Changes in extracellular pH are neither required nor sufficient for activation of mitogen-activated protein kinases (MAPKs) in response to systemin and fusicoccin in tomato

Planta

Volumn 225, Issue 6, 2007, Pages 1535-1546

  Higgins, Rebecca ^a   Lockwood, Thomas ^a,b   Holley, Susan ^a   Yalamanchili, Roopa ^a   Stratmann, Johannes W ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Fusicoccin; LeMPK; MAPK; Plant stress responses; Plasma membrane proton ATPase; Systemin; Tomato

Indexed keywords

FUSICOCCIN; GLYCOSIDE; MITOGEN ACTIVATED PROTEIN KINASE; MYCOTOXIN; PEPTIDE; SYSTEMIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CHEMISTRY; DRUG EFFECT; ENZYME ACTIVATION; EXTRACELLULAR FLUID; METABOLISM; PH; PLANT LEAF; TOMATO;

ENZYME ACTIVATION; EXTRACELLULAR FLUID; GLYCOSIDES; HYDROGEN-ION CONCENTRATION; LYCOPERSICON ESCULENTUM; MITOGEN-ACTIVATED PROTEIN KINASES; MYCOTOXINS; PEPTIDES; PLANT LEAVES; PLANT PROTEINS;

LYCOPERSICON ESCULENTUM;

EID: 34247352872     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-006-0440-8     Document Type: Article

References (54)

