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Journal of Plant Growth Regulation

, Volume 36, Issue 1, pp 96–105 | Cite as

Proteomic Analysis of Phloem Proteins Leads to the Identification of Potential Candidates for JA-Mediated RKN-Resistant Elements in Solanum lycopersicum

  • Wenchao Zhao
  • Jinghong Hao
  • Jiayi Xing
  • Rui Yang
  • Fukuan Zhao
  • Jianli Wang
  • Shaohui Wang
Article
  • 275 Downloads

Abstract

Tomato production has been severely affected by root-knot nematode (RKN) diseases, leading to huge economic losses in tomato cultivation, production, and processing. To gain insight into the signal mechanism of resistance to RKN (Meloidogyne incongnita), tomato lines with different endogenous jasmonic acid levels were inoculated with RKN, and the differential proteome of their phloem was analyzed with two-dimensional gel electrophoresis. Analysis of 1400 protein spots from each gel revealed 74 differentially expressed proteins, 30 of which were identifed via matrix-assisted laser-desorption ionization time-of-flight mass spectrometry (MALDI-TOF–MS). Among these 30, the abundance of 25 proteins was elevated in 35S::PS, and five proteins were not expressed in spr2. The total differentially expressed proteins were grouped into multiple functional categories, the largest of which was energy conversion (38 %). Furthermore, we proposed several candidates that might function as potential signal molecules under RKN stress and dissected the multiple roles of proteins related to photosynthesis and energy conversion. The mRNA levels of nine proteins associated with defense responses and energy metabolism were analyzed by qRT-PCR, and the expression levels of five were in line with the proteome data.

Keywords

Tomato Jasmonic acid Root-knot nematodes resistance Proteome Signal 

Notes

Acknowledgments

CM, spr2, and 35S::PS seeds were donated by Prof. Chuanyou Li from the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences. This work was supported by the Project of Great Wall Scholar, Beijing Municipal Commission of Education (CIT&TCD20130323) and the Modern Agricultural Industry Technology System of Beijing Innovation Team (BAIC01-2016).

Supplementary material

344_2016_9622_MOESM1_ESM.tif (522 kb)
Localization of identified spots on the master gel (TIFF 522 kb)
344_2016_9622_MOESM2_ESM.xlsx (11 kb)
Supplementary material 2 (XLSX 10 kb)
344_2016_9622_MOESM3_ESM.tif (828 kb)
Supplementary material 3 (TIFF 828 kb)

