A Rhizosphere Fungus Enhances Arabidopsis Thermotolerance Through Production of an HSP90 Inhibitor

Overview

Journal Plant Physiol

Specialty Physiology

Date 2007 Jul 17

PMID 17631526

Citations 44

Authors

Catherine A McLellan

Thomas J Turbyville

E M Kithsiri Wijeratne

Arthur Kerschen

Elizabeth Vierling

Christine Queitsch

Luke Whitesell

A A Leslie Gunatilaka

Affiliations

Soon will be listed here.

Abstract

The molecular chaperone HEAT SHOCK PROTEIN90 (HSP90) is essential for the maturation of key regulatory proteins in eukaryotes and for the response to temperature stress. Earlier, we have reported that fungi living in association with plants of the Sonoran desert produce small molecule inhibitors of mammalian HSP90. Here, we address whether elaboration of the HSP90 inhibitor monocillin I (MON) by the rhizosphere fungus Paraphaeosphaeria quadriseptata affects plant HSP90 and plant environmental responsiveness. We demonstrate that MON binds Arabidopsis (Arabidopsis thaliana) HSP90 and can inhibit the function of HSP90 in lysates of wheat (Triticum aestivum) germ. MON treatment of Arabidopsis seedlings induced HSP101 and HSP70, conserved components of the stress response. Application of MON, or growth in the presence of MON, allowed Arabidopsis wild type but not AtHSP101 knockout mutant seedlings to survive otherwise lethal temperature stress. Finally, cocultivation of P. quadriseptata with Arabidopsis enhanced plant heat stress tolerance. These data demonstrate that HSP90-inhibitory compounds produced by fungi can influence plant growth and responses to the environment.

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References

Gomes N, Fagbola O, Costa R, Rumjanek N, Buchner A, Mendona-Hagler L . Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol. 2003; 69(7):3758-66. PMC: 165189. DOI: 10.1128/AEM.69.7.3758-3766.2003. View

David C, Smith H, Raynes D, Pulcini E, Whitesell L . Expression of a unique drug-resistant Hsp90 ortholog by the nematode Caenorhabditis elegans. Cell Stress Chaperones. 2003; 8(1):93-104. PMC: 514859. DOI: 10.1379/1466-1268(2003)8<93:eoaudh>2.0.co;2. View

Thulasiraman V, Matts R . Effect of geldanamycin on the kinetics of chaperone-mediated renaturation of firefly luciferase in rabbit reticulocyte lysate. Biochemistry. 1996; 35(41):13443-50. DOI: 10.1021/bi9615396. View

Zou J, Guo Y, Guettouche T, Smith D, Voellmy R . Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell. 1998; 94(4):471-80. DOI: 10.1016/s0092-8674(00)81588-3. View

Rutherford S, Lindquist S . Hsp90 as a capacitor for morphological evolution. Nature. 1998; 396(6709):336-42. DOI: 10.1038/24550. View

Roe S, Prodromou C, OBrien R, Ladbury J, Piper P, Pearl L . Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J Med Chem. 1999; 42(2):260-6. DOI: 10.1021/jm980403y. View

Sangster T, Queitsch C . The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr Opin Plant Biol. 2005; 8(1):86-92. DOI: 10.1016/j.pbi.2004.11.012. View

Noutoshi Y, Ito T, Seki M, Nakashita H, Yoshida S, Marco Y . A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J. 2005; 43(6):873-88. DOI: 10.1111/j.1365-313X.2005.02500.x. View

Whitesell L, Lindquist S . HSP90 and the chaperoning of cancer. Nat Rev Cancer. 2005; 5(10):761-72. DOI: 10.1038/nrc1716. View

10.

Turbyville T, Wijeratne E, Liu M, Burns A, Seliga C, Luevano L . Search for Hsp90 inhibitors with potential anticancer activity: isolation and SAR studies of radicicol and monocillin I from two plant-associated fungi of the Sonoran desert. J Nat Prod. 2006; 69(2):178-84. PMC: 1876775. DOI: 10.1021/np058095b. View

11.

Gunatilaka A . Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod. 2006; 69(3):509-26. PMC: 3362121. DOI: 10.1021/np058128n. View

12.

Rinehart J, Hayward S, Elnitsky M, Sandro L, Lee Jr R, Denlinger D . Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. Proc Natl Acad Sci U S A. 2006; 103(38):14223-7. PMC: 1599938. DOI: 10.1073/pnas.0606840103. View

13.

Voellmy R, Boellmann F . Chaperone regulation of the heat shock protein response. Adv Exp Med Biol. 2007; 594:89-99. DOI: 10.1007/978-0-387-39975-1_9. View

14.

Marquez L, Redman R, Rodriguez R, Roossinck M . A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science. 2007; 315(5811):513-5. DOI: 10.1126/science.1136237. View

15.

Yeyati P, Bancewicz R, Maule J, Heyningen V . Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet. 2007; 3(3):e43. PMC: 1839141. DOI: 10.1371/journal.pgen.0030043. View

16.

Schulze-Lefert P . Plant immunity: the origami of receptor activation. Curr Biol. 2004; 14(1):R22-4. View

17.

Sangster T, Lindquist S, Queitsch C . Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. Bioessays. 2004; 26(4):348-62. DOI: 10.1002/bies.20020. View

18.

Kerschen A, Napoli C, Jorgensen R, Muller A . Effectiveness of RNA interference in transgenic plants. FEBS Lett. 2004; 566(1-3):223-8. DOI: 10.1016/j.febslet.2004.04.043. View

19.

Belkhadir Y, Subramaniam R, Dangl J . Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol. 2004; 7(4):391-9. DOI: 10.1016/j.pbi.2004.05.009. View

20.

Omura S, Iwai Y, Takahashi Y, Sadakane N, Nakagawa A, Oiwa H . Herbimycin, a new antibiotic produced by a strain of Streptomyces. J Antibiot (Tokyo). 1979; 32(4):255-61. DOI: 10.7164/antibiotics.32.255. View