Barley mildew and its elicitor chitosan promote closed stomata by stimulating guard-cell S-type anion channels

Plant Journal

Volumn 68, Issue 4, 2011, Pages 670-680

  Koers, Sandra ^a   Guzel Deger, Aysin ^b   Marten, Irene ^a   Roelfsema, M Rob G ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b MERSIN UNIVERSITY   (Turkey)

Author keywords

Blumeria graminis; chitosan; guard cell; Hordeum vulgare; light dependent; plasma membrane potential; S type anion channel

Indexed keywords

ANION CHANNELS; BLUMERIA GRAMINIS; GUARD CELLS; HORDEUM VULGARE; LIGHT-DEPENDENT; PLASMA MEMBRANE POTENTIAL;

CELL MEMBRANES; CHITOSAN; FUNGI; NEGATIVE IONS; PLANT SHUTDOWNS; PLASMAS;

CYTOLOGY;

CHITOSAN; ION CHANNEL; POTASSIUM;

ARTICLE; ASCOMYCETES; CELL MEMBRANE POTENTIAL; CHANNEL GATING; FUNGUS HYPHAE; HORDEUM; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT STOMA;

ASCOMYCOTA; CHITOSAN; HORDEUM; HOST-PATHOGEN INTERACTIONS; HYPHAE; ION CHANNEL GATING; ION CHANNELS; MEMBRANE POTENTIALS; PLANT DISEASES; PLANT STOMATA; POTASSIUM;

BLUMERIA GRAMINIS; FUNGI; HORDEUM; HORDEUM VULGARE;

EID: 80855123473     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04719.x     Document Type: Article

References (73)