References

  1. Afzal AJ, Natarajan A, Saini N, Iqbal MJ, Geisler M, El Shemy HA, Mungur R, Willmitzer L, Lightfoot DA (2009) The nematode resistance allele at the rhg1 locus alters the proteome and primary metabolism of soybean roots. Plant Physiol 151:1264–1280CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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 72:248–254CrossRefPubMedGoogle Scholar
  3. Callahan FE, Jenkins JN, Creech RG, Lawrence GW (1997) Changes in cotton root proteins correlated with resistance to root knot nematode development. J Cotton Sci 1:38–47Google Scholar
  4. Carlson M (1998) Regulation of glucose utilization in yeast. Curr Opin Genet Dev 8:560–564CrossRefPubMedGoogle Scholar
  5. Cooper WR, Jia L, Goggin L (2005) Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. J Chem Ecol 31:1953–1967CrossRefPubMedGoogle Scholar
  6. Curtis D, Lehmann R, Zamore PD (1995) Translational regulation in development. Cell 81:171–178CrossRefPubMedGoogle Scholar
  7. de Moor C, Richter JD (2001) Translational control in vertbrate development. In: Etkin LD, Jeon KW (eds) Cell lineage specification and patterning of the embryo. Academic Press, San Diego, pp 567–608CrossRefGoogle Scholar
  8. Ding CK, Wang C, Gross KC, David LS (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214(6):895–901CrossRefPubMedGoogle Scholar
  9. Dropkin VH (1969) Cellular responses of plants to nematode infections. Annu Rev Phytopathol 7:101–122CrossRefGoogle Scholar
  10. Epstein PN, Boschero AC, Atwater I, Cai X, Overbeek PA (1992) Expression of yeast hexokinase in pancreatic β cells of transgenic mice reduces blood glucose, enhances insulin secretion, and decreases diabetes. Proc Natl Acad Sci USA 89:12038–12042CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fan JW, Hu CL, Zhang LN, Li ZL, Zhao FK, Wang SH (2015) Jasmonic acid mediates tomato’s response to root knot nematodes. J Plant Growth Regul 34:196–205CrossRefGoogle Scholar
  12. Faurobert M, Pelpoir E, Chab J (2007) Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. Methods Mol Biol 355:9–14PubMedGoogle Scholar
  13. Fedoroff NV (2002) RNA-binding proteins in plants: the tip of an iceberg? Curr Opin Plant Biol 5:452–459CrossRefPubMedGoogle Scholar
  14. Förster B, Mathesius U, Pogson BJ (2006) Comparative proteomics of high light stress in the model alga Chlamydomonas reinhardtii. Proteomics 6:4309–4320CrossRefPubMedGoogle Scholar
  15. Fujimoto T, Tomitakab Y, Abec H, Tsudab S, Futaia K, Mizukubob T (2011) Expression profile of jasmonic acid-induced genes and the induced resistance against the root-knot nematode (Meloidogyne incognita) in tomato plants (Solanum lycopersicum) after foliar treatment with methyl jasmonate. J Plant Physiol 168:1084–1097CrossRefPubMedGoogle Scholar
  16. Gancedo JM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361PubMedPubMedCentralGoogle Scholar
  17. Gómez-Ariza J, Campo S, Rufat M, Estopà M, Messeguer J, San Segundo B, Coca M (2007) Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mole Plant-Microbe In 20(7):832–842CrossRefGoogle Scholar
  18. Grupe A, Hultgren B, Ryan A, Ma YH, Bauer M, Stewart TA (1995) Transgenic knockouts reveal a critical requirement for pancreatic β cell glucokinase in maintaining glucose homeostasis. Cell 83:69–78CrossRefPubMedGoogle Scholar
  19. Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776CrossRefPubMedGoogle Scholar
  20. Hammond-Kosack KE, Atkinson HJ, Bowles DJ (1990) Changes in abundance of translatable mRNA species in potato roots and leaves following root invasion by cyst-nematode G, rostochiensis pathotypes. Physiol Mol Plant Pathol 37:339–354CrossRefGoogle Scholar
  21. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272CrossRefPubMedGoogle Scholar
  22. Herbers K, Meuwly P, Frommer WB, Metraux JP, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jarsch IK, Ott T (2011) Perspectives on remorin proteins, membrane rafts, and their role during plant–microbe interactions. Mol Plant Microbe Interact 24:7–12CrossRefPubMedGoogle Scholar
  24. Jensen RG (2000) Activation of Rubisco regulates photosynthesis at high temperature and CO2. Proc Natl Acad Sci USA 97:12937–12938CrossRefPubMedPubMedCentralGoogle Scholar
  25. Johnston M (1999) Feasting, fasting and fermenting: glucose sensing in yeast and other cells. Trends Genet 15:29–33CrossRefPubMedGoogle Scholar
  26. Johnstone O, Lasko P (2001) Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu Rev Genet 35:365–406CrossRefPubMedGoogle Scholar
  27. Jorge I, Navarro RM, Lenz C, Ariza D, Porras C, Jorrín J (2005) The Holm Oak leaf proteome: analytical and biological variability in the protein expression level assessed by 2-DE and protein identification tandem mass spectrometry de novo sequencing and sequence similarity searching. Proteomics 5:222–234CrossRefPubMedGoogle Scholar
