Proteomic analysis of a compatible interaction between Pisum sativum (pea) and the downy mildew pathogen Peronospora viciae

  • R. C. Amey
  • T. Schleicher
  • J. Slinn
  • M. Lewis
  • H. Macdonald
  • S. J. Neill
  • P. T. N. Spencer-Phillips


A proteomic approach was used to identify host proteins altering in abundance during Peronospora viciae infection of a susceptible cultivar of pea (Pisum sativum cv. Livioletta). Proteins were extracted from fully developed pea leaflets at 4 days post-inoculation, before visible symptoms were apparent. Cytoplasmic proteins and membrane- and nucleic acid-associated proteins from infected and control leaves were examined using two-dimensional difference gel electrophoresis. The majority of proteins had a similar abundance in control and infected leaves; however, several proteins were altered in abundance and twelve were found to have increased significantly in the latter. These proteins were selected for either matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry or electro-spray ionisation quadrupole time-of-flight tandem mass spectrometry analysis following trypsin digestion, with sequence identity being assigned to eight of the proteins. These included the ABR17 stress-response protein, the pathogen-induced PI176 protein, three photosynthetic proteins, a glycine-rich RNA binding protein and two glyceraldehyde 3-phosphate dehydrogenases (cytosolic and chloroplastic) which can be induced by a range of abiotic and biotic stresses in many plant species. The possible roles of these proteins in the response of the pea plant during P. viciae infection are discussed. This study represents the first proteomic analysis of downy mildew infection of pea leaves, and provides the basis for further work to elucidate molecular mechanisms of compatibility in P. viciae infections.


Electrophoresis DIGE MALDI-TOF Mass spectrometry Oomycete Protein 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amey, R. C., & Spencer-Phillips, P. T. N. (2006). Towards developing diagnostics for downy mildew diseases. Outlooks on Pest Management, 17, 4–8.Google Scholar
  2. Aneeta Sanan-Mishra, N., Tuteja, N., & Sopory, S. K. (2002). Salinity- and ABA-induced up-regulation and light-mediated modulation of mRNA encoding glycine-rich RNA-binding protein from Sorghum bicolor. Biochemical and Biophysical Research Communications, 296, 1063–1068.CrossRefGoogle Scholar
  3. Bantignies, B., Seguin, J., Muzac, I., Dedaldechamp, F., Gulick, P., & Ibrahim, R. (2000). Direct evidence of ribonucleolytic activity of a PR-10-like protein from white lupin roots. Plant Molecular Biology, 42, 871–881.PubMedCrossRefGoogle Scholar
  4. Baudo, M. M., Meza-Zepeda, L. A., Palva, E. T., & Heino, P. (1999). Isolation of a cDNA corresponding to a low temperature- and ABA-responsive gene encoding a putative glycine-rich RNA-binding protein from Solanum commersonii. Journal of Experimental Botany, 50, 1867–1868.CrossRefGoogle Scholar
  5. Beranova-Giorgianni, S. (2003). Proteome analysis by two-dimensional gel electrophoresis and mass spectrometry: strengths and limitations. Trends in Analytical Chemistry, 22, 273–281.CrossRefGoogle Scholar
  6. Bergeron, D., Beauseigle, D., & Bellemare, G. (1993). Sequence and expression of a gene encoding a protein with RNA-binding and glycine-rich domains in Brassica napus. Biochimica et Biophysica Acta, 1216, 123–125.PubMedGoogle Scholar
