Role of the HaHOG1 MAP kinase in response of the conifer root and but rot pathogen (heterobasidion annosum) to osmotic and oxidative stress

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Raffaello, Tommaso ^a,b   Keriö, Susanna ^a   Asiegbu, Fred O ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Viikki Graduate School in Molecular Biosciences (VGSB)   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE;

ARTICLE; BASIDIOMYCETES; CELLULAR DISTRIBUTION; CONIFER; CONTROLLED STUDY; FUNGAL STRAIN; GENE EXPRESSION; GENE FUNCTION; GENE PRODUCT; HAHOG1 GENE; HETEROBASIDION ANNOSUM; MAPK GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; OXIDATIVE STRESS; PHOSPHORYLATION; PLANT GROWTH; PLANT ROOT; SACCHAROMYCES CEREVISIAE; SALT STRESS; ENZYMOLOGY; GENETICS; MICROBIOLOGY; OSMOSIS; PHYSIOLOGY; PLANT DISEASE;

CONIFEROPHYTA; FUNGI; HETEROBASIDION ANNOSUM; SACCHAROMYCES CEREVISIAE;

BASIDIOMYCOTA; CONIFEROPHYTA; GENE EXPRESSION; MITOGEN-ACTIVATED PROTEIN KINASES; OSMOSIS; OXIDATIVE STRESS; PLANT DISEASES; PLANT ROOTS; SACCHAROMYCES CEREVISIAE;

EID: 84856442969     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031186     Document Type: Article

References (47)

