The ethylene pathway contributes to root hair elongation induced by the beneficial bacteria Phyllobacterium brassicacearum STM196

Plant Science

Volumn 190, Issue , 2012, Pages 74-81

  Galland, Marc ^a,c   Gamet, Lydia ^a   Varoquaux, Fabrice ^a   Touraine, Brigitte ^b   Touraine, Bruno ^a   Desbrosses, Guilhem ^a  

^a CIRAD   (France)

^b CNRS   (France)

^c CEMAGREF   (France)

Author keywords

Arabidopsis; Ethylene; Plant growth promoting rhizobacteria; Root hairs

Indexed keywords

ARABIDOPSIS PROTEIN; ETHYLENE; ETHYLENE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; MESSENGER RNA;

ARABIDOPSIS; ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; PHYLLOBACTERIACEAE; PHYSIOLOGY; PLANT ROOT; PROTEIN STABILITY; SEEDLING; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; INDOLEACETIC ACIDS; MUTATION; PHYLLOBACTERIACEAE; PLANT ROOTS; PROTEIN STABILITY; RNA, MESSENGER; SEEDLING; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); BRASSICA NAPUS; PHYLLOBACTERIUM BRASSICACEARUM; RHIZOBIALES;

EID: 84860118012     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2012.03.008     Document Type: Article

References (71)