  7. Bestel-Corre, G., Dumas-Gaudot, E., Poinsot, V., Dieu, M., Dierick, J. F., van Tuinen, D., et al. (2002). Proteome analysis and identification of symbiosis-related proteins from Medicago truncatula Gaertn. by two-dimensional electrophoresis and mass spectrometry. Electrophoresis, 23, 122–137.PubMedCrossRefGoogle Scholar
  8. Beyer, K., Jiménez, S., Randall, T. A., Lam, S., Binder, A., Boller, T., et al. (2002). Characterization of Phytophthora infestans genes regulated during the interaction with potato. Molecular Plant Pathology, 3, 473–485.CrossRefGoogle Scholar
  9. Biesiadka, J., Bujacz, G., Sikorski, M. M., & Jaskolski, M. (2002). Crystal structures of two homologous pathogenesis-related proteins from yellow lupine. Journal of Molecular Biology, 319, 1223–1234.PubMedCrossRefGoogle Scholar
  10. Carpenter, C. D., Kreps, J. A., & Simon, A. E. (1994). Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiology, 104, 1015–1025.PubMedCrossRefGoogle Scholar
  11. Castillejo, M. Á., Amiour, N., Dumas-Gaudot, E., Rubiales, D., & Jorrín, J. V. (2004). A proteomic approach to studying plant response to crenate broomrape (Orobanche crenata) in pea (Pisum sativum). Phytochemistry, 65, 1817–1828.CrossRefGoogle Scholar
  12. Chang, M. M., Chiang, C. C., Martin, M. W., & Hadwiger, L. A. (1993). Expression of a pea disease resistance response gene in the potato cultivar Shepody. American Potato Journal, 70, 635–647.CrossRefGoogle Scholar
  13. Chivasa, S., Ndimba, B. K., Simon, W. J., Robertson, D., Yu, X. L., Knox, J. P., et al. (2002). Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis, 23, 1754–1765.PubMedCrossRefGoogle Scholar
  14. Chuisseu Wandji, J. L., Amey, R. C., Butt, E., Harrison, J., Macdonald, H., & Spencer-Phillips, P. T. N. (2007). Towards proteomic analysis of Peronospora viciae conidiospores. In A. Lebeda, & P. T. N. Spencer-Phillips (Eds.), Advances in Downy Mildew Research (vol. 3, pp. 95–100). Kostelec na Hane (Czech Republic): Palacky University in Olomouc and JOLA.Google Scholar
  15. Clark, J. S. C., & Spencer-Phillips, P. T. N. (2000). Downy Mildews. In J. Lederberg, M. Alexander, B. R. Bloom, D. Hopwood, R. Hull, B. H. Inglearski, A. I. Laskia, S. G. Oliver, M. Schaechter, & W. C. Summers (Eds.), Encyclopaedia of microbiology (vol. 2, pp. 117–129). San Diego: Academic.Google Scholar
  16. Clark, J. S. C., & Spencer-Phillips, P. T. N. (2004). The compatible interaction in downy mildew infections. In P. T. N. Spencer-Phillips, & M. J. Jeger (Eds.), Advances in downy mildew research (vol. 2, pp. 1–34). Dordrecht: Kluwer Academic.Google Scholar
  17. Colditz, F., Nyamsuren, O., Niehaus, K., Eubel, H., Braun, H-P., & Krajinski, F. (2004). Proteomic approach: identification of Medicago truncatula proteins induced in roots after infection with the pathogenic oomycete Aphanomyces euteiches. Plant Molecular Biology, 55, 109–120.PubMedCrossRefGoogle Scholar
  18. Corbett, M., Virtue, S., Bell, K., Birch, P., Burr, T., Hyman, L., et al. (2005). Identification of a new quorum-sensing-control led virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Molecular Plant-Microbe Interactions, 18, 334–342.PubMedCrossRefGoogle Scholar
  19. Coulthurst, S. J., Lilley, K. S., & Salmond, G. P. C. (2006). Genetic and proteomic analysis of the role of luxS in the enteric phytopathogen, Erwinia carotovora. Molecular Plant Pathology, 7, 31–45.CrossRefGoogle Scholar
