Skip to main content
SpringerLink
Log in

Defining the phosphite-regulated transcriptome of the plant pathogen Phytophthora cinnamomi

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Phosphite, an analog of phosphate is used to control oomycete diseases on a wide range of horticultural crops and in native ecosystems. In this study, we investigated morphological and transcriptional changes induced in Phytophthora cinnamomi by phosphite. Cytological observations revealed that phosphite caused hyphal distortions and lysis of cell walls and had an adverse effect on hyphal growth. At the molecular level, the expression levels of 43 transcripts were changed. Many of these encoded proteins involved in cell wall synthesis, or cytoskeleton functioning. The results of both the microscopic and molecular investigations are consistent with phosphite inhibiting the function of the cytoskeleton and cell wall synthesis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbasi PA, Lazarovits G (2006) Seed treatment with phosphonate (AG3) suppresses Pythium damping-off of cucumber seedlings. Plant Dis 90:459–464

    Article  CAS  Google Scholar 

  • Altschul SF, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Balci Y, Balci S, Eggers J, MacDonald WL, Juzwik J, Long RP, Gottschalk KW (2007) Phytophthora spp. associated with forest soils in eastern and north-central US oak ecosystems. Plant Dis 91:705–710

    Article  Google Scholar 

  • Barchietto T, Saindrenan P, Bompeix G (1992) Physiological responses of Phytophthora citrophthora to a sub-inhibitory concentration of phosphonate. Pesticide Biochem Physiol 42:151–166

    Article  CAS  Google Scholar 

  • Beyer K, Jimenez SJ, Randall TA, Lam S, Binder A, Boller T, Collinge MA (2002) Characterization of Phytophthora infestans genes regulated during the interaction with potato. Mol Plant Pathol 3:473–485

    Article  CAS  PubMed  Google Scholar 

  • Birch PRJ, Avrova AO, Duncan JM, Lyon GD, Toth RL (1999) Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophthora infestans. Mol Plant Microbe Interact 12:356–361

    Article  CAS  Google Scholar 

  • Blair JE, Coffey MD, Park SY, Geiser DM, Kang S (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol 45:266–277

    Article  CAS  PubMed  Google Scholar 

  • Bouzenzana J, Pelosi L, Briolay A, Briolay J, Bulone V (2006) Identification of the first Oomycete annexin as a (1 → 3)-beta-d-glucan synthase activator. Mol Microbiol 62:552–565

    Article  CAS  PubMed  Google Scholar 

  • Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:792–808. doi:10.1111/j.1365-3059.2008.01886.x

    Article  Google Scholar 

  • Brasier C, Beales P, Kirk S, Denman S, Rose J (2005) Phytophthora kernoviae sp. nov., an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in the UK. Mycol Res 109:853–859

    Article  PubMed  Google Scholar 

  • Brown AV, Brasier CM (2007) Colonization of tree xylem by Phytophthora ramorum, P-kernoviae and other Phytophthora species. Plant Pathol 56:227–241

    Article  Google Scholar 

  • Brown S, Koike S, Ochoa O, Laemmlen F, Michelmore R (2003) Insensitivity to the fungicide Fosetyl-aluminium in California isolates of the downy mildew pathogen Bremia lactuca. Plant Dis 88:502–508

    Article  Google Scholar 

  • Cahill DM, Rookes JE, Wilson BA, Gibson L, McDougall KL (2008) Phytophthora cinnamomi and Australia’s biodiversity: impacts, predictions and progress towards control. Aust J Bot 56:279–310

    Article  Google Scholar 

  • Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32

    Article  CAS  PubMed  Google Scholar 

  • D’Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7:347–358

    Article  PubMed  Google Scholar 

  • Dadke S, Cotteret S, Yip SC, Jaffer ZM, Haj F, Ivanov A, Rauscher F, Shuai K, Ng T, Neel BG, Chernoff J (2007) Regulation of protein tyrosine phosphatase 1B by sumoylation. Nat Cell Biol 9:80–102

    Article  CAS  PubMed  Google Scholar 

  • Delaure SL, van Hemelrijck W, De Bolle MFC, Cammue BPA, De Coninck BMA (2008) Building up plant defences by breaking down proteins. Plant Sci 174:375–385

    Article  CAS  Google Scholar 

  • Fenn ME, Coffey MD (1985) Further evidence for the direct mode of action of fosetyl-Al and phosphorus acid. Phytopathology 75:1064–1068

    Article  CAS  Google Scholar 

  • Ferreira R, Monteiro S, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–700

    Article  CAS  PubMed  Google Scholar 

  • Gaulin E, Jauneau A, Villalba F, Rickauer M, Esquerre-Tugaaye M, Bottin A (2002) The CBEL glycoprotein of Phytophthora parasitica var. nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. J Cell Sci 115:4565–4575

