Skip to main content

Advertisement

Log in

Proteomic analysis of responsive root proteins of Fusarium oxysporum-infected watermelon seedlings

  • Regular article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Fusarium oxysporum is a causal disease that threatens watermelon production, but little information on the molecular mechanisms involved in host defense is available. To understand the defense response, a proteome-level changes that occur in watermelon roots during F. oxysporum infection were investigated.

Methods

We utilized two-dimensional gel electrophoresis (2-DE) to compare changes in the root proteome profiles and validated their expression using real-time PCR.

Results

A total of 690 spots were detected, and 32 proteins had significant changes in abundance and were further identified by mass spectrometry. These proteins were mainly involved in metabolism, stress and defense and amino acid biosynthesis. RT-PCR analysis revealed that transcripts corresponding to the nine randomly selected proteins could be significantly induced, their expression patterns were consistent with the proteomic results except for Apx and Tdh. The involvement of these proteins in regulating watermelon response against F. oxysporum is discussed.

Conclusions

The reprogrammed proteins were involved in several biological processes, which indicates that watermelon can directly alter the abundance of these proteins to establish a defense response. This work helps us understand the basic processes during the watermelon-F. oxysporum interaction and may contribute to improve resistance breeding toward this pathogen.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Afroz A, Ali GM, Mir A, Komatsu S (2011) Application of proteomics to investigate stress induced proteins for improvement in crop protection. Plant Cell Rep 30:745–763

    Article  CAS  PubMed  Google Scholar 

  • Baayen RP, Van Eijk C, Elgersma DM (1989) Histology of roots of resistant and susceptible carnation cultivars from soil infested with Fusarium oxysporum f. Sp. dianthi. Eur J Plant Pathol 95:3–13

    Google Scholar 

  • Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482

    Article  PubMed  PubMed Central  Google Scholar 

  • Bian YW, Lv DW, Cheng ZW, Gu AQ, Cao H, Yan YM (2015) Integrative proteome analysis of Brachypodium distachyon roots and leaves reveals a synergetic responsive network under H2O2 stress. J Proteome 128:388–402

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Carlsen SCK, Understrup A, Fomsgaard IS, Mortensen AG, Ravnskov S (2008) Flavonoids in roots of white clover: interaction of arbuscular mycorrhizal fungi and a pathogenic fungus. Plant Soil 302:33–43

    Article  CAS  Google Scholar 

  • Casati P, Drincovich MF, Edwards GE, Andreo CS (1999) Malate metabolism by NADP-malic enzyme in plant defense. Photosynth Res 61:99–105

    Article  CAS  Google Scholar 

  • Chang PFL, Hsu CC, Lin YH, Chen KS, Huang JW, Liou TD (2008) Histopathology comparison and phenylalanine ammonia lyase (PAL) gene expressions in fusarium wilt infected watermelon. Aust J Agric Res 59:1146–1155

    Article  CAS  Google Scholar 

  • Cipriano AKAL, Gondim DMF, Vasconcelos IM, Martins JAM, Moura AA, Moreno FB et al (2015) Proteomic analysis of responsive stem proteins of resistant and susceptible cashew plants after Lasiodiplodia theobromae infection. J Proteome 113:90–109

    Article  CAS  Google Scholar 

  • De Bruyne L, Höfte M, De Vleesschauwer D (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Mol Plant 7:943–959

    Article  CAS  PubMed  Google Scholar 

  • Ding W, Smulan LJ, Hou NS, Taubert S, Watts JL, Walker AK (2015) s-Adenosylmethionine levels govern innate immunity through distinct m ethylation-dependent pathways. Cell Metab 22:633–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández-garcía N, Carvajal M, Olmos E (2004) Graft union formation in tomato plants: peroxidase and catalase involvement. Ann Bot 93:53–60

    Article  PubMed  PubMed Central  Google Scholar 

  • Garrett SD (1970) Pathogenic root-infecting fungi. University Press, Cambridge

    Google Scholar 

  • Guo SG, Zhang JG, Sun HH, Salse J, Lucas WJ, Zhang HY et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58

    Article  CAS  PubMed  Google Scholar 

  • Heyno E, Alkan N, Fluhr R (2013) A dual role for plant quinone reductases in host-fungus interaction. Physiol Plantaru 149:340–353

    CAS  Google Scholar 

  • Hinault MP, Ben-Zvi A, Goloubinoff P (2006) Chaperones and proteases: cellular fold-controlling factors of proteins in neurodegenerative diseases and aging. J Mol Neurosci 30:249–265

    Article  CAS  PubMed  Google Scholar 

  • Imahori Y (2014) Role of ascorbate peroxidase in postharvest treatments of horticultural crops. P. Ahmad (Ed.), Oxidative damage to plants: antioxidant networks and signaling, Elsevier Inc., San Diego, pp 425-451

