The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis
Article first published online: 4 JUL 2013
© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust
Special Issue: Featured papers on ‘Drought-induced forest mortality’
Volume 200, Issue 2, pages 558–569, October 2013
How to Cite
Bresson, J., Varoquaux, F., Bontpart, T., Touraine, B. and Vile, D. (2013), The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytologist, 200: 558–569. doi: 10.1111/nph.12383
- Issue published online: 18 SEP 2013
- Article first published online: 4 JUL 2013
- Manuscript Accepted: 24 MAY 2013
- Manuscript Received: 25 APR 2013
- the French Ministry of Higher Education and Research
- 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91–94. , , , , , , , , .
- 2010. RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant and Cell Physiology 51: 1975–1987. , , , , , , , .
- 2000. The monoclonal antibody MAC252 does not react with the (−) enantiomer of abscisic acid. Journal of Experimental Botany 51: 305–307. , .
- 2009. Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytologist 181: 413–423. , , , , , .
- 2005. A physiological overview of the genetics of flowering time control. Plant Biotechnology Journal 3: 3–16. , .
- 2001. Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biology and Fertility of Soils 33: 152–156. , , , .
- 2005. Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research 56: 1159–1168. .
- 1985. Water transport. Annual Review of Plant Physiology and Plant Molecular Biology 36: 473–516. .
- 2004. Grain yields with limited water. Journal of Experimental Botany 55: 2385–2394. , .
- 2001. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell 13: 1499–1510. , , , , , , .
- 2004. Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168: 2169–2185. , , , , , , , .
- 2009. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botanique 87: 455–462. , , , .
- 2008. Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Science 175: 178–189. , , , , , , , , .
- 2010. The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232: 1455–1470. , , , , , , , , .
- 2007. Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. Annals of Botany 99: 703–711. , , .
- 2004. Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Canadian Journal of Botany – Revue Canadienne de Botanique 82: 273–281. , , .
- 2009. PGPR–Arabidopsis interactions is a useful system to study signaling pathways involved in plant developmental control. Plant Signaling & Behavior 4: 321–323. , , , , .
- 2009. Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant, Cell & Environment 32: 1682–1694. , , .
- 2010. Rhizobacterial mediation of plant hormone status. Annals of Applied Biology 157: 361–379. , , , .
- 2008. Key impact of Vgt1 on flowering time adaptation in maize: evidence from association mapping and ecogeographical information. Genetics 178: 2433–2437. , , , , , , , , .
- 2009. Plant drought stress: effects, mechanisms and management. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C, eds. Sustainable agriculture. Dordrecht, the Netherlands: Springer, 153–188. , , , , .
- 2008. Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Applied Soil Ecology 40: 182–188. , , , .
- 2011. Microbially mediated plant functional traits. Annual Review of Ecology, Evolution, and Systematics 42: 23–46. , , , , , .
- 2012. The ethylene pathway contributes to root hair elongation induced by the beneficial bacteria Phyllobacterium brassicacearum STM196. Plant Science 190: 74–81. , , , , .
- 2004. A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. The Plant Cell 16: 3304–3325. , , , , , , , , , .
- 1998. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. Journal of Theoretical Biology 190: 63–68. , , .
- 2006. PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist 169: 623–635. , , , , , , , , , et al.
- 2010. Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiology 154: 1254–1271. , , , .
- 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology 60: 579–598. , , , , .
- 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347: 1–32. , .
- 2011. The control of developmental phase transitions in plants. Development 138: 4117–4129. , .
- 2010. Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiology 154: 357–372. , , , , , , , , , et al.
- 2007. Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids and Surfaces B: Biointerfaces 60: 7–11. , , , , , , .
- 2005. Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: delta C-13, stomatal conductance and transpiration efficiency. Plant, Cell & Environment 28: 697–708. , , , , , , , , .
- 2009. Flowering time control and applications in plant breeding. Trends in Plant Science 14: 563–573. , .
- 2013. The NRT2.5 and NRT2.6 genes are involved in growth promotion of Arabidopsis by the plant growth-promoting rhizobacterium (PGPR) strain Phyllobacterium brassicacearum STM196. New Phytologist 198: 514–524. , , , , , .
- 1989. Free-living bacterial inocula for enhancing crop productivity. Trends in Biotechnology 7: 39–44. , , .