1. Lugtenberg B.J., Kamilova F. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 2009, 63:541-556.
2. Van Wees S.C., Van der Ent S., Pieterse C.M. Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology 2008, 11:443-448.
3. Bertrand H., Plassard C., Pinochet X., Touraine B., Normand P., Cleyet-Marel J.C. Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Canadian Journal of Microbiology 2000, 46:229-236.
4. Vessey J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 2003, 255:571-586.
5. Mantelin S., Touraine B. Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. Journal of Experimental Botany 2004, 55:27-34.
6. Lucy M., Reed E., Glick B.R. Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2004, 86:1-25.
7. Gupta A., Gopal M., Tilak K.V. Mechanism of plant growth promotion by rhizobacteria. Indian Journal of Experimental Biology 2000, 38:856-862.
8. Barbieri P., Galli E. Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Research in Microbiology 1993, 144:69-75.
9. Malhotra M., Srivastava S. An ipdC gene knock-out of Azospirillum brasilense strain SM and its implications on indole-3-acetic acid biosynthesis and plant growth promotion. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 2008, 93:425-433.
10. Patten C.L., Glick B.R. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Applied and Environment Microbiology 2002, 68:3795-3801.
11. Suzuki S., He Y., Oyaizu H. Indole-3-acetic acid production in Pseudomonas fluorescens HP72 and its association with suppression of creeping bentgrass brown patch. Current Microbiology 2003, 47:138-143.
12. Blaha D., Prigent-Combaret C., Mirza M.S., Moenne-Loccoz Y. Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiology Ecology 2006, 56:455-470.
13. Contesto C., Desbrosses G., Lefoulon C., Bena G., Borel F., Galland M., Gamet L., Varoquaux F., Touraine B. Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Science 2008, 1/2:178-189.
14. Okazaki S., Nukui N., Sugawara M., Minamisawa K. Rhizobial strategies to enhanced symbiotic interaction: rhizobitoxine and 1-aminocyclopropane-1-carboxylate deaminase. Microbes and Environments 2004, 19:99-111.
15. Glick B.R. Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiology Letters 2005, 251:1-7.
16. Lopez-Bucio J., Campos-Cuevas J.C., Hernandez-Calderon E., Velasquez-Becerra C., Farias-Rodriguez R., Macias-Rodriguez L.I., Valencia-Cantero E. Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 2007, 20:207-217.
17. Ribaudo C.M., Krumpholz E., Cassan F.D., Bottini R., Cantoren M., Cura J. Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. Journal of Plant Growth Regulation 2006, 24:175-185.
18. Kapulnik Y., Okon Y., Henis Y. Changes in root morphology of wheat caused by Azospirillum inoculation. Canadian Journal of Microbiology 1985, 31:881-887.
19. Dobbelaere S., Croonenborghs A., Thys A., Vande Broek A., Vanderleyden J. Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 1999, 212:153-162.
20. Grebe M., Friml J., Swarup R., Ljung K., Sandberg G., Terlou M., Palme K., Bennett M.J., Scheres B. Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Current Biology 2002, 12:329-334.
21. Ikeda Y., Men S., Fischer U., Stepanova A.N., Alonso J.M., Ljung K., Grebe M. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nature Cell Biology 2009, 11:731-738.
22. Jones A.R., Kramer E.M., Knox K., Swarup R., Bennett M.J., Lazarus C.M., Leyser H.M., Grierson C.S. Auxin transport through non-hair cells sustains root-hair development. Nature Cell Biology 2009, 11:78-84.
23. Knox K., Grierson C.S., Leyser O. AXR3 and SHY2 interact to regulate root-hair development. Development 2003, 130:5769-5777.
24. Masucci J.D., Schiefelbein J.W. Hormones act downstream of TTG and GL2 to promote root-hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 1996, 8:1505-1517.
25. Pitts R.J., Cernac A., Estelle M. Auxin and ethylene promote root-hair elongation in Arabidopsis. Plant Journal 1998, 16:553-560.
26. Rahman A., Hosokawa S., Oono Y., Amakawa T., Goto N., Tsurumi S. Auxin and ethylene response interactions during Arabidopsis root-hair development dissected by auxin influx modulators. Plant Physiology 2002, 130:1908-1917.
27. Leon-Kloosterziel K.M., Verhagen B.W., Keurentjes J.J., VanPelt J.A., Rep M., VanLoon L.C., Pieterse C.M. Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Molecular Biology 2005, 57:731-748.
28. Li J., Ovakim D.H., Charles T.C., Glick B.R. An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Current Microbiology 2000, 41:101-105.
29. Knoester M., Pieterse C.M., Bol J.F., Van Loon L.C. Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signalling at the site of application. Molecular Plant-Microbe Interactions 1999, 12:720-727.
30. Pieterse C.M., van Wees S.C., van Pelt J.A., Knoester M., Laan R., Gerrits H., Weisbeek P.J., van Loon L.C. A novel signalling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 1998, 10:1571-1580.
31. Bertrand H., Nalin R., Bally R., Cleyet-Marel J.C. Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biology and Fertility of Soils 2001, 33:152-156.
32. Mantelin S., Saux M.F., Zakhia F., Bena G., Bonneau S., Jeder H., de Lajudie P., Cleyet-Marel J.C. Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots: Phyllobacterium bourgognense sp. nov., Phyllobacterium ifriqiyense sp. nov., Phyllobacterium leguminum sp. nov. and Phyllobacterium brassicacearum sp. nov. International Journal of Systematic and Evolutionary Microbiology 2006, 56:827-839.
33. Mantelin S., Desbrosses G., Larcher M., Tranbarger T.J., Cleyet-Marel J.C., Touraine B. Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 2006, 223:591-603.
34. Czechowski T., Stitt M., Altmann T., Udvardi M.K., Scheible W.R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 2005, 139:5-17.
35. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
36. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