    Article  CAS  PubMed  Google Scholar 

  • Goritschnig S, Zhang YL, Li X (2007) The ubiquitin pathway is required for innate immunity in Arabidopsis. Plant J 49:540–551

    Article  CAS  PubMed  Google Scholar 

  • Grenville-Briggs LJ, Anderson VL, Fugelstad J, Avrova AO, Bouzenzana J, Williams A, Wawra S, Whisson SC, Birch PRJ, Bulone V, van West P (2008) Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell 20:720–738

    Article  CAS  PubMed  Google Scholar 

  • Hardham AR (2005) Phytophthora cinnamomi. Mol Plant Pathol 6:589–604

    Article  CAS  PubMed  Google Scholar 

  • Hardham AR (2007) Cell biology of plant–oomycete interactions. Cell Microbiol 9:31–39

    Article  CAS  PubMed  Google Scholar 

  • Hardy GES, Barrett S, Shearer BL (2001) The future of phosphite as a fungicide to control the soilborne plant pathogen Phytophthora cinnamomi in natural ecosystems. Australas Plant Pathol 30:133–139

    Article  Google Scholar 

  • Huberli D, Tommerup IC, Hardy GESJ (2000) False negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi. Australas Plant Pathol 29:164–169

    Article  Google Scholar 

  • Jin YJ, Blue EK, Gallagher PJ (2006) Control of death-associated protein kinase (DAPK) activity by phosphorylation and proteasomal degradation. J Biol Chem 281:39033–39040

    Article  CAS  PubMed  Google Scholar 

  • Kamoun S (2003) Molecular genetics of pathogenic Oomycetes. Eukaryot Cell 2:191–199

    Article  CAS  PubMed  Google Scholar 

  • Kamoun S, van West P, Vleeshouwers V, de Groot KE, Govers F (1998) Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10:1413–1425

    Article  CAS  PubMed  Google Scholar 

  • Konopka-Postupolska D (2007) Annexins: putative linkers in dynamic membrane–cytoskeleton interactions in plant cells. Protoplasma 230:203–215

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong QQ, Ma SS, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  CAS  PubMed  Google Scholar 

  • Leonardi J, Wiley AW, Langdon PW, Pegg KG, Cheyne J (1999) Progress on the use of foliar applications of phosphonate for the control of Phytophthora root rot in avocados. Talking Avocados 10:18–21

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Logemann J, Schell J, Willmitzer L (1987) Improved method for isolation of RNA from plant tissue. Anal Biochem 163:16–20

    Article  CAS  PubMed  Google Scholar 

  • Long PJ, Miller SA, Davis SK (1989) Duration of fungicidal effect following injection of apple trees with fosetyl-Al. J Phytopathol 124:89–96

    CAS  Google Scholar 

  • McComb JA, O’Brien PA, Calver M, Staskowski P, Jardine N, Eshraghi L, Ellery J, Gilovitz J, Scott P, O’Brien J, O’Gara E, Howard K, Dell B and Hardy GES (2008) Research into natural and induced resistance in Australian vegetation to Phytophthora cinnamomi and innovative methods to eradicate and/or contain within localised incursions within areas of high biodiversity in Australia Subproject 19.2.2 Enhancing the efficacy of phosphite with supplementation with other chemicals such as those known to be involved in resistance. Report 19/2005 subproject 91.2.2 Dept. of Environment and Heritage, Commonwealth Government of Australia

  • McDonald AE, Grant BR, Plaxton WC (2001) Phosphite (phosphorous acid): its relevance in the environment and agriculture and influence on plant phosphate starvation response. J Plant Nutr 24:1505–1519

    Article  CAS  Google Scholar 

  • McKay A, Floyd R, Boyd C (1992) Phosphonic acid controls downy mildew (Peronospora parasitica) in cauliflower curds. Aust J Exp Agric 32:127–129

    Article  CAS  Google Scholar 

  • Miller JS, Olsen N, Woodell L, Porter LD, Clayson S (2006) Post-harvest applications of zoxamide and phosphite for control of potato fiber rots caused by oomycetes at harvest. Am J Potato Res 83:269–278

    Article  CAS  Google Scholar 

  • Perez V, Mamdouh AM, Huet JC, Pernollet JC, Bompeix G (1995) Enhanced secretion of elicitins by Phytophthora fungi exposed to phosphonate. Cryptogamie Mycologie 16:191–194

    Google Scholar 

  • Ribeiro CA (1978) A source book of the genus Phytophthora. J. Cramer, Vaduz

    Google Scholar 

  • Rizzo DM, Garbelotto M, Hansen EA (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43:309–335