  20. Curto, M., Camafeita, E., Lopez, J. A., Maldonado, A. M., Rubiales, D., & Jorrín, J. V. (2006). A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi). Proteomics, 6, S163–S174.PubMedCrossRefGoogle Scholar
  21. Dangl, J. L., & Jones, J. D. G. (2001). Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833.PubMedCrossRefGoogle Scholar
  22. Djordjevic, M. A., Chen, H. C., Netera, S., Van Noorden, G., Menzel, C., Taylor, S., et al. (2003). A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation. Molecular Plant-Microbe Interactions, 16, 508–524.PubMedCrossRefGoogle Scholar
  23. Dubos, C., & Plomion, C. (2001). Drought differentially affects expression of a PR-10 protein in needles of maritime pine (Pinus pinaster Ait.) seedlings. Journal of Experimental Botany, 52, 1143–1144.PubMedCrossRefGoogle Scholar
  24. Ebstrup, T., Saalbach, G., & Egsgaard, H. (2005). A proteomics study of in vitro cyst germination and appressoria formation in Phytophthora infestans. Proteomics, 5, 2839–2848.PubMedCrossRefGoogle Scholar
  25. El-Gariani, N. K., & Spencer-Phillips, P. T. N. (2004). Isolation of viable Peronospora viciae hyphae from infected Pisum sativum leaves and accumulation of nutrients in vitro. In P. T. N. Spencer-Phillips, & M. J. Jeger (Eds.), Advances in downy mildew research: Volume 2 (pp. 249–264). Dordrecht: Kluwer Academic.Google Scholar
  26. Fristensky, B., Horovitz, D., & Hadwiger, L. A. (1988). cDNA sequences for pea disease resistance response genes. Plant Molecular Biology, 11, 713–715.CrossRefGoogle Scholar
  27. Geri, C., Cecchini, E., Giannakou, M. E., Covey, S. N., & Milner, J. J. (1999). Altered patterns of gene expression in Arabidopsis elicited by Cauliflower mosaic virus (CaMV) infection and by a CaMV gene VI transgene. Molecular Plant–Microbe Interactions, 12, 377–384.PubMedCrossRefGoogle Scholar
  28. Giavalisco, P., Nordhoff, E., Lehrach, H., Gobom, J., & Klose, J. (2003). Extraction of proteins from plant tissues for two-dimensional electrophoresis analysis. Electrophoresis, 24, 207–216.PubMedCrossRefGoogle Scholar
  29. Gomez, J., Sanchez-Martinez, D., Stiefel, V., Rigau, J., Puigdomènech, P., & Pagès, M. (1988). A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature, 344, 262–264.CrossRefGoogle Scholar
  30. Grenville-Briggs, L. J., Avrova, A. O., Bruce, C. R., Williams, A., Whisson, S. C., Birch, P. R. J., et al. (2005). Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. Fungal Genetics and Biology, 42, 244–256.PubMedCrossRefGoogle Scholar
  31. Gygi, S. P., Rochon, Y., Franza, B. R., & Abersold, R. (1999). Correlation between protein and mRNA abundance in yeast. Molecular Cell Biology, 19, 1720–1730.Google Scholar
  32. Hancock, J. T., Henson, D., Nyirenda, M., Desikan, R., Harrison, J., Lewis, M., et al. (2005). Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis. Plant Physiology and Biochemistry, 43, 828–835.PubMedCrossRefGoogle Scholar
  33. Hopkins, W. G., & Hüner, N. P. A. (2004). Introduction to plant physiology. New York: Wiley.Google Scholar
  34. Kamoun, S., Hraber, P., Sobral, B., Nuss, D., & Govers, F. (1999a). Initial assessment of gene diversity for the oomycete pathogen Phytophthora infestans based on expressed sequences. Fungal Genetics and Biology, 28, 94–106.PubMedCrossRefGoogle Scholar
  35. Kamoun, S., Huitema, E., & Vleeshouwers, V. G. A. A. (1999b). Resistance to oomycetes: a general role for the hypersensitive response. Trends in Plant Science, 4, 196–200.PubMedCrossRefGoogle Scholar
