Skip to content
1887

Journal of General Virology header logo Journal of General Virology

Volume 89, Issue 8

HC-Pro protein of sugar cane mosaic virus interacts specifically with maize ferredoxin-5 and No Access

Abstract

Symptom development of a plant viral disease is a result of molecular interactions between the virus and its host plant; thus, the elucidation of specific interactions is a prerequisite to reveal the mechanism of viral pathogenesis. Here, we show that the chloroplast precursor of ferredoxin-5 (Fd V) from maize () interacts with the multifunctional HC-Pro protein of sugar cane mosaic virus (SCMV) in yeast, cells and maize protoplasts. Our results demonstrate that the transit peptide rather than the mature protein of Fd V precursor could interact with both N-terminal (residues 1–100) and C-terminal (residues 301–460) fragments, but not the middle part (residues 101–300), of HC-Pro. In addition, SCMV HC-Pro interacted only with Fd V, and not with the other two photosynthetic ferredoxin isoproteins (Fd I and Fd II) from maize plants. SCMV infection significantly downregulated the level of Fd V mRNA in maize plants; however, no obvious changes were observed in levels of Fd I and Fd II mRNA. These results suggest that SCMV HC-Pro interacts specifically with maize Fd V and that this interaction may disturb the post-translational import of Fd V into maize bundle-sheath cell chloroplasts, which could lead to the perturbation of chloroplast structure and function.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.2008/001271-0
2008-08-01
2026-01-16

Metrics

Loading full text...

Full text loading...