1. Widmann C, Gibson S, Jarpe MB, Johnson GL, (1999) Mitogen-activated protein kinase: Conservation of a three-kinase module from yeast to human. Physiol Rev 79: 143-180.
2. Smith DA, Morgan BA, Quinn J, (2010) Stress signalling to fungal stress-activated protein kinase pathways. FEMS Microbiol Lett 306: 1-8.
3. Brewster JL, Devaloir T, Dwyer ND, Winter E, Gustin MC, (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763.
4. Posas F, WurglerMurphy SM, Maeda T, Witten EA, Thai TC, et al. (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 86: 865-875.
5. Reiser V, Ruis H, Ammerer G, (1999) Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 10: 1147-1161.
6. Bilsland-Marchesan E, Swaminathan S, Molin C, Ramne A, Sunnerhagen P, (2003) Rck1 and Rck2 MAPKAP kinases mediate oxidative stress resistance from the HOG pathway. Yeast 20: S203-S203.
7. Alonso-Monge R, Navarro-Garcia F, Roman E, Negredo AI, Eisman B, et al. (2003) The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot Cell 2: 351-361.
8. Bahn YS, Kojima K, Cox GM, Heitman J, (2005) Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol Biol Cell 16: 2285-2300.
9. Kawasaki L, Sánchez O, Shiozaki K, Aguirre J, (2002) SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol 45: 1153-1163.
10. Ádám AL, Kohut G, Hornok L, (2008) Fphog1, a HOG-type MAP kinase gene, is involved in multistress response an Fusarium proliferatum. J Basic Microbiol 48: 151-159.
11. Dixon KP, Xu JR, Smirnoff N, Talbot NJ, (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11: 2045-2058.
12. Lin C, Chung K, (2010) Specialized and shared functions of the histidine kinase- and HOG1 MAP kinase-mediated signaling pathways in Alternaria alternata, a filamentous fungal pathogen of citrus. Fungal Genet Biol 47: 818-827.
13. Jin Y, Song WN, Nevo E, (2005) A MAPK gene from dead sea fungus confers stress tolerance to lithium salt and freezing-thawing: Prospects for saline agriculture. Proc Natl Acad Sci U S A 102: 18992-18997.
14. Zhang Y, Lamm R, Pillonel C, Lam S, Xu JR, (2002) Osmoregulation and fungicide resistance: The Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68: 532-538.
15. Eaton CJ, Jourdain I, Foster SJ, Hyams JS, Scott B, (2008) Functional analysis of a fungal endophyte stress-activated MAP kinase. Curr Genet 53: 163-174.
16. Niemela T, Korhonen K, (1998) Taxonomy of the genus Heterobasidion. In: Woodward S, Stenlid J, Karjalainen R, Hütterman A, editors. Heterobasidion annosum: Biology, Ecology, Impact and Control London CAB International pp. 27-34.
17. Asiegbu FO, Adomas A, Stenlid J, (2005) Conifer root and butt rot caused by Heterobasidion annosum (fr.) bref. s.l. Mol Plant Pathol 6: 395-409.
18. Vasiliauskas R, Stenlid J, (1998) Spread of S and P group isolates of Heterobasidion annosum within and among Picea abies trees in central Lithuania. Can J for Res-Rev can Rech for 28: 961-966.
19. Korhonen K, Stenlid J, (1998) Biology of Heterobasidion annosum. In: Woodward S, Stenlid J, Karjalainen R, Hütterman A, editors. Heterobasidion annosum: Biology, Ecology, Impact and Control London CAB International pp. 43-70.
20. Jones AS, (1953) The isolation of bacterial nucleic acids using cetyltrimethylammonium bromide (cetavlon). Biochim Biophys Acta 10: 607-612.
21. Pfaffl M, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
22. Rodaki A, Bohovych IM, Enjalbert B, Young T, Odds FC, et al. (2009) Glucose promotes stress resistance in the fungal pathogen Candida albicans. Mol Biol Cell 20: 4845-4855.
23. Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, et al. (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9: 44.
24. Segmüeller N, Ellendorf U, Tudzynski B, Tudzynski P, (2007) BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot Cell 6: 211-221.
25. Igbaria A, Lev S, Rose MS, Lee BN, Hadar R, et al. (2008) Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol Plant-Microbe Interact 21: 769-780.
26. Berridge MJ, Bootman MD, Roderick HL, (2003) Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529.
27. Silverman-Gavrila LB, Lew RP, (2001) Regulation of the tip-high [Ca2+] gradient in growing hyphae of the fungus Neurospora crassa. Eur J Cell Biol 80: 379-390.
28. Pinson-Gadais L, Richard-Forget F, Frasse P, Barreau C, Cahagnier B, et al. (2008) Magnesium represses trichothecene biosynthesis and modulates Tri5, Tri6, and Tri12 genes expression in Fusarium graminearum. Mycopathologia 165: 51-59.
29. Oliva J, Romeralo C, Stenlid J, (2011) Accuracy of the Rotfinder instrument in detecting decay on Norway spruce (Picea abies) trees. For Ecol Manage 262: 1378-1386.
30. Posas F, Chambers J, Heyman J, Hoeffler J, de Nadal E, et al. (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275: 17249-17255.
31. Albertyn J, Hohmann S, Thevelein J, Prior B, (1994) GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14: 4135-4144.
32. Lee S, Park S, Na J, Kim Y, (2002) Osmolarity hypersensitivity of hog1 deleted mutants is suppressed by mutation in KSS1 in budding yeast Saccharomyces cerevisiae. FEMS Microbiol Lett 209: 9-14.
33. Leonhardt S, Fearon K, Danese P, Mason T, (1993) Hsp78 encodes a yeast mitochondrial heat-shock protein in the clp family of ATP-dependent proteases. Mol Cell Biol 13: 6304-6313.
34. Miura T, Minegishi H, Usami R, Abe F, (2006) Systematic analysis of HSP gene expression and effects on cell growth and survival at high hydrostatic pressure in Saccharomyces cerevisiae. Extremophiles 10: 279-284.
35. Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R, et al. (2005) A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol Biol Cell 16: 2068-2076.
36. Kayingo G, Martins A, Andrie R, Neves L, Lucas C, et al. (2009) A permease encoded by STL1 is required for active glycerol uptake by Candida albicans. Microbiology-(UK) 155: 1547-1557.
37. Chen C, Porubleva L, Shearer G, Svrakic M, Holden L, et al. (2003) Associating protein activities with their genes: Rapid identification of a gene encoding a methylglyoxal reductase in the yeast Saccharomyces cerevisiae. Yeast 20: 545-554.
38. Posas F, Chambers J, Heyman J, Hoeffler J, de Nadal E, et al. (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275: 17249-17255.
39. Benito B, Garciadeblás B, Rodríguez-Navarro A, (2002) Potassium- or sodium-efflux ATPase, a key enzyme in the evolution of fungi. Microbiology-(UK) 148: 933-941.
40. Benito B, Garciadeblás B, Pérez-Martín J, Rodríguez-Navarro A, (2009) Growth at high pH and sodium and potassium tolerance in media above the cytoplasmic pH depend on ENA ATPases in Ustilago maydis. Eukaryot Cell 8: 821-829.
41. Antebi A, Fink GR, (1992) The yeast Ca2+-ATPase homologue, PMR1, is required for normal golgi function and localizes in a novel golgi-like distribution. Mol Biol Cell 3: 633-654.
42. Marchi V, Sorin A, Wei Y, Rao R, (1999) Induction of vacuolar Ca2+-ATPase and H+/Ca2+ exchange activity in yeast mutants lacking Pmr1, the golgi Ca2+-ATPase. FEBS Lett 454: 181-186.
43. Hernandez-Lopez MJ, Randez-Gil F, Prieto JA, (2006) Hog1 mitogen-activated protein kinase plays conserved and distinct roles in the osmotolerant yeast Torulaspora delbrueckii. Eukaryot Cell 5: 1410-1419.
44. Takatsume Y, Ohdate T, Maeta K, Nomura W, Izawa S, et al. (2010) Calcineurin/Crz1 destabilizes Msn2 and Msn4 in the nucleus in response to Ca2+ in Saccharomyces cerevisiae. Biochem J 427: 275-287.
45. Qian J, Qin X, Yin Q, Chu J, Wang Y, (2011) Cloning and characterization of Kluyveromyces marxianus Hog1 gene. Biotechnol Lett 33: 571-575.
46. Reiser V, Ruis H, Ammerer G, (1999) Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 10: 1147-1161.
47. Bilsland E, Molin C, Swaminathan S, Ramne A, Sunnerhagen P, (2004) Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol 53: 1743-1756.