  36. Kav, N. N. V., Srivastava, S., Goonewardene, L., & Blade, S. F. (2004). Proteome-level changes in the roots of Pisum sativum in response to salinity. Annals of Applied Biology, 145, 217–230.CrossRefGoogle Scholar
  37. Kim, Y-O., Kim, J. S., & Kang, H. (2005). Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant Journal, 42, 890–900.PubMedCrossRefGoogle Scholar
  38. Laberge, S., Castonguay, Y., & Vezina, L. P. (1993). New cold- and drought-regulated gene from Medicago sativa. Plant Physiology, 101, 1411–1412.PubMedCrossRefGoogle Scholar
  39. Laxalt, A. M., Cassia, R. O., Sanllorenti, P. M., Madrid, E. A., Andreu, A. B., Daleo, G. R., et al. (1996). Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Molecular Biology, 30, 961–972.PubMedCrossRefGoogle Scholar
  40. Liu, J. J., Ekramoddoullah, A. K. M., & Yu, X. S. (2003). Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiologia Plantarum, 119, 544–553.CrossRefGoogle Scholar
  41. Lucas, J. A. (1998). Plant pathology and plant pathogens. Oxford: Blackwell.Google Scholar
  42. Luo, M., Lin, L., Hill, R. D., & Mohapatra, S. S. (1991). Primary structure of an environmental stress and abscisic acid-inducible alfalfa protein. Plant Molecular Biology, 17, 1267–1269.PubMedCrossRefGoogle Scholar
  43. Luo, M., Liu, J-H., Mohapatra, S., Hill, R. D., & Mohapatra, S. S. (1992). Characterization of a gene family encoding abscisic acid- and environmental stress-inducible proteins of alfalfa. Journal of Biological Chemistry, 267, 15367–15374.PubMedGoogle Scholar
  44. Matton, D. P., & Brisson, N. (1989). Cloning, expression, and sequence conservation of pathogenesis-related gene transcripts of potato. Molecular Plant–Microbe Interactions, 2, 325–331.PubMedGoogle Scholar
  45. McDowell, J. M., & Dangl, J. L. (2000). Signal transduction in the plant immune response. Trends in Biochemical Science, 25, 79–82.CrossRefGoogle Scholar
  46. McGee, J. D., Hamer, J. E., & Hodges, T. K. (2001). Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Molecular Plant–Microbe Interactions, 14, 877–886.PubMedCrossRefGoogle Scholar
  47. Mence, M. J., & Pegg, G. F. (1971). The biology of Peronospora viciae on pea: factors affecting the susceptibility of plants to local infection and systemic colonisation. Annals of Applied Biology, 67, 297–308.CrossRefGoogle Scholar
  48. Mitchell, H. J., Kovac, K. A., & Hardham, A. R. (2002). Characterisation of Phytophthora nicotianae zoospore and cyst membrane proteins. Mycological Research, 106, 1211–1223.CrossRefGoogle Scholar
  49. Moiseyev, G. P., Beintema, J. J., Fedoreyeva, L. I., & Yakovlev, G. I. (1994). High sequence similarity between a ribonuclease from ginseng calluses and fungus-elicited proteins from parsley indicates that intracellular pathogenesis-related proteins are ribonucleases. Planta, 193, 470–472.PubMedCrossRefGoogle Scholar
  50. Moons, A., Bauw, G., Prinsen, E., van Montagu, M., & van der Straeten, D. (1995). Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant Indica rice varieties. Plant Physiology, 107, 177–186.PubMedCrossRefGoogle Scholar
  51. Moons, A., Prinsen, E., Bauw, G., & Van Montagu, M. (1997). Antagonistic effects of abscisic acid and jasmonates on salt-stress inducible transcripts in rice roots. Plant Cell, 9, 2243–2259.PubMedCrossRefGoogle Scholar