  • Jiang Y, Chen X, Ding X, Wang Y, Chen Q, Song WY (2013) The XA21 binding protein XB25 is required for maintaining XA21-mediated disease resistance. Plant J 73:814–823

    Article  CAS  PubMed  Google Scholar 

  • Kadota Y, Shirasu K, Guerois R (2010) NLR sensors meet at the SGT1-HSP90 crossroad. Trends Biochem Sci 35:199–207

    Article  CAS  PubMed  Google Scholar 

  • King SR, Davis AR, Liu WG, Levi A (2008) Grafting for disease resistance. Hortscience 43:1673–1676

    Google Scholar 

  • Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M et al (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci U S A 103:18008–18013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Bonawitz ND, Weng JK, Chapple C (2010) The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. Plant Cell 22:1620–1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JHG, America AHP et al (2013) Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci U S A 110:10010–10015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Bruch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279:2101–2108

    Article  CAS  PubMed  Google Scholar 

  • Liu YM, Du HM, He XX, Huang BR, Wang ZL (2012) Identification of differentially expressed salt-responsive proteins in roots of two perennial grass species contrasting in salinity tolerance. J Plant Physiol 169:117–126

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • López-Gresa MP, Maltese F, Bellés JM, Conejero V, Kim HK, Choi YH et al (2009) Metabolic response of tomato leaves upon different plant-pathogen interactions. Phytochem Anal 21:89–94

    Article  Google Scholar 

  • Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–272

    Article  CAS  PubMed  Google Scholar 

  • Martyn RD (1996) Fusarium wilt of watermelon. In: Zither TA, Hopkins DL, Thomas CA (eds) Compendium of cucurbit diseases. The American Phytopathology Society, St. Paul, MN, pp 13–14

    Google Scholar 

  • Mazel A, Leshem Y, Tiwari BS, Levine A (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol 134:118–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meru G, McGregor C (2016) Genotyping by sequencing for SNP discovery and genetic mapping of resistance to race 1 of Fusarium oxysporum in watermelon. Sci Hortic 209:31–40

    Article  CAS  Google Scholar 

  • Mhamdi A, Noctor G (2015) Analysis of the roles of the Arabidopsis peroxisomal isocitrate dehydrogenase in leaf metabolism and oxidative stress. Environ Exp Bot 114:22–29

    Article  CAS  Google Scholar 

  • Miernyk JA, Thelen JJ (2008) Biochemical approaches for discovering protein-protein interactions. Plant J 53:597–609

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Zilinskas BA (2004) Activated oxygen species in multiple stress situations and protective systems. In: Sandermann H (ed) Molecular ecotoxicology of plants, Springer. Berlin Heidelberg, New York, pp 51–73

    Chapter  Google Scholar 

  • Mohr U, Lange J, Boller T, Wiemken A, Vögeli-Lange R (1998) Plant defense genes are induced in the pathogenic interaction between bean roots and Fusarium solani, but not in the symbiotic interaction with the arbuscular mycorrhizal fungus Glomus mosseae. New Phytol 138:589–598

    Article  CAS  Google Scholar 

  • Moreira RC, Lima JS, Silva LGC, Cardoso JE (2013) Resistance to gummosis in wild cashew genotypes in northern Brazil. Crop Prot 52:10–13

    Article  Google Scholar 

  • Mourad G, King J (1995) L-O-Methylthreonine-resistant mutant of Arabidopsis defective in isoleucine feedback regulation. Plant Physiol 107:43–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller-Uri F, Parthier B, Nover L (1988) Jasmonate-induced alteration of gene expression in barley leaf segments analyzed by in-vivo and in-vitro protein synthesis. Planta 176:241–247

    Article  CAS  PubMed  Google Scholar 

  • Münzenberger B, Otter T, Wüstrich D, Polle A (1997) Peroxidase and laccase activities in mycorrhizal and non-mycorrhizal roots of Norway spruce (Picea abies L.) and larch (Larix decidua). Can J Bot 75:932–938

    Article  Google Scholar 

  • Navarro L, Bari R, Achard P, Lisón P, Nemri A, Harberd NP et al (2008) DELLAs control plant immune responses by modulating the balance and salicylic acid signaling. Curr Biol 18:650–655

    Article  CAS  PubMed  Google Scholar 

  • Ochi A, Hori H (2007) Hydroxyl radical probing of rRNA (Gm18) methyltransferase [TrmH]-AdoMet-artificial rRNA ternary complex. Nucleic Acids Symp Ser 51:373–374