    Article  PubMed  Google Scholar 

  • Roetschi A, Si-Ammour A, Belbahri L, Mauch F, Mauch-Mani B (2001) Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 28:293–305

    Article  CAS  PubMed  Google Scholar 

  • Saindrenan P, Barchietto T, Bompeix G (1990) Effect of phosphonate on the elicitor activity of culture filtrates of Phytophthora cryptogea in Vigna unguiculata. Plant Sci 67:245–251

    Article  CAS  Google Scholar 

  • Sala FC, da Costa CP, Echer MD, Martins MC, Blat SF (2004) Phosphite effect on hot and sweet pepper reaction to Phytophthora capsici. Scientia Agricola 61:492–495

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Shearer BL, Fairman RG (2007) A stem injection of phosphite protects Banksia species and Eucalyptus marginata from Phytophthora cinnamomi for at least four years. Australas Plant Pathol 36:78–86

    Article  CAS  Google Scholar 

  • Shearer BL, Crane CE, Fairman RG (2004) Phosphite reduces disease extension of a Phytophthora cinnamomi front in Banksia woodland, even after fire. Australas Plant Pathol 33:249–254

    Article  CAS  Google Scholar 

  • Shearer BL, Crane CE, Barrett S, Cochrane A (2007) Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-West Botanical Province of Western Australia. Aust J Bot 55:225–238

    Article  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin proteasome pathway. Annu Rev Plant Biol 55:555–590

    Article  CAS  PubMed  Google Scholar 

  • Smillie R, Grant B, Guest D (1989) The mode of action of phosphite: evidence for both direct and indirect modes of action on three Phytophthora spp. in plants. Phytopathology 79:921–926

    Article  CAS  Google Scholar 

  • Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:1

    Google Scholar 

  • Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31:265–273

    Article  CAS  PubMed  Google Scholar 

  • Tyler BM, Tripathy S, Zhang XG, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CMB, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour KH, Lee M, McDonald WH, Medina M, Meijer HJG, Nordberg EK, Maclean DJ, Ospina-Giraldo MD, Morris PF, Phuntumart V, Putnam NH, Rash SR, Rose JKC, Sakihama Y, Salamov AA, Savidor A, Scheuring CF, Smith BM, Sobral BS, Terry A, Torto-Alalibo TA, Win J, Xu Z, Zhang H, Grigoriev IV, Rokhsar DS, Boore JL (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of disease. Science 313:1261–1266

    Article  CAS  PubMed  Google Scholar 

  • van West P, Reid B, Campbell TA, Sandrock RW, Fry WE, Kamoun S, Gow NAR (1999) Green fluorescent protein (GFP) as a reporter gene for the plant pathogenic oomycete Phytophthora palmivora. FEMS Microbiol Lett 178:71–80

    Article  PubMed  Google Scholar 

  • Wilkinson CJ, Holmes JM, Dell B, Tynan KM, McComb JA, Shearer BL, Colquhoun IJ, Hardy GES (2001) Effect of phosphite on in planta zoospore production of Phytophthora cinnamomi. Plant Pathol 50:587–593

    Article  CAS  Google Scholar 

  • Wong M, McComb JA, Hardy GES, O’Brien PA (2008) Phosphite induces expression of a putative proteophosphoglycan gene in Phytophthora cinnamomi. Australas Plant Pathol 38:235–241

    Article  Google Scholar 

  • Yan H, Liou R (2006) Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica. Fungal Genet Biol 43:430–438

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was in part funded by the Australian Research Council, Project Number LP0219473.

Author information

Authors and Affiliations

  1. Centre for Phytophthora Science and Management, School of Biological Sciences and Biotechnology, Murdoch University, Perth, WA, 6150, Australia

    Michaela King, Wayne Reeve, Nari Williams, Jen McComb, Philip A. O’Brien & Giles E. St. J. Hardy

  2. Adelaide Microarray Centre, Hanson Institute, Adelaide, SA, 5005, Australia

    Mark B. Van der Hoek

Authors
  1. Michaela King
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wayne Reeve
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark B. Van der Hoek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nari Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jen McComb
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Philip A. O’Brien
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giles E. St. J. Hardy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip A. O’Brien.

Additional information

Communicated by J. Perez-Martin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

King, M., Reeve, W., Van der Hoek, M.B. et al. Defining the phosphite-regulated transcriptome of the plant pathogen Phytophthora cinnamomi . Mol Genet Genomics 284, 425–435 (2010). https://doi.org/10.1007/s00438-010-0579-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-010-0579-7

Keywords

Search

Navigation