceptibility to insecticides in two whitefly species. Ecotoxicology 21(7):1889–1898

    CAS  PubMed  Article  Google Scholar 

  28. Liu HW, Liang CQ, Liu PF, Luo LX, Li JQ (2015) Quantitative proteomics identifies 38 proteins that are differentially expressed in cucumber in response to cucumber green mottle mosaic virus infection. Virol J 12:216

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408

    CAS  PubMed  Article  Google Scholar 

  30. Lu J, Du ZX, Kong J, Chen LN, Qiu YH, Li GF, Meng XH, Zhu SF (2012) Transcriptome analysis of Nicotiana tabacum infected by Cucumber mosaic virus during systemic symptom development. PLoS One 7(8):e43447

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. Mayer RT, Inbar M, McKenzie CL, Shatters R, Borowicz V, Albrecht U, Powell CA, Doostdar H (2002) Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Arch Insect Biochem Physiol 51(4):151–169

  32. Menz RI, Walker JE, Leslie AG (2001) Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106(3):331–341

    CAS  PubMed  Article  Google Scholar 

  33. Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125(4):1558–1566

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2002) Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of two genes encoding extrinsic 33-kDa proteins in photosystem II. FEBS Lett 523(1–3):138–142

    CAS  PubMed  Article  Google Scholar 

  35. Nadimpalli R, Yalpani N, Johal GS, Simmons CR (2000) Prohibitins, stomatins, and plant disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. J Biol Chem 275(38):29579–29586

    CAS  PubMed  Article  Google Scholar 

  36. Park YB, Cosgrove DJ (2012) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 158(1):465–475

    CAS  PubMed  Article  Google Scholar 

  37. Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10(9):1571–1580

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. Plader W, Yukawa Y, Sugiura M, Malepszy S (2007) The complete structure of the cucumber (Cucumis sativus L.) chloroplast genome: its composition and comparative analysis. Cell Mol Biol Lett 12(4):584–594

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. Ponstein AS, Bres-Vloemans SA, Sela-Buurlage MB, van den Elzen PJ, Melchers LS, Cornelissen BJ (1994) A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity. Plant Physiol 104(1):109–118

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. 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(11):1271–1285

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Rostoks N, Schmierer D, Kudrna D, Kleinhofs A (2003) Barley putative hypersensitive induced reaction genes: genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theor Appl Genet 107(6):1094–1101

    CAS  PubMed  Article  Google Scholar 

  42. Sanchez-Hernandez C, Lopez MG, Delano-Frier JP (2006) Reduced levels of volatile emissions in jasmonate-deficient spr2 tomato mutants favour oviposition by insect herbivores. Plant Cell Environ 29(4):546–557

    CAS  PubMed  Article  Google Scholar 

  43. Thakur N, Upadhyay SK, Verma PC, Chandrashekar K, Tuli R, Singh PK (2014) Enhanced whitefly resistance in transgenic tobacco plants expressing double stranded RNA of v-ATPase A gene. PLoS ONE 9(3):e87235

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  44. Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance and interplant signal transfer in Alnusglutinosa. Biochem Syst Ecol 29(10):1025–1047

    CAS  Article  Google Scholar 

  45. Walker JE, Dickson VK (2006) The peripheral stalk of the mitochondrial ATP synthase. Biochim Biophys Acta 1757(5–6):286–296

    CAS  PubMed  Article  Google Scholar 

  46. Westhuizen AJ, Qian XM, Botha AM (1998a) Differential induction of apoplastic peroxidase and chitinase activities in susceptible and resistant wheat cultivars by Russian wheat aphid infestation. Plant Cell Rep 18(1–2):132–137

    Article  Google Scholar 

  47. Westhuizen AJ, Qian XM, Botha AM (1998b) β-1,3-glucanases in wheat and resistance to the Russian wheat aphid. Physiol Plantarum 103(1):125–131

    Article  Google Scholar 

  48. Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6(5):359–362

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24

    CAS  PubMed  Article  Google Scholar 

  50. Xu HX, Hong Y, Zhang MZ, Wang YL, Liu SS, Wang XW (2015) Transcriptional responses of invasive and indigenous whiteflies to different host plants reveal their disparate capacity of adaptation. Sci Rep 5:10774

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Yamori W, Takahashi S, Makino A, Price GD, Badger MR, von Caemmerer S (2011) The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol 155(2):956–962

    CAS  PubMed  Article  Google Scholar 

  52. Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 280(16):16170–16174

    CAS  PubMed  Article  Google Scholar 

  53. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143(2):866–875

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. Zhang SZ, Zhang F, Zhen HB (2008) Enhancement of phenylalanine ammonia lyase, polyphenoloxidase, and peroxidase in cucumber seedlings by Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) infestation. Agric Sci China 7(1):82–87

    CAS  Article  Google Scholar 

  55. Zhao H, Zhang X, Xue M, Zhang X (2015) Feeding of whitefly on tobacco decreases aphid performance via increased salicylate signaling. PLoS ONE 10(9):e0138584

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  56. Zong N, Wang CZ (2007) Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226(1):215–224

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the Natural Science Foundation of Henan Province (CN) (No. 182300410065), and the science and technology key projects of China tobacco corporation (No. 110201202003).

Author information

Affiliations

Authors

Contributions

YL conducted the experiments; SZ and NL prepared figures; DC prepared the samples; HJ and HZ discussed the data; SZ and YY designed the experiments and wrote the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Song-tao Zhang or Yong-xia Yang.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Additional information

Handling Editor: Ritu Chaudhary.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 75 KB)

Supplementary material 2 (XLSX 69 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, S., Long, Y., Zhang, S. et al. iTRAQ-based proteomic analysis of resistant Nicotiana tabacum in response to Bemisia tabaci infestation. Arthropod-Plant Interactions 13, 505–516 (2019). https://doi.org/10.1007/s11829-018-9662-5

Download citation

Keywords

  • Nicotiana tabacum
  • Bemisia tabaci
  • iTRAQ
  • Proteomic analysis
  • Defence mechanism