1. +-sensing ion channel. FEBS Lett. 486, 93-98.
2. + channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. Plant J. 19, 453-462.
3. Blume, B., Nürnberger, T., Nass, N., and, Scheel, D., (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell, 12, 1425-1440.
4. Boller, T., and, Felix, G., (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379-406.
5. Both, M., Csukai, M., Stumpf, M.P.H., and, Spanu, P.D., (2005) Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell, 17, 2107-2122.
6. + channels between guard cells and subsidiary cells within the maize stomatal complex. Planta, 222, 968-976. (Pubitemid 41706034)
7. Carden, D.E., and, Felle, H.H., (2003) The mode of action of cell wall-degrading enzymes and their interference with Nod factor signalling in Medicago sativa root hairs. Planta, 216, 993-1002. (Pubitemid 36761708)
8. Carver, T.L.W., Ingerson-Morris, S.M., Thomas, B.J., and, Gay, A.P., (1994) Light-mediated delay of primary haustorium formation by erysiphe-graminis f.sp avenae. Physiol. Mol. Plant Pathol. 45, 59-79. (Pubitemid 2127206)
9. 2+ concentration and protein phosphorylation. Plant J. 61, 816-825.
10. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nurnberger, T., Jones, J.D.G., Felix, G., and, Boller, T., (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 448, 497-500. (Pubitemid 47123516)
11. Colcombet, J., Mathieu, Y., Peyronnet, R., Agier, N., Lelievre, F., Barbier-Brygoo, H., and, Frachisse, J.M., (2009) R-type anion channel activation is an essential step for ROS-dependent innate immune response in Arabidopsis suspension cells. Funct. Plant Biol. 36, 832-843.
12. El-Maarouf, H., Barny, M.A., Rona, J.P., and, Bouteau, F., (2001) Harpin, a hypersensitive response elicitor from Erwinia amylovora, regulates ion channel activities in Arabidopsis thaliana suspension cells. FEBS Lett. 497, 82-84. (Pubitemid 32476881)
13. + current across the plasma-membrane of guard cells from a grass -Zea mays. Planta, 186, 282-293.
14. Felix, G., Regenass, M., and, 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.
15. Felix, G., Duran, J.D., Volko, S., and, Boller, T., (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276.
16. Felle, H.H., Kondorosi, E., Kondorosi, A., and, Schultze, M., (2000) How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. Plant Physiol. 124, 1373-1380.
17. Felle, H.H., Herrmann, A., Hanstein, S., Hückelhoven, R., and, Kogel, K.H., (2004) Apoplastic pH signaling in barley leaves attacked by the powdery mildew fungus Blumeria graminis f. sp hordei. Mol. Plant Microbe Interact. 17, 118-123. (Pubitemid 38398234)
18. Felle, H.H., Herrmann, A., Schaefer, P., Hueckelhoven, R., and, Kogel, K.H., (2008) Interactive signal transfer between host and pathogen during successful infection of barley leaves by Blumeria graminis and Bipolaris sorokiniana. J. Plant Physiol. 165, 52-59. (Pubitemid 350266914)
19. Geiger, D., Scherzer, S., Mumm, P., et al. (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl Acad. Sci. USA, 106, 21425-21430.
20. 2+ affinities. Proc. Natl Acad. Sci. USA, 107, 8023-8028.
21. Geiger, D., Maierhofer, T., Al-Rasheid, K.A.S., et al. (2011) Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci. Signal. 4, ra32.
22. Hanstein, S.M., and, Felle, H.H., (2004) Nanoinfusion: an integrating tool to study elicitor perception and signal transduction in intact leaves. New Phytol. 161, 595-606. (Pubitemid 38126971)
23. 2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. EMBO J. 9, 3889-3892. (Pubitemid 20379978)
24. Hückelhoven, R., Fodor, J., Preis, C., and, Kogel, K.H., (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol. 119, 1251-1260. (Pubitemid 29388219)
25. 2+-associated opening of plasma membrane anion channels. Plant J. 62, 367-378.
26. Jones, J.D.G., and, Dangl, J.L., (2006) The plant immune system. Nature, 444, 323-329. (Pubitemid 44764102)
27. Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., and, Shibuya, N., (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl Acad. Sci. USA, 103, 11086-11091. (Pubitemid 44148422)
28. Krol, E., Mentzel, T., Chinchilla, D., et al. (2010) Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 285, 13471-13479.
29. Kuchitsu, K., Yazaki, Y., Sakano, K., and, Shibuya, N., (1997) Transient cytoplasmic pH change and ion fluxes through the plasma membrane in suspension-cultured rice cells triggered by N-acetylchitooligosaccharide elicitor. Plant Cell Physiol. 38, 1012-1018. (Pubitemid 27434082)
30. Lecourieux, D., Lamotte, O., Bourque, S., Wendehenne, D., Mazars, C., Ranjeva, R., and, Pugin, A., (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium, 38, 527-538. (Pubitemid 41614432)
31. Lee, S., Choi, H., Suh, S., Doo, I.S., Oh, K.Y., Choi, E.J., Taylor, A.T.S., Low, P.S., and, Lee, Y., (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol. 121, 147-152. (Pubitemid 29452000)
32. Lee, S.C., Lan, W.Z., Buchanan, B.B., and, Luan, S., (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl Acad. Sci. USA, 106, 21419-21424.
33. Lin, M.R., and, Edwards, H.H., (1974) Primary penetration process in powdery mildew related to host-cell age, cell type, and occurence of basic staining material. New Phytol. 73, 131-137.
34. Linder, B., and, Raschke, K., (1992) A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing. FEBS Lett. 313, 27-30.
35. +-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol. 7, e1000139.
36. Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., and, Grill, E., (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064-1068.
37. MacRobbie, E.A.C., (1987) Ionic relations of guard cells. In Stomatal Function (, Zeiger, E., Farquhar, G.D., and, Cowan, I.R., eds). Palo Alto, CA: Stanford University Press, pp. 125-162.
38. Maffi, D., Bassi, M., Brambilla, A., and, Conti, C.G., (1998) Possible role of chitosan in the interaction between barley and Erysiphe graminis after tetraconazole treatment. Mycol. Res. 102, 599-606. (Pubitemid 28278463)