References

  1. Anandalakshmi R., Marathe R., Ge X., Herr J. M. Jr, Mau C., Mallory A., Pruss G., Bowman L., Vance V. B. 2000; A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290:142–144 [CrossRef]
     [Google Scholar]
  2. Atreya C. D., Pirone T. P. 1993; Mutational analysis of the helper component-proteinase gene of a potyvirus: effects of amino acid substitutions, deletions, and gene replacement on virulence and aphid transmissibility. Proc Natl Acad Sci U S A 90:11919–11923 [CrossRef]
     [Google Scholar]
  3. Ballut L., Drucker M., Pugnière M., Cambon F., Blanc S., Roquet F., Candresse T., Schmid H. P., Nicolas P. other authors 2005; HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities. J Gen Virol 86:2595–2603 [CrossRef]
     [Google Scholar]
  4. Carrington J. C., Freed D. D., Oh C. S. 1990; Expression of potyviral polyproteins in transgenic plants reveals three proteolytic activities required for complete processing. EMBO J 9:1347–1353
     [Google Scholar]
  5. Darie C. C., De Pascalis L., Mutschler B., Haehnel W. 2006; Studies of the Ndh complex and photosystem II from mesophyll and bundle sheath chloroplasts of the C4-type plant Zea mays . J Plant Physiol 163:800–808 [CrossRef]
     [Google Scholar]
  6. Dawson W. O. 1992; Tobamovirus-plant interactions. Virology 186:359–367 [CrossRef]
     [Google Scholar]
  7. Ducruet J. M., Roman M., Havaux M., Janda T., Gallais A. 2005; Cyclic electron flow around PSI monitored by afterglow luminescence in leaves of maize inbred lines ( Zea mays L.): correlation with chilling tolerance. Planta 221:567–579 [CrossRef]
     [Google Scholar]
  8. Fan Z. F., Chen H. Y., Liang X. M., Li H. F. 2003; Complete sequence of the genomic RNA of the prevalent strain of a potyvirus infecting maize in China. Arch Virol 148:773–782 [CrossRef]
     [Google Scholar]
  9. Gissot L., Polge C., Jossier M., Girin T., Bouly J. P., Kreis M., Thomas M. 2006; AKIN βγ contributes to SnRK1 heterotrimeric complexes and interacts with two proteins implicated in plant pathogen resistance through its KIS/GBD sequence. Plant Physiol 142:931–944 [CrossRef]
     [Google Scholar]
  10. Guo D., Spetz C., Saarma M., Valkonen J. P. T. 2003; Two potato proteins, including a novel RING finger protein (HIP1), interact with the potyviral multifunctional protein HCpro. Mol Plant Microbe Interact 16:405–410 [CrossRef]
     [Google Scholar]
  11. Hase T., Kimata Y., Yonekura K., Matsumura T., Sakakibara H. 1991; Molecular cloning and differential expression of the maize ferredoxin gene family. Plant Physiol 96:77–83 [CrossRef]
     [Google Scholar]
  12. Holtgrefe S., Bader K. P., Horton P., Scheibe R., von Schaewen A., Backhausen J. E. 2003; Decreased content of leaf ferredoxin changes electron distribution and limits photosynthesis in transgenic potato plants. Plant Physiol 133:1768–1778 [CrossRef]
     [Google Scholar]
  13. Hull R. 2001 Matthews' Plant Virology, 4th edn. San Diego: Academic Press;
     [Google Scholar]
  14. Jiménez I., López L., Alamillo J. M., Valli A., García J. A. 2006; Identification of a plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol Plant Microbe Interact 19:350–358 [CrossRef]
     [Google Scholar]
  15. Jin Y., Ma D., Dong J., Jin J., Li D., Deng C., Wang T. 2007a; HC-Pro protein of Potato virus Y can interact with three Arabidopsis 20S proteasome subunits in planta. J Virol 81:12881–12888 [CrossRef]
     [Google Scholar]
  16. Jin Y., Ma D., Dong J., Li D., Deng C., Jin J., Wang T. 2007b; The HC-Pro protein of potato virus Y interacts with NtMinD of tobacco. Mol Plant Microbe Interact 20:1505–1511 [CrossRef]
     [Google Scholar]
  17. Kasschau K. D., Carrington J. C. 1998; A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–470 [CrossRef]
     [Google Scholar]
  18. Kasschau K. D., Carrington J. C. 2001; Long-distance movement and replication maintenance functions correlate with silencing suppression activity of potyviral HC-Pro. Virology 285:71–81 [CrossRef]
     [Google Scholar]
  19. Kasschau K. D., Xie Z., Allen E., Llave C., Chapman E. J., Krizan K. A., Carrington J. C. 2003; P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217 [CrossRef]
     [Google Scholar]
  20. Kimata-Ariga Y., Matsumura T., Kada S., Fujimoto H., Fujita Y., Endo T., Mano J., Sato F., Hase T. 2000; Differential electron flow around photosystem I by two C4-photosynthetic-cell-specific ferredoxins. EMBO J 19:5041–5050 [CrossRef]
     [Google Scholar]
  21. Klein P. G., Klein R. R., Rodríguez-Cerezo E., Hunt A. G., Shaw J. G. 1994; Mutational analysis of the tobacco vein mottling virus genome. Virology 204:759–769 [CrossRef]
