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Title: Pseudomonas fluorescens transportome is linked to strain-specific plant growth promotion in Aspen seedlings under nutrient stress

Abstract

Diverse communities of bacteria colonize plant roots and the rhizosphere. Many of these rhizobacteria are symbionts and provide plant growth promotion (PGP) services, protecting the plant from biotic and abiotic stresses and increasing plant productivity by providing access to nutrients that would otherwise be unavailable to roots. In return, these symbiotic bacteria receive photosynthetically-derived carbon (C), in the form of sugars and organic acids, from plant root exudates. PGP activities have been characterized for a variety of forest tree species and are important in C cycling and sequestration in terrestrial ecosystems. The molecular mechanisms of these PGP activities, however, are less well-known. In a previous analysis of Pseudomonas genomes, we found that the bacterial transportome, the aggregate activity of a bacteria's transmembrane transporters, was most predictive for the ecological niche of Pseudomonads in the rhizosphere. Here, we used Populus tremuloides Michx. (trembling aspen) seedlings inoculated with one of three Pseudomonas fluorescens strains (Pf0-1, SBW25, and WH6) and one Pseudomonas protegens (Pf-5) as a laboratory model to further investigate the relationships between the predicted transportomic capacity of a bacterial strain and its observed PGP effects in laboratory cultures. Conditions of low nitrogen (N) or low phosphorus (P) availability and the correspondingmore » replete media conditions were investigated. We measured phenotypic and biochemical parameters of P. tremuloides seedlings and correlated P fluorescens strain-specific transportomic capacities with P. tremuloides seedling phenotype to predict the strain and nutrient environment-specific transporter functions that lead to experimentally observed, strain, and media-specific PGP activities and the capacity to protect plants against nutrient stress. These predicted transportomic functions fall in three groups: (i) transport of compounds that modulate aspen seedling root architecture, (ii) transport of compounds that help to mobilize nutrients for aspen roots, and (iii) transporters that enable bacterial acquisition of C sources from seedling root exudates. Lastly, these predictions point to specific molecular mechanisms of PGP activities that can be directly tested through future, hypothesis-driven biological experiments.« less

Authors:
 [1];  [2];  [1];  [1];  [3]
  1. Argonne National Lab. (ANL), Lemont, IL (United States)
  2. West Virginia Univ., Morgantown, WV (United States)
  3. Argonne National Lab. (ANL), Lemont, IL (United States); Univ. of Illinois at Chicago, Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1366508
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; plant growth promotion; Aspen; Pseudomonas; computational modeling; nitrogen; phosphorus; transportomics

Citation Formats

Shinde, Shalaka, Cumming, Jonathan R., Collart, Frank R., Noirot, Philippe H., and Larsen, Peter E. Pseudomonas fluorescens transportome is linked to strain-specific plant growth promotion in Aspen seedlings under nutrient stress. United States: N. p., 2017. Web. doi:10.3389/fpls.2017.00348.
Shinde, Shalaka, Cumming, Jonathan R., Collart, Frank R., Noirot, Philippe H., & Larsen, Peter E. Pseudomonas fluorescens transportome is linked to strain-specific plant growth promotion in Aspen seedlings under nutrient stress. United States. https://doi.org/10.3389/fpls.2017.00348
Shinde, Shalaka, Cumming, Jonathan R., Collart, Frank R., Noirot, Philippe H., and Larsen, Peter E. Tue . "Pseudomonas fluorescens transportome is linked to strain-specific plant growth promotion in Aspen seedlings under nutrient stress". United States. https://doi.org/10.3389/fpls.2017.00348. https://www.osti.gov/servlets/purl/1366508.
@article{osti_1366508,
title = {Pseudomonas fluorescens transportome is linked to strain-specific plant growth promotion in Aspen seedlings under nutrient stress},
author = {Shinde, Shalaka and Cumming, Jonathan R. and Collart, Frank R. and Noirot, Philippe H. and Larsen, Peter E.},
abstractNote = {Diverse communities of bacteria colonize plant roots and the rhizosphere. Many of these rhizobacteria are symbionts and provide plant growth promotion (PGP) services, protecting the plant from biotic and abiotic stresses and increasing plant productivity by providing access to nutrients that would otherwise be unavailable to roots. In return, these symbiotic bacteria receive photosynthetically-derived carbon (C), in the form of sugars and organic acids, from plant root exudates. PGP activities have been characterized for a variety of forest tree species and are important in C cycling and sequestration in terrestrial ecosystems. The molecular mechanisms of these PGP activities, however, are less well-known. In a previous analysis of Pseudomonas genomes, we found that the bacterial transportome, the aggregate activity of a bacteria's transmembrane transporters, was most predictive for the ecological niche of Pseudomonads in the rhizosphere. Here, we used Populus tremuloides Michx. (trembling aspen) seedlings inoculated with one of three Pseudomonas fluorescens strains (Pf0-1, SBW25, and WH6) and one Pseudomonas protegens (Pf-5) as a laboratory model to further investigate the relationships between the predicted transportomic capacity of a bacterial strain and its observed PGP effects in laboratory cultures. Conditions of low nitrogen (N) or low phosphorus (P) availability and the corresponding replete media conditions were investigated. We measured phenotypic and biochemical parameters of P. tremuloides seedlings and correlated P fluorescens strain-specific transportomic capacities with P. tremuloides seedling phenotype to predict the strain and nutrient environment-specific transporter functions that lead to experimentally observed, strain, and media-specific PGP activities and the capacity to protect plants against nutrient stress. These predicted transportomic functions fall in three groups: (i) transport of compounds that modulate aspen seedling root architecture, (ii) transport of compounds that help to mobilize nutrients for aspen roots, and (iii) transporters that enable bacterial acquisition of C sources from seedling root exudates. Lastly, these predictions point to specific molecular mechanisms of PGP activities that can be directly tested through future, hypothesis-driven biological experiments.},
doi = {10.3389/fpls.2017.00348},
journal = {Frontiers in Plant Science},
number = ,
volume = 8,
place = {United States},
year = {Tue Mar 21 00:00:00 EDT 2017},
month = {Tue Mar 21 00:00:00 EDT 2017}
}