39. 2+ signals in Nicotiana tabacum guard cells. Plant J. 55, 698-708.
40. Melotto, M., Underwood, W., Koczan, J., Nomura, K., and, He, S.Y., (2006) Plant stomata function in innate immunity against bacterial invasion. Cell, 126, 969-980. (Pubitemid 44310774)
41. Melotto, M., Underwood, W., and, He, S.Y., (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol. 46, 101-122.
42. +-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J. 26, 3216-3226. (Pubitemid 47057490)
43. Mithofer, A., Ebel, J., and, Felle, H.H., (2005) Cation fluxes cause plasma membrane depolarization involved in β-glucan elicitor-signaling in soybean roots. Mol. Plant Microbe Interact. 18, 983-990. (Pubitemid 41170162)
44. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H., and, Shibuya, N., (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl Acad. Sci. USA, 104, 19613-19618.
45. Mustilli, A.C., Merlot, S., Vavasseur, A., Fenzi, F., and, Giraudat, J., (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell, 14, 3089-3099. (Pubitemid 36029134)
46. Nürnberger, T., and, Kemmerling, B., (2006) Receptor protein kinases-pattern recognition receptors in plant immunity. Trends Plant Sci. 11, 519-522. (Pubitemid 44636303)
47. Park, S.Y., Fung, P., Nishimura, N., et al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068-1071.
48. Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M., and, Schroeder, J.I., (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell, 9, 409-423. (Pubitemid 27176827)
49. Pelissier, B., Thibaud, J.B., Grignon, C., and, Esquerretugaye, M.T., (1986) Cell surfaces in plant-microorganism interactions. VII. Elicitor preparations from two fungal pathogens depolarize plant membranes. Plant Sci. 46, 103-109.
50. Prats, E., Gay, A.P., Mur, L.A.J., Thomas, B.J., and, Carver, T.L.W., (2006) Stomatal lock-open, a consequence of epidermal cell death, follows transient suppression of stomatal opening in barley attacked by Blumeria graminis. J. Exp. Bot. 57, 2211-2226. (Pubitemid 44289117)
51. Prats, E., Gay, A.P., Roberts, P.C., Thomas, B.J., Sanderson, R., Paveley, N., Lyngkjaer, M.F., Carver, T.L.W., and, Mur, L.A.J., (2010) Blumeria graminis interactions with barley conditioned by different single R genes demonstrate a temporal and spatial relationship between stomatal dysfunction and cell death. Phytopathology, 100, 21-32.
52. 2+ signals induced by abiotic and biotic stresses. Plant J. 53, 287-299.
53. Raschke, K., and, Fellows, M.P., (1971) Stomatal movement in Zea mays- shuttle of potassium and chloride between guard cells and subsidiary cells. Planta, 101, 296-316.
54. Raschke, K., Hedrich, R., Reckmann, U., and, Schroeder, J.I., (1988) Exploring biophysical and biochemical components of the osmotic motor that drives stomatal movement. Bot. Acta, 101, 283-294.
55. Read, N.D., Kellock, L.J., Collins, T.J., and, Gundlach, A.M., (1997) Role of topography sensing for infection-structure differentiation in cereal rust fungi. Planta, 202, 163-170. (Pubitemid 27243117)
56. Roelfsema, M.R.G., and, Hedrich, R., (2005) In the light of stomatal opening: new insights into 'the Watergate'. New Phytol. 167, 665-691. (Pubitemid 43923805)
57. Roelfsema, M.R.G., Steinmeyer, R., Staal, M., and, Hedrich, R., (2001) Single guard cell recordings in intact plants: light-induced hyperpolarization of the plasma membrane. Plant J. 26, 1-13. (Pubitemid 32489179)
58. Roelfsema, M.R.G., Levchenko, V., and, Hedrich, R., (2004) ABA depolarizes guard cells in intact plants, through a transient activation of R- and S-type anion channels. Plant J. 37, 578-588. (Pubitemid 38258778)
59. Ron, M., and, Avni, A., (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell, 16, 1604-1615. (Pubitemid 38774252)
60. Ryan, C.A., (1987) Oligosaccharide signaling in plants. Annu. Rev. Cell Biol. 3, 295-317.
61. Schmidt, C., and, Schroeder, J.I., (1994) Anion selectivity of slow anion channels in the plasma membrane of guard cells: large nitrate permeability. Plant Physiol. 106, 383-391.
62. Schroeder, J.I., and, Hagiwara, S., (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature, 338, 427-430.
63. Schroeder, J.I., and, Keller, B.U., (1992) Two types of anion channel currents in guard cells with distinct voltage regulation. Proc. Natl Acad. Sci. USA, 89, 5025-5029.
64. Schulze-Lefert, P., and, Panstruga, R., (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16, 117-125.
65. Shimazaki, K.I., Doi, M., Assmann, S.M., and, Kinoshita, T., (2007) Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58, 219-247. (Pubitemid 46986324)
66. Shimizu, T., Nakano, T., Takamizawa, D., et al. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204-214.
67. 2+-dependent activation of guard cell anion channels, triggered by hyperpolarization, is promoted by prolonged depolarization. Plant J. 62, 265-276.
68. Szyroki, A., Ivashikina, N., Dietrich, P., et al. (2001) KAT1 is not essential for stomatal opening. Proc. Natl Acad. Sci. USA, 98, 2917-2921. (Pubitemid 32209584)
69. Vahisalu, T., Kollist, H., Wang, Y.F., et al. (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature, 452, 487-491. (Pubitemid 351450835)
70. Vahisalu, T., Puzorjova, I., Brosche, M., et al. (2010) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J. 62, 442-453.
71. + transport in higher plants. Annu. Rev. Plant Biol. 54, 575-603. (Pubitemid 37400006)
72. Wendehenne, D., Lamotte, O., Frachisse, J.M., Barbier-Brygoo, H., and, Pugin, A., (2002) Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell, 14, 1937-1951. (Pubitemid 35002943)
73. Zhang, Z., Henderson, C., Perfect, E., Carver, T.L.W., Thomas, B.J., Skamnioti, P., and, Gurr, S.J., (2005) Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. Mol. Plant Pathol. 6, 561-575. (Pubitemid 43942895)