- 2008. Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Functional Plant Biology 35: 141–151. , , , .
- 1998. Genetic control of flowering time in Arabidopsis. Annual Review of Plant Physiology and Plant Molecular Biology 49: 345–370. , , , .
- 2007. Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. American Naturalist 169: E141–E157. , , , , , , .
- 2003. Early modifications of Brassica napus root system architecture induced by a plant growth-promoting Phyllobacterium strain. New Phytologist 160: 119–125. , , , , .
- 2004. Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86: 1–25. , , .
- 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63: 541–556. , .
- 2006. 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 56: 827–839. , , , , , , , .
- 2009. Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. Journal of Plant Growth Regulation 28: 115–124. , , .
- 2003. Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology 12: 1137–1151. , , .
- 2009. Simulating crop phenological responses to water deficits. In: Ahuja LR, Reddy VR, Anapalli SA, Yu Q, eds. Modeling the response of crops to limited water: recent advances in understanding and modeling water stress effects on plant growth processes. Madison, WI, USA: ASA-SSA-CSSA, 277–300. , , , , , , .
- 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969–980. , , , , .
- 2009. Life history in a model system: opening the black box with Arabidopsis thaliana. Ecology Letters 12: 593–600. , .
- 2011. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany 62: 1715–1729. , , , , , , .
- 2003. Tales from the underground: molecular plant–rhizobacteria interactions. Plant, Cell & Environment 26: 189–199. , , .
- 1992. The effect of water-stress on photosynthetic carbon metabolism in four species grown under field conditions. Plant, Cell & Environment 15: 25–35. , , , , , , , , , .
- R Development Core Team. 2009. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
- 2000. Auxin regulates the initiation and radial position of plant lateral organs. The Plant Cell 12: 507–518. , , .
- 2008. Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth promoting rhizobacterium. Tree Physiology 28: 1693–1701. , , , .
- 2011. Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. Journal of Plant Physiology 168: 1031–1037. , , , , , , .
- 2003. Bacterial volatiles promote growth in Arabidopsis. Proceedings of the National Academy of Sciences, USA 100: 4927–4932. , , , , , , .
- 2005. Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant and Soil 268: 285–292. , , , .
- 2005. Delay in flowering and increase in biomass of transgenic tobacco expressing the Arabidopsis floral repressor gene FLOWERING LOCUS C. Journal of Plant Physiology 162: 711–717. , , , , .
- 2011. A naturally associated rhizobacterium of Arabidopsis thaliana induces a starvation-like transcriptional response while promoting growth. PLoS ONE 6: e29382. , , , , , , , , .
- 2010. More from less: plant growth under limited water. Current Opinion in Biotechnology 21: 197–203. , .
- 2001. Alteration in flowering time causes accelerated or decelerated progression through Arabidopsis vegetative phases. Canadian Journal of Botany 79: 657–665. , , .
- 2012. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. Journal of Experimental Botany 63: 25–31. .
- 2011. Water deficit and growth. Co-ordinating processes without an orchestrator? Current Opinion in Plant Biology 14: 283–289. , , .
- 2010. Keep on growing under drought: genetic and developmental bases of the response of rosette area using a recombinant inbred line population. Plant, Cell & Environment 33: 1875–1887. , , , , , , .
- 2011. Drought, metabolites, and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments. Current Opinion in Plant Biology 14: 240–245. , .
- 2012. Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant, Cell & Environment 35: 702–718. , , , , , , , .
- 2012. Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE 7: e52565. , , , , , , , .
- 2005. Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Molecular Plant–Microbe Interactions 18: 385–396. , , , , .
- 1985. Osmotic adjustment and the inhibition of leaf, root, stem and silk growth at low water potentials in maize. Planta 164: 540–549. , .
- 2011. The effect of the floral repressor FLC on the timing and progression of vegetative phase change in Arabidopsis. Development 138: 677–685. , .
- 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends in Plant Science 14: 1–4. , , .
- 1997. Regulation of levels of proline as an osmolyte in plants under water stress. Plant and Cell Physiology 38: 1095–1102. , , , , .
- 2008. Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. Journal of Microbiology and Biotechnology 18: 958–963. , , , , .
- 2008. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant Journal 56: 264–273. , , , , , .