  52. Moore, B. D. (2004). Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends in Plant Science, 9, 221–228.PubMedCrossRefGoogle Scholar
  53. Mousavi, A., & Hotta, Y. (2005). Glycine-rich proteins – a class of novel proteins. Applied Biochemistry and Biotechnology, 120, 169–174.PubMedCrossRefGoogle Scholar
  54. Naqvi, S. M. S., Park, K.-S., Yi, S.-Y., Lee, H.-W., Bok, S. H., & Choi, D. (1998). A glycine-rich RNA-binding protein gene is differentially expressed during acute hypersensitive response following Tobacco mosaic virus infection in tobacco. Plant Molecular Biology, 37, 571–576.PubMedCrossRefGoogle Scholar
  55. Nyamsuren, O., Colditz, F., Rosendahl, S., Tamasloukht, M., Bekel, T., Meyer, F., et al. (2003). Transcriptional profiling of Medicago truncatula roots after infection with Aphanomyces euteiches (oomycota) identifies novel genes upregulated during this pathogenic interaction. Physiological and Molecular Plant Pathology, 63, 17–26.CrossRefGoogle Scholar
  56. Park, C.-J., Kim, K.-J., Shin, R., Park, J. M., Shin, Y.-C., & Paek, K.-H. (2004). Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant Journal, 37, 186–198.PubMedGoogle Scholar
  57. Pinto, P. M., & Ricardo, C. P. P. (1995). Lupinus albus L. pathogenesis-related proteins that show similarity to PR10 proteins. Plant Physiology, 109, 1345–1351.PubMedCrossRefGoogle Scholar
  58. Pfender, W. F. (1989). Aphanomyces root rot. In D. J. Hagedorn (Ed.), Compendium of pea diseases (pp. 25–28). St. Paul: American Phytopathological Society.Google Scholar
  59. Qutob, D., Hraber, P. T., Sobral, B. W. S., & Gijzen, M. (2000). Comparative analysis of expressed sequences in Phytophthora sojae. Plant Physiology, 123, 243–253.PubMedCrossRefGoogle Scholar
  60. Repetto, O., Bestel-Corre, G., Dumus-Gaudot, B. G., Gianinazzi-Pearson, V., & Gianinazzi, S. (2003). Targeted proteomics to identify calcium-induced protein modifications in Glomus mossae-inoculated pea roots. New Phytologist, 157, 555–567.CrossRefGoogle Scholar
  61. Richard, S., Drevet, C., Jouanin, L., & Séguin, A. (1999). Isolation and characterization of a cDNA clone encoding a putative white spruce glycine-rich RNA binding protein. Gene, 240, 379–388.PubMedCrossRefGoogle Scholar
  62. Ruiz-Lozano, J. M., Roussel, H., Gianinazzi, S., & Gianinazzi-Pearson, V. (1999). Defense genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes. Molecular Plant–Microbe Interactions, 12, 976–984.CrossRefGoogle Scholar
  63. Schmelzer, E., Kruger-Lebus, S., & Hahlbrok, K. (1989). Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell, 1, 993–1001.PubMedCrossRefGoogle Scholar
  64. Scholes, J. D. (1992). Photosynthesis: cellular and tissue aspects in diseased leaves. In P. G. Ayres (Ed.), Pests and pathogens: plant responses to foliar attack (pp. 85–106). Oxford: BIOS Scientific.Google Scholar
  65. Shepherd, S. J., van West, P., & Gow, N. A. R. (2003). Proteomic analysis of asexual development of Phytophthora palmivora. Mycological Research, 107, 395–400.PubMedCrossRefGoogle Scholar
  66. Showalter, A. M. (1993). Structure and function of plant cell wall proteins. Plant Cell, 5, 9–23.PubMedCrossRefGoogle Scholar
  67. Somssich, I. E., Schmelzer, E., Kawalleck, P., & Hahlbrook, K. (1988). Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Molecular and General Genetics, 213, 93–98.PubMedCrossRefGoogle Scholar