37. Yanagisawa S., Yoo S.D., Sheen J. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 2003, 425:521-525.
38. Konishi M., Yanagisawa S. Ethylene signalling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant Journal 2008, 55:821-831.
39. Guzman P., Ecker J.R. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 1990, 2:513-523.
40. Kieber J.J., Rothenberg M., Roman G., Feldmann K.A., Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 1993, 72:427-441.
41. Contesto C., Milesi S., Mantelin S., Zancarini A., Desbrosses G., Varoquaux F., Bellini C., Kowalczyk M., Touraine B. The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 2010, 232:1455-1470.
42. Normanly J., Bartel B. Redundancy as a way of life-IAA metabolism. Current Opinion in Plant Biology 1999, 2:207-213.
43. Stepanova A.N., Hoyt J.M., Hamilton A.A., Alonso J.M. A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 2005, 17:2230-2242.
44. Abel S., Nguyen M.D., Chow W., Theologis A. ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. Journal of Biological Chemistry 1995, 270:19093-19099.
45. Tsuchisaka A., Theologis A. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiology 2004, 136:2982-3000.
46. Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K., Scheres B. Cellular organisation of the Arabidopsis thaliana root. Development 1993, 119:71-84.
47. Potuschak T., Vansiri A., Binder B.M., Lechner E., Vierstra R.D., Genschik P. The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell 2006, 18:3047-3057.
48. Olmedo G., Guo H., Gregory B.D., Nourizadeh S.D., Aguilar-Henonin L., Li H., An F., Guzman P., Ecker J.R. ETHYLENE-INSENSITIVE5 encodes a 5'→3' exoribonuclease required for regulation of the EIN3-targeting F-box proteins EBF1/2. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:13286-13293.
49. Gagne J.M., Smalle J., Gingerich D.J., Walker J.M., Yoo S.D., Yanagisawa S., Vierstra R.D. Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:6803-6808.
50. Guo H., Ecker J.R. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 2003, 115:667-677.
51. Potuschak T., Lechner E., Parmentier Y., Yanagisawa S., Grava S., Koncz C., Genschik P. EIN3-dependent regulation of plant ethylene hormone signalling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 2003, 115:679-689.
52. He J., Benedito V.A., Wang M., Murray J.D., Zhao P.X., Tang Y., Udvardi M.K. The Medicago truncatula gene expression atlas web server. BMC Bioinformatics 2009, 10:441.
53. Høgslund N., Radutoiu S., Krusell L., Voroshilova V., Hannah M.A., Goffard N., Sanchez D.H., Lippold F., Ott T., Sato S., Tabata S., Liboriussen P., Lohmann G.V., Schauser L., Weiller G.F., Udvardi M.K., Stougaard J. Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS One 2009, 4:e6556.
54. Alonso J.M., Hirayama T., Roman G., Nourizadeh S., Ecker J.R. EIN2 a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 1999, 284:2148-2152.
55. Chao Q.M., Rothenberg M., Solano R., Roman G., Terzaghi W., Ecker J.R. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 1997, 89:1133-1144.
56. Chang C., Kwok S.F., Bleecker A.B., Meyerowitz E.M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 1993, 262:539-544.
57. Alonso J.M., Stepanova A.N., Solano R., Wisman E., Ferrari S., Ausubel F.M., Ecker J.R. Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:2992-2997.
58. Binder B.M., Mortimore L.A., Stepanova A.N., Ecker J.R., Bleecker A.B. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent. Plant Physiology 2004, 136:2921-2927.
59. Penmetsa R.V., Uribe P., Anderson J., Lichtenzveig J., Gish J.C., Nam Y.W., Engstrom E., Xu K., Sckisel G., Pereira M., Baek J.M., Lopez-Meyer M., Long S.R., Harrison M.J., Singh K.B., Kiss G.B., Cook D.R. The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant Journal 2008, 55:580-595.
60. Hunter W.J. Ethylene production by root nodules and effect of ethylene on nodulation in Glycine max. Applied and Environment Microbiology 1993, 59:1947-1950.
61. Desbrosses G.J., Stougaard J. Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 2011, 10:348-358.
62. Dong X. SA, JA, ethylene, and disease resistance in plants. Current Opinion in Plant Biology 1998, 1:316-323.
63. Broekaert W.F., Delaure S.L., De Bolle M.F., Cammue B.P. The role of ethylene in host-pathogen interactions. Annual Review of Phytopathology 2006, 44:393-416.
64. Zhu C., Gan L., Shen Z., Xia K. Interactions between jasmonates and ethylene in the regulation of root-hair development in Arabidopsis. Journal of Experimental Botany 2006, 57:1299-1308.
65. Zhu Z., An F., Feng Y., Li P., Xue L., Jiang M.A.Z., Kim J.M., To T.K., Li W., Zhang X., Yu Q., Dong Z., Chen W.Q., Seki M., Zhou J.M., Guo H. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signalling synergy in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:12539-12544.
66. Stepanova A.N., Alonso J.M. Ethylene signalling and response: where different regulatory modules meet. Current Opinion in Plant Biology 2009, 12:548-555.
67. Desbrosses G., Contesto C., Varoquaux F., Galland M., Touraine B. PGPR-Arabidopsis interactions is a useful system to study signalling pathways involved in plant developmental control. Plant Signaling & Behavior 2009, 4:321-323.
68. Dubrovsky J.G., Esther Puente M., Bashan Y. Arabidopsis thaliana as a model system for the study of the effect of inoculation by Azospirillum brasilense SP-245 on root-hair growth. Soil Biology and Biochemistry 1994, 26:1657-1664.
69. Ortiz-Castro R., Diaz-Perez C., Martinez-Trujillo M., del Rio R.E., Campos-Garcia J., Lopez-Bucio J. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:7253-7258.
70. Ortiz-Castro R., Martinez-Trujillo M., Lopez-Bucio J. N-acyl-l-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 2008, 31:1497-1509.
71. Karas B., Amyot L., Johansen C., Sato S., Tabata S., Kawaguchi M., Szczyglowski K. Conservation of lotus and Arabidopsis basic helix-loop-helix proteins reveals new players in root-hair development. Plant Physiology 2009, 151:1175-1185.