Pseudomonas putida and Pseudomonas fluorescens Influence Arabidopsis Root System Architecture Through an Auxin Response Mediated by Bioactive Cyclodipeptides

Aguilar JA, Zavala AN, Díaz-Pérez C, Cervántes C, Díaz-Pérez AL, Campos-García J (2006) The atu and liu clusters are involved in the catabolic pathways for acyclic monoterpenes and leucine in Pseudomonas aeruginosa. Appl Environ Microbiol 72:2070–2079 Badri DV, Weir TL, Van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotech 20:642–650 Barazani O, Friedman J (1999) Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J Chem Ecol 25:2397–2406 Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett M, Sandberg G, Bellini C (2000) The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97:14819–14824 Benková E, Michniewicz MSM, Teichmann T, Seifertova D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602 Blakely L, Evans T (1979) Cell dynamics studies on the pericycle of radish seedling roots. Plant Sci Lett 14:79–83 Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr-, Hg- and Pb-contaminated soil by bioaugmentation with siderophoreproducing bacteria. Chemosphere 74:280–286 Brazelton JN, Pfeufer EE, Sweat TA, Gardener BB, Coenen C (2008) 2,4-Diacetylphloroglucinol alters plant root development. Mol Plant-Microbe Interact 21:1349–1358 Campbell J, Lin Q, Geske GD, Blackwell HE (2009) New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem Biol 4:1051–1059 Carrillo-Castaneda G, Munoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL (2003) Plant growth-promoting bacteria promote copper and iron translocation from root to shoot in alfalfa seedlings. J Plant Nutr 26:1801–1814 Colón-Carmona A, You R, Haimovitch-Gal T, Doermer P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508 Contesto C, Milesi S, Mantelin S, Zancarini A, Desbrosses G, Varoquaux F, Bellini C, Kowalczyk M, Touraine B (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455–1470 Dey R, Pal KK, Bhat DM (2004) Grwoth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394 Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann J, Jürgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119 Dobblelaere SA, Croonenborghs A, Thys A, Vanden Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164 Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168 Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of maize. Int J Biol Life Sci 1:35–40 Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012) Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Phil Trans R Soc B 367:1461–1468 González O, Ortiz-Castro R, Díaz-Pérez C, Díaz-Pérez AL, Magaña-Dueñas V, López-Bucio J, Campos-García J (2017) Non-ribosomal peptide synthases from Pseudomonas aeruginosa play a role in cyclodipeptide biosynthesis, quorum-sensing regulation, and root development in a plant host. Microb Ecol 73:616–629 Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:1270–1273 Gupta A, Rai V, Bagdwal N, Goel R (2005) In situ characterization of mercury resistant growth promoting fluorescent pseudomonads. Microbiol Res 160:385–388 Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: b-glucuronidase as a sensitive and versatile fusion marker in higher plants. EMBO J 6:3901–3907 Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451 Kloepper JW, Zablotowivz RM, Tipping EM, Lifshitz R (1990) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic, Dordrecht, pp 315–326 López-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287 López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velasquez-Becerra C, Farías-Rodríguez R, Macías-Rodriguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant-Microbe Interact 20:207–217 Malamy JF, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44 Martínez-Morales LJ, Soto-Urzúa L, Baca BE, Sánchez-Ahédo JA (2003) Indole-3 butyric acid (IBA) production in culture medium by wild strain Azospirillum brasilense. FEMS Microbiol Lett 228:167–173 Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root hair initiation through an auxin and ethylene associated process. Plant Physiol 106:1335–1346 Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–614 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 Oono Y, Chen QG, Overvoorde PJ, Kôhler C, Theologis A (1998) age Mutants of Arabidopsis exhibit altered auxin-regulated gene expression. Plant Cell 10:1649–1662 Ortiz-Castro R, Martínez-Trujillo M, López-Bucio J (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509 Ortiz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbiol signals in plant growth and development. Plant Signal Behav 4:1–12 Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujilo M, del Río R, 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 Ortiz-Castro R, Campos-García J, López-Bucio J (2013) Rapid identification of plant-growth-promoting rhizobacteria using an agar plate cocultivation system with Arabidopsis. In: de Bruijn FJ (ed) Molecular microbiol ecology of the rhizosphere. Wiley, New Jersey, pp 345–353 Plotnikova JM, Rahme LG, Ausubel FM (2000) Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol 124:1766–1774 Preston GM (2004) Plant perceptions of plant growth promoting Pseudomonas. Phil Trans R Soc Lond B 359:907–918 Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficia soil bacteria. Plant Physiol 148:1547–1556 Sieberer T, Hauser MT, Seifert GJ, Lusching C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842 Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448 Tripathi M, Munot HP, Schouch Y, Meyer JM, Goel R (2005) Isolation and functional characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas putida KNP9. Curr Microbiol 5:233–237 Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) AUX/IAA proteins repress expression of report genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971 Venturi V (2006) Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30:274–291 Von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85 Walker TS, Bais HP, Déziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol 134:320–331 Wang R, Estelle M (2014) Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway. Curr Opin Plant Biol 21:51–58 Yan PS, Song Y, Sakuno E, Nakajima H, Nakagawa H, Yabe K (2004) Cyclo(L-leucyl-L-prolyl) produced by Achromobacter xylosoxidans inhibits aflatoxin production by Aspergillus parasiticus. Appl Environ Microbiol 70:7466–7473 Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ (2013) Unraveling root development programs initiated by beneficial Pseudomonas spp. Bacteria Plant Physiol 162:304–318 Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534