  68. Stafstrom, J. P., Ripley, B. D., Devitt, M. L., & Drake, B. (1998). Dormancy-associated gene expression in pea axillary buds. Planta, 205, 547–552.PubMedCrossRefGoogle Scholar
  69. Swoboda, I., Hoffmann-Sommergruber, K., O’Ríordáin, G., Scheiner, O., Heberle-Bors, E., & Vicente, O. (1996). Bet v1 proteins, the major birch pollen allergens and members of a family of conserved pathogenesis-related proteins, show ribonuclease activity in vitro. Physiologia Plantarum, 96, 433–438.CrossRefGoogle Scholar
  70. Ünlü, M., Morgan, M. E., & Minden, J. S. (1997). Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis, 18, 2071–2077.PubMedCrossRefGoogle Scholar
  71. Utriainen, M., Kokko, H., Auriola, S., Sarrazin, O., & Karenlampi, S. (1998). PR-10 protein is induced by copper stress in roots and leaves of a Cu/Zn tolerant clone of birch, Betula pendula. Plant Cell and Environment, 21, 821–828.CrossRefGoogle Scholar
  72. Velasco, R., Salamini, F., & Bartels, D. (1994). Dehydration and ABA increase mRNA levels and enzyme activity of cytosolic GAPDH in the resurrection plant Craterostigma plantineum. Plant Molecular Biology, 26, 541–546.PubMedCrossRefGoogle Scholar
  73. von Heijne, G. (1985). Signal sequences. The limits of variation. Journal of Molecular Biology, 184, 99–105.CrossRefGoogle Scholar
  74. Walter, M. H., Liu, J.-W., Grand, C., Lamb, C. J., & Hess, D. (1990). Bean pathogenesis-related (PR) proteins deduced from elicitor-induced transcripts are members of a ubiquitous new class of conserved PR proteins including pollen allergens. Molecular and General Genetics, 222, 353–360.PubMedCrossRefGoogle Scholar
  75. Wan, J., Torres, M., Ganapathy, A., Thelen, J., DaGue, B. B., Mooney, B., et al. (2005). Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum. Molecular Plant–Microbe Interactions, 18, 458–467.PubMedCrossRefGoogle Scholar
  76. Wang, C. S., Huang, J. C., & Hu, J. H. (1999a). Characterization of two subclasses of PR-10 transcripts in lily anthers and induction of their genes through separate signal transduction pathways. Plant Molecular Biology, 40, 807–814.PubMedCrossRefGoogle Scholar
  77. Wang, Y. P., Nowak, G., Culley, D., Hadwiger, L. A., & Fristensky, B. (1999b). Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). Molecular PlantMicrobe Interactions, 12, 410–418.CrossRefGoogle Scholar
  78. Warner, S. A. J., Scott, R., & Draper, J. (1992). Characterisation of a wound-induced transcript from the monocot asparagus that shares similarity with a class of intracellular pathogenesis-related PR10 proteins. Plant Molecular Biology, 19, 555–561.PubMedCrossRefGoogle Scholar
  79. Warner, S. A. J., Scott, R., & Draper, J. (1993). Isolation of an asparagus intracellular PR gene (AoPR1) wound-responsive promoter by the inverse polymerase chain reaction and its characterization in transgenic tobacco. Plant Journal, 3, 191–201.PubMedCrossRefGoogle Scholar
  80. Wienkoop, S., & Saalbach, G. (2003). Proteome analysis. Novel protein identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiology, 131, 1080–1090.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2008

Authors and Affiliations

  • R. C. Amey
    • 1
  • T. Schleicher
    • 1
  • J. Slinn
    • 1
  • M. Lewis
    • 1
  • H. Macdonald
    • 1
  • S. J. Neill
    • 1
  • P. T. N. Spencer-Phillips
    • 1
  1. 1.Centre for Research in Plant Science, Faculty of Health and Life SciencesUniversity of the West of EnglandBristolUK

Personalised recommendations