  28. Katayama H, Nagasu T, Oda Y (2001) Improvement of in-gel digestion protocol for peptide mass fingerprinting by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 15:1416–1421CrossRefPubMedGoogle Scholar
  29. Lee MO, Kim KP, Kim B, Hahn JS, Hong CB (2009) Flooding stress-induced glycine-rich RNA-binding protein from Nicotiana tabacum. Mol Cells 27:47–54CrossRefPubMedGoogle Scholar
  30. León J (2013) Role of plant peroxisomes in the production of jasmonic acid-based signals. Subcell Biochem 69:299–313CrossRefPubMedGoogle Scholar
  31. Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232CrossRefPubMedGoogle Scholar
  33. Maris C, Dominguez C, Allain FHT (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272:2118–2131CrossRefPubMedGoogle Scholar
  34. McGurl B, Ryan CA (1992) The organization of the prosystemin gene. Plant Mol Biol 20:405–409CrossRefPubMedGoogle Scholar
  35. Moeder W, Del Pozo O, Navarre DA, Martin GB (2007) Plant aconitase functions as an RNA2-binding protein and plays a role in regulating resistance to oxidative stress and hypersensitive cell death. Plant Mol Biol 63:273–287CrossRefPubMedGoogle Scholar
  36. Nahar K, Kyndt T, De Vleesschauwer D, Höfte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–316CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pérez-Bueno ML, Rahoutei J, Sajnani C, García-Luque I, Barón M (2004) Proteomic analysis of the oxygen-evolving complex of photosystem II under biotec stress: studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425CrossRefPubMedGoogle Scholar
  38. Popova LP, Stanka GV (1988) Effect of jasmonic acid on the synthesis of ribulose-1, 5-bisphosphate carboxylase-oxygenase in barley leaves. J Plant Physiol 133:210–215CrossRefGoogle Scholar
  39. Popova LP, Tsonev TD, Vaklinova SG (1988) Changes in some photosynthetic and photorespiratory properties in barley leaves after treatment with jasmonic acid. J Plant Physiol 132:257–261CrossRefGoogle Scholar
  40. Raffaele S, Bayer E, Lafarge D, Cluzet S, ReS German, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J, Noirot E, Satiat-Jeunemaître B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, Reymond P, Simon-Plas F, Farmer EE, Bessoule JJ, Mongrand S (2009) Remorin, a Solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21:1541–1555CrossRefPubMedPubMedCentralGoogle Scholar
  41. Rakwal R, Komatsu S (2001) Jasmonic acid-induced necrosis and drastic decreases in ribulose-1, 5-bisphosphate carboxylase/oxygenase in rice seedlings under light involves reactive oxygen species. J Plant Physiol 58:679–688CrossRefGoogle Scholar
  42. Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206CrossRefPubMedGoogle Scholar
  43. Salzman RA, Tikhonova I, Bordelon BP, Hasegawa PM, Bressan RA (1998) Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. Plant Physiol 117:465–472CrossRefPubMedPubMedCentralGoogle Scholar
  44. Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin PlantGoogle Scholar
  45. Sugihara K, Hanagata N, Dubinsky Z, Baba S, Karube I (2000) Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza. Plant Cell Physiol 41:1279–1285CrossRefPubMedGoogle Scholar
  46. Thorpe MR, Ferrieri AP, Herth MM, Ferrieri RA (2007) 11C-imaging: methyl jasmonate moves in both phloem and xylem, promotes transport of jasmonate, and of photoassimilate even after proton transport is decoupled. Planta 226:541–551CrossRefPubMedGoogle Scholar
  47. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104:1075–1080CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wickens M, Bernstein D, Crittenden S, Luitjens C, Kimble J (2001) PUF proteins and 3′UTR regulation in the Caenorhabditis elegans germ line. Cold Spring Harb Symp Quant Biol 66:337–343CrossRefPubMedGoogle Scholar
  49. Yang EJ, Oh YA, Lee ES, Park AR, Cho SK, Yoo YJ, Park OK (2003) Oxygen-evolving enhancer protein 2 is phosphorylated by glycine-rich protein 3/wall-associated kinase 1 in Arabidopsis. Biochem Biophys Res Commun 305:862–868CrossRefPubMedGoogle Scholar
  50. Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49(7):1092–1111CrossRefPubMedGoogle Scholar
  51. Zhao WC, Li ZL, Fan JW, Hu CL, Yang R, Qi X, Chne H, ZhaoFK Wang SH (2015) Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J Exp Bot 66:4653–4667CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhuang WB, Shi T, Gao ZH, Zhang Z, Zhang JY (2013) Differential expression of proteins associated with seasonal bud dormancy at four critical stages in Japanese apricot. Plant Biol 15(233–242):20Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Wenchao Zhao
    • 1
  • Jinghong Hao
    • 1
  • Jiayi Xing
    • 1
  • Rui Yang
    • 1
  • Fukuan Zhao
    • 2
  • Jianli Wang
    • 1
  • Shaohui Wang
    • 1
  1. 1.Beijing Key Laboratory for Agricultural Application and New Technique, Plant Science and Technology CollegeBeijing University of AgricultureBeijingChina
  2. 2.Biological Science and Engineering CollegeBeijing University of AgricultureBeijingChina

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