Unraveling root developmental programs initiated by beneficial Pseudomonas spp. Bacteria

Plant Physiology

Volumn 162, Issue 1, 2013, Pages 304-318

  Zamioudis, Christos ^a   Mastranesti, Parthena ^a   Dhonukshe, Pankaj ^a,b   Blilou, Ikram ^a,c   Pieterse, Corné M J ^a,d  

^a UTRECHT UNIVERSITY   (Netherlands)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEACETIC ACID DERIVATIVE;

ARABIDOPSIS; ARTICLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT ROOT; PSEUDOMONAS; SEEDLING; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; MUTATION; PHENOTYPE; PLANT ROOTS; PSEUDOMONAS; SEEDLING; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); PSEUDOMONAS; RHIZOBIALES;

EID: 84877026599     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.212597     Document Type: Article

References (82)

1. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120
2. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9: 26-32.
3. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
4. Benková E, Bielach A (2010) Lateral root organogenesis: from cell to organ. Curr Opin Plant Biol 13: 677-683.
5. Bennett T, Scheres B (2010) Root development: two meristems for the price of one? Curr Top Dev Biol 91: 67-102.
6. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486.
7. Binder BM, Walker JM, Gagne JM, Emborg TJ, Hemmann G, Bleecker AB, Vierstra RD (2007) The Arabidopsis EIN3 binding F-box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19: 509-523.
8. Bisseling T, Dangl JL, Schulze-Lefert P (2009) Next-generation communication. Science 324: 691.
9. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
10. Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13: 3047-3058.
11. Brown SD, Utturkar SM, Klingeman DM, Johnson CM, Martin SL, Land ML, Lu T-YS, Schadt CW, Doktycz MJ, Pelletier DA (2012) Twenty-one genome sequences from Pseudomonas species and 19 genome sequences from diverse bacteria isolated from the rhizosphere and endosphere of Populus deltoides. J Bacteriol 194: 5991-5993.
12. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91-95.
13. Campanoni P, Nick P (2005) Auxin-dependent cell division and cell elongation: 1-naphthaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol 137: 939-948.
14. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang HM, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8: 165-171.
15. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89: 1133-1144.
16. Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, et al (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23: 3335-3352.
17. Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Spatiotemporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20: 503-508.
18. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, et al (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19: 1062-1071.
19. Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxindependent mechanism in Arabidopsis. Plant Physiol 149: 1579-1592.
20. Crookshanks M, Taylor G, Dolan L (1998) A model system to study the effects of elevated CO2 on the developmental physiology of roots: the use of Arabidopsis thaliana. J Exp Bot 49: 593-597.
21. De Vleesschauwer D, Höfte M (2009) Rhizobacteria-induced systemic resistance. In LC Van Loon, ed, Plant Innate Immunity, Vol 51. Academic Press/Elsevier Science, London, pp 223-281.
22. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
23. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86: 423-433.
24. Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120: 2465-2474.
25. Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105: 8790-8794.
26. Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legué V (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol 151: 1991-2005.
27. Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751-759.
28. Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RW, Schiefelbein JW (1994) The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166: 740-754.
29. Geels FP, Schippers B (1983) Selection of antagonistic fluorescent Pseudomonas spp. and their root colonization and persistence following treatment of seed potatoes. Phytopathol Z 108: 193-206.
30. Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61: 793-796.
31. Grebe M (2012) The patterning of epidermal hairs in Arabidopsis: updated. Curr Opin Plant Biol 15: 31-37.
32. Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513-523.
33. Hassan H, Scheres B, Blilou I (2010) JACKDAW controls epidermal patterning in the Arabidopsis root meristem through a non-cell-autonomous mechanism. Development 137: 1523-1529.
34. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101: 555-567.
35. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59: 365-386.
36. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55: 335-347.
37. Knoester M, Pieterse CMJ, Bol JF, Van Loon LC (1999) Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Mol Plant Microbe Interact 12: 720-727.
38. Lamers JG, Schippers B, Geels FP (1988) Soil-borne diseases of wheat in the Netherlands and results of seed bacterization with pseudomonads against Gaeumannomyces graminis var. tritici, associated with disease resistance. In ML Jorna, LAJ Slootmaker, eds, Cereal Breeding Related to Integrated Cereal Production. Pudoc, Wageningen, The Netherlands, pp 134-139.
39. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Marée AFM, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6: e307.
40. Lee MM, Schiefelbein J (2002) Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14: 611-618.
41. Leeman M, Van Pelt JA, Den Ouden FM, Heinsbroek M, Bakker PAHM, Schippers B (1995) Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85: 1021-1027.
42. Leyser HMO, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161-164.
43. López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter rootsystem architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20: 207-217.
44. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280-287.
45. Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) JASMONATEINSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950.
46. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541-556.
47. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90.
48. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44.
49. Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18: 2066-2073.
50. Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-associated and ethyleneassociated process. Plant Physiol 106: 1335-1346.
51. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332: 1097-1100.
52. Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55: 175-187.
53. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ ASL genes in Arabidopsis. Plant Cell 19: 118-130.
54. Ortega-Martínez O, Pernas M, Carol RJ, Dolan L (2007) Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 317: 507-510.
55. Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río RE, Campos-García J, López-Bucio J (2011) Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci USA 108: 7253-7258.
56. Pickett FB, Wilson AK, Estelle M (1990) The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol 94: 1462-1466.
57. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521.
58. Pieterse CMJ, van Wees SCM, Hoffland E, van Pelt JA, van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8: 1225-1237.
59. Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571-1580.
60. Pozo MJ, Van Der Ent S, Van Loon LC, Pieterse CMJ (2008) Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol 180: 511-523.
61. Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130: 1908-1917.
62. Ruzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19: 2197-2212.
63. Ryu C-M, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100: 4927-4932.
64. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, et al (1999) An auxindependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463-472.
65. Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17: 354-358.
66. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814.
67. Schiefelbein J (2003) Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 6: 74-78.
68. Schwachtje J, Karojet S, Thormählen I, Bernholz C, Kunz S, Brouwer S, Schwochow M, Köhl K, van Dongen JT (2011) A naturally associated rhizobacterium of Arabidopsis thaliana induces a starvation-like transcriptional response while promoting growth. PLoS ONE 6: e29382.
69. Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25: 28-36.
70. Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19: 2169-2185.
71. Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, et al (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21: 1495-1511.
72. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15: 2648-2653.
73. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19: 2186-2196.
74. Timpte C, Wilson AK, Estelle M (1994) The axr2-1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an early step in auxin response. Genetics 138: 1239-1249.
75. Ueda M, Koshino-Kimura Y, Okada K (2005) Stepwise understanding of root development. Curr Opin Plant Biol 8: 71-76.
76. Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70: 1581-1588.
77. Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, Pel MJC, Joosten RG, Proveniers MCG, Van Loon LC, Ton J, et al (2008) MYB72 is required in early signaling steps of rhizobacteriainduced systemic resistance in Arabidopsis. Plant Physiol 146: 1293-1304.
78. Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van't Westende YAM, Hartog F, Van Loon LC (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact 10: 716-724.
79. Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11: 443-448.
80. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277: 1113-1116.
81. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14: 1-4.
82. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25: 139-150