    Article  Google Scholar 

  • Parrott DL, Huang L, Fischer AM (2016) Downregulation of a barley (Hordeum vulgare) leucine-rich repeat, non-arginine-aspartate receptor-like protein kinase reduces expression of numerous genes involved in plant pathogen defense. Plant Physiol Bioc 100:130–140

    Article  CAS  Google Scholar 

  • Patridge EV, Ferry JG (2006) WrbA from Escherichia coli and Archaeoglobus fulgidus is an NAD (P) H: Quinone oxidoreductase. J Bacteriol 188:3498–3506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piterková J, Luhová L, Mieslerová B, Lebeda A, Petřivalský M (2013) Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Sci 207:57–65

    Article  PubMed  Google Scholar 

  • Roje S (2006) S-adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698

    Article  CAS  PubMed  Google Scholar 

  • Romeo S, Trupiano D, Ariani A, Renzone G, Scippa GS, Scaloni A et al (2014) Proteomic analysis of Populus × euramericana (clone I-214) roots to identify key factors involved in zinc stress response. J Plant Physiol 171:1054–1063

    Article  CAS  PubMed  Google Scholar 

  • Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJM et al (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21:2829–2843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid KM, Patterson GW (1988) Effects of cyclopropenoid fatty acids on fungal growth and lipid composition. Lipids 23:248–252

    Article  CAS  PubMed  Google Scholar 

  • Shibata Y, Kawakita K, Takemoto D (2011) SGT1 and HSP90 are essential for age-related non-host resistance of Nicotiana benthamiana against the oomycete pathogen Phytophthora infestans. Physiol Mol Plant 75:120–128

    Article  CAS  Google Scholar 

  • Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164

    Article  CAS  PubMed  Google Scholar 

  • Sinha R, Chattopadhyay S (2011) Changes in the leaf proteome profile of Mentha arvensis in response to Alternaria alternate infection. J Proteome 74:327–336

    Article  CAS  Google Scholar 

  • Stenlid MH, Ahlsson F, Forslund A, von Döbeln U, Gustafsson J (2014) Energy substrate metabolism in pyruvate dehydrogenase complex deficiency. J Pediatr Endocrinol Metab 27:1059–1064

    CAS  PubMed  Google Scholar 

  • Tena G, Boudsocq M, Sheen J (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14:519–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147

    Article  CAS  Google Scholar 

  • Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL et al (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635–3646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang YJ, Wang LP, Tian J, Li J, Sun J, He LZ et al (2012) Proteomic study participating the enhancement of growth and salt tolerance of bottle gourd rootstock-grafted watermelon seedlings. Plant Physiol Bioc 58:54–65

    Article  CAS  Google Scholar 

  • Yoshimura K, Masuda A, Kuwano M, Yokota A, Akashi K (2008) Programmed proteome response for drought avoidance/tolerance in the root of a C3 xerophyte (wild watermelon) under water deficits. Plant Cell Physiol 49:226–241

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Xu JH, Liu G, Yao XF, Li PF, Yang XP (2015a) Characterization of the watermelon seedling infection process by Fusarium oxysporum f.Sp. niveum. Plant Pathol 64:1076–1084

    Article  CAS  Google Scholar 

  • Zhang M, Yang XP, Xu JH, Liu G, Yao XF, Li PF (2015b) Physiological responses of watermelon grafted onto bottle gourd to Fusarium oxysporum f. Sp. niveum infection. Acta Hortic 1086:107–111

    Article  Google Scholar 

  • Zhao C, Smith EC, Whiteheart SW (2011) Requirements for the catylytic cycle of the N-ethylmaleimide-sensitive factor (NSF). Biochim Biophys Acta 1823:159–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou XG, Everts KL, Bruton BD (2010) Race 3, a new and highly virulent race of Fusarium oxysporum f. Sp. niveum causing fusarium wilt in watermelon. Plant Dis 94:92–98

    Article  Google Scholar 

  • Zvirin T, Herman R, Brotman Y, Denisov Y, Belausov E, Freeman S et al (2010) Differential colonization and defence responses of resistant and susceptible melon lines infected by Fusarium oxysporum race 1.2. Plant Pathol 59:576–585

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by National Industrial Technology System for Watermelon & Melon. Title: Breeding of Grafting Rootstocks for Watermelon & Melon (CARS-NO.26), and Jiangsu Provincial Support Program for Agriculture, 2015 to 2017. Title: Innovation and integrated application of commercial chain techniques of good product direct selling to e-commerce and store in Watermelon [CX(15)1018].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jinhua Xu.

Additional information

Responsible Editor: Stéphane Compant.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Xu, J., Liu, G. et al. Proteomic analysis of responsive root proteins of Fusarium oxysporum-infected watermelon seedlings. Plant Soil 422, 169–181 (2018). https://doi.org/10.1007/s11104-017-3294-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3294-x

Keywords

Navigation