1. Arango M, Gévaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355-365
2. Bergey DR, Howe G, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93:12053-12058
3. Bögre L, Ligterink W, Meskiene I, Barker PJ, Heberle-Bors E, Huskisson NS, Hirt H (1997) Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell 9:75-83
4. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237-19242
5. De Jong CF, Honee G, Joosten MHAJ, De Wit PJGM (2000) Early defence responses induced by AVR9 and mutant analogues in tobacco cell suspensions expressing the Cf-9 resistance gene. Physiol Mol Plant Pathol 56:169-177
6. Felix G, Boller T (1995) Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant J 7:381-389
7. Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 4:307-316
8. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265-276
9. Frick U, Schaller A (2002) cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants. Planta 216:83-94
10. Granado J, Felix G, Boller T (1995) Perception of fungal sterols in plants. Plant Phys 107:485-490
11. Halitschke R, Gase K, Hui D, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Phys 131:1894-1902
12. Hamel L-P, Nicole M-C, Sritubtim S, Morency M-J, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192-198
13. Hirt H (1999) Transcriptional upregulation of signaling pathways: more complex than anticipated? Trends Plant Sci 4:7-8
14. Holley SR, Yalamanchili RD, Moura SD, Ryan CA, Stratmann JW (2003) Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol 132:1728-1738
15. Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223-237
16. Ichimura K et al (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301-308
17. Izaguirre M, Scopel AL, Baldwin IT, Ballaré CL (2003) Convergent responses to stress. Solar UV-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in Weld-grown plants of Nicotiana longiflora. Plant Physiol 132:1755-1767
18. Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud J-L, Boutry M (2005) Activation of the plant plasma membrane H + -ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer. Proc Natl Acad Sci USA 102:11675-11680
19. Kao S-C, Jaiswal RK, Kolch W, Landreth GE (2001) Identification of the mechanisms regulating the differential activation of the MAPK cascade by epidermal growth factor and nerve growth factor in PC12 cells. J Biol Chem 276:18169-18177
20. Lapous D, Mathieu Y, Guern J, Laurière C (1998) Increase of defense gene transcripts by cytoplasmic acidification in tobacco cell suspensions. Planta 205:452-458
21. Lebrun-Garcia A, Ouaked F, Chiltz A, Pugin A (1998) Activation of MAPK homologues by elicitors in tobacco cells. Plant J 15:773-781
22. Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567-576
23. Maffei M, Bossi S, Spiteller D, Mithofer A, Boland W (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 134:1752-1762
24. Malone M (1996) Rapid, long-distance signal transmission in higher plants. In: Callow JA (ed) Advances in botanical research, vol 22. Academic, New York, pp 163-228
25. Marré E (1979) Fusicoccin: a tool in plant biology. Ann Rev Plant Physiol 30:273-288
26. Mayrose M, Bonshtien A, Sessa G (2004) LeMPK3 is a mitogen-activated protein kinase with dual specificity induced during tomato defense and wounding responses. J Biol Chem 279:14819-14827
27. McGurl B, Pearce G, Orozco-Cardenas ML, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255:1570-1573
28. Meindl T, Boller T, Felix G (1998) The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10:1561-1570
29. Moyen C, Johannes E (1996) Systemin transiently depolarizes the tomato mesophyll cell membrane and antagonizes fusicoccin-induced extracellular acidification of mesophyll tissue. Plant Cell Environ 19:464-470
30. Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB (2002) Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J 32:299-315
31. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339-346
32. Oecking C, Piotrowski M, Hagemeier J, Hagemann K (1997) Topology and target interaction of the fusicoccin-binding 14-3-3 homologs of Commelina communis. Plant J 12:441-453
33. Pearce G, Ryan CA (2003) Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J Biol Chem 278:30044-30050
34. Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induced wound-inducible proteinase inhibitor proteins. Science 253:895-898
35. Pearce G, Moura D, Stratmann J, Ryan CA (2001a) Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817-820
36. Pearce G, Moura D, Stratmann J, Ryan CA (2001b) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 98:12843-12847
37. Pedley KF, Martin GB (2004) Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J Biol Chem 279:49229-49235
38. Rhodes JD, Thain JF, Wildon CD (1996) The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200:50-57
39. Romeis T, Piedras P, Zhang S, Klessig DF, Hirt H, Jones JDG (1999) Rapid avr9- and cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11:273-287
40. Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112-121
41. Sabbagh WJ, Flatauer LJ, Bardwell J, Bardwell L (2001) Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol Cell 8:683-691
42. +-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263-272
43. Schaller A, Phillipe R, Amrhein N (2000) Salicylic acid-independent induction of pathogenesis-related gene expression by fusicoccin. Planta 210:599-606
44. Scheer J, Ryan CA (1999) A 160-kD systemin receptor on the surface of Lycopersicon peruvianum suspension-cultured cells. Plant Cell 11:1525-1535
45. Singh J, Roberts MR (2004) Fusicoccin activates pathogen-responsive gene expression independently of common resistance signalling pathways, but increases disease symptoms in Pseudomonas syringae-infected tomato plants. Planta 219:261-269
46. Stahlberg R, Cosgrove D (1996) Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. Planta 200:416-425
47. Stratmann J, Scheer J, Ryan CA (2000) Suramin inhibits initiation of defense signaling by systemin, chitosan and pmg-elicitor in suspension cultured Lycopersicon peruvianum cells. Proc Natl Acad Sci USA 97:8862-8867
48. Stratmann JW, Ryan CA (1997) Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc Natl Acad Sci USA 94:11085-11089
49. Thain JF, Gubb IR, Wildon DC (1995) Depolarization of tomato leaf cells by oligogalacturonide elicitors. Plant Cell Environ 18:211-214
50. Vera-Estrella R, Higgins VJ, Blumwald E (1994) Plant defense response to fungal pathogens. Plant Physiol 106:97-102
51. Yalamanchili RD, Stratmann J (2002) Ultraviolet-B activates components of the systemin signaling pathway in Lycopersicon peruvianum suspension-cultured cells. J Biol Chem 277:28424-28430
52. Zhang S, Klessig DF (1998a) The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci USA 95:7225-7230
53. Zhang S, Klessig DF (2000) Pathogen-induced MAP kinases in tobacco. Results Probl Cell Differ 27:65-84
54. Zhang S, Du H, Klessig DF (1998b) Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10:435-449