     [Google Scholar]
  22. Lehto K., Tikkanen M., Hiriart J. B., Paakkarinen V., Aro E. M. 2003; Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus. Mol Plant Microbe Interact 16:1135–1144 [CrossRef]
     [Google Scholar]
  23. Matsumura T., Kimata-Ariga Y., Sakakibara H., Sugiyama T., Murata H., Takao T., Shimonishi Y., Hase T. 1999; Complementary DNA cloning and characterization of ferredoxin localized in bundle-sheath cells of maize leaves. Plant Physiol 119:481–488 [CrossRef]
     [Google Scholar]
  24. McClintock K., Lamarre A., Parsons V., Laliberté J. F., Fortin M. G. 1998; Identification of a 37 kDa plant protein that interacts with the turnip mosaic potyvirus capsid protein using anti-idiotypic-antibodies. Plant Mol Biol 37:197–204 [CrossRef]
     [Google Scholar]
  25. Mlotshwa S., Verver J., Sithole-Niang I., Gopinath K., Carette J., van Kammen A., Wellink J. 2002; Subcellular location of the helper component-proteinase of Cowpea aphid-borne mosaic virus. Virus Genes 25:207–216 [CrossRef]
     [Google Scholar]
  26. Petracek M. E., Dickey L. F., Nguyen T. T., Gatz C., Sowinski D. A., Allen G. C., Thompson W. F. 1998; Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc Natl Acad Sci U S A 95:9009–9013 [CrossRef]
     [Google Scholar]
  27. Pilon M., Wienk H., Sips W., de Swaaf M., Talboom I., , van't Hof R., de Korte-Kool G., Demel R., Weisbeek P., de Kruijff B. 1995; Functional domains of the ferredoxin transit sequence involved in chloroplast import. J Biol Chem 270:3882–3893 [CrossRef]
     [Google Scholar]
  28. Plisson C., Drucker M., Blanc S., German-Retana S., Le Gall O., Thomas D., Bron P. 2003; Structural characterization of HC-Pro, a plant virus multifunctional protein. J Biol Chem 278:23753–23761 [CrossRef]
     [Google Scholar]
  29. Rensink W. A., Schnell D. J., Weisbeek P. J. 2000; The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope. J Biol Chem 275:10265–10271 [CrossRef]
     [Google Scholar]
  30. Richter S., Lamppa G. K. 2002; Determinants for removal and degradation of transit peptides of chloroplast precursor proteins. J Biol Chem 277:43888–43894 [CrossRef]
     [Google Scholar]
  31. Rumeau D., Peltier G., Cournac L. 2007; Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051 [CrossRef]
     [Google Scholar]
  32. Sakakibara H. 2003; Differential response of genes for ferredoxin and ferredoxin : NADP+ oxidoreductase to nitrate and light in maize leaves. J Plant Physiol 160:65–70 [CrossRef]
     [Google Scholar]
  33. Shi Y. H., Chen J., Hong X. Y., Chen J. P., Adams M. J. 2007; A potyvirus P1 protein interacts with the Rieske Fe/S protein of its host. Mol Plant Pathol 8:785–790 [CrossRef]
     [Google Scholar]
  34. Shiboleth Y. M., Haronsky E., Leibman D., Arazi T., Wassenegger M., Whitham S. A., Gaba V., Gal-On A. 2007; The conserved FRNK box in HC-Pro, a plant viral suppressor of gene silencing, is required for small RNA binding and mediates symptom development. J Virol 81:13135–13148 [CrossRef]
     [Google Scholar]
  35. Takabayashi A., Kishine M., Asada K., Endo T., Sato F. 2005; Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. Proc Natl Acad Sci U S A 102:16898–16903 [CrossRef]
     [Google Scholar]
  36. Takaki F., Sano T., Yamashita K. 2006; The complete nucleotide sequence of attenuated onion yellow dwarf virus: a natural potyvirus deletion mutant lacking the N-terminal 92 amino acids of HC-Pro. Arch Virol 151:1439–1445 [CrossRef]
     [Google Scholar]
  37. Tribodet M., Glais L., Kerlan C., Jacquot E. 2005; Characterization of potato virus Y (PVY) molecular determinants involved in the vein necrosis symptom induced by PVYN isolates in infected Nicotiana tabacum cv. Xanthi. J Gen Virol 86:2101–2105 [CrossRef]
     [Google Scholar]
  38. Walter M., Chaban C., Schütze K., Batistic O., Weckermann K., Näke C., Blazevic D., Grefen C., Schumacher K. other authors 2004; Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438 [CrossRef]
     [Google Scholar]
  39. Wang D., Maule A. J. 1995; Inhibition of host gene expression associated with plant virus replication. Science 267:229–231 [CrossRef]
     [Google Scholar]
/content/journal/jgv/10.1099/vir.0.2008/001271-0
Loading
HC-Pro protein of sugar cane mosaic virus interacts specifically with maize ferredoxin-5 in vitro and in planta
J. Gen. Virol. 89, 2046 (2008); https://doi.org/10.1099/vir.0.2008/001271-0
/content/journal/jgv/10.1099/vir.0.2008/001271-0
/content/journal/jgv/10.1099/vir.0.2008/001271-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error