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Works referenced in this record:

Lysopine and Octopine Promote Crown-Gall Tumor Growth in vivo
journal, October 1970


Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types
journal, July 2011

  • Gottel, Neil R.; Castro, Hector F.; Kerley, Marilyn
  • Applied and Environmental Microbiology, Vol. 77, Issue 17
  • DOI: 10.1128/AEM.05255-11

Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5
journal, June 2005

  • Paulsen, Ian T.; Press, Caroline M.; Ravel, Jacques
  • Nature Biotechnology, Vol. 23, Issue 7
  • DOI: 10.1038/nbt1110

Phosphate solubilizing bacteria and their role in plant growth promotion
journal, October 1999


Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti.
journal, January 1995

  • Cook, D.; Dreyer, D.; Bonnet, D.
  • The Plant Cell, Vol. 7, Issue 1
  • DOI: 10.1105/tpc.7.1.43

The impact of supplemental carbon sources on Arabidopsis thaliana growth, chlorophyll content and anthocyanin accumulation
journal, October 2009


Biological costs and benefits to plant–microbe interactions in the rhizosphere
journal, May 2005

  • Morgan, J. A. W.; Bending, G. D.; White, P. J.
  • Journal of Experimental Botany, Vol. 56, Issue 417
  • DOI: 10.1093/jxb/eri205

Involvement of polyamines in root development
journal, January 2004

  • Couée, Ivan; Hummel, Irène; Sulmon, Cécile
  • Plant Cell, Tissue and Organ Culture, Vol. 76, Issue 1, p. 1-10
  • DOI: 10.1023/A:1025895731017

Erratum: Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency
journal, July 2013

  • Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri
  • Journal of Plant Nutrition and Soil Science, Vol. 176, Issue 4
  • DOI: 10.1002/jpln.201390025

Involvement of the Lipopolysaccharides of Azospirilla in the Interaction with Wheat Seedling Roots
journal, January 2001

  • Fedonenko, Yu. P.; Egorenkova, I. V.; Konnova, S. A.
  • Microbiology, Vol. 70, Issue 3, p. 329-334
  • DOI: 10.1023/A:1010411629428

Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species
journal, February 2009


The stimulatory effects of L-tryptophan and plant growth promoting rhizobacteria (PGPR) on soil health and physiology of wheat
journal, January 2015


Plant assimilation of phosphorus from an insoluble organic form is improved by addition of an organic anion producing Pseudomonas sp.
journal, January 2014


An improved, high-quality draft genome sequence of the Germination-Arrest Factor-producing Pseudomonas fluorescens WH6
journal, January 2010


Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists
journal, November 2011

  • Frey-Klett, P.; Burlinson, P.; Deveau, A.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4
  • DOI: 10.1128/MMBR.00020-11

Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective
journal, June 2009


The impact of mannose and other carbon sources on the elongation and diameter of the primary root of Arabidopsis thaliana
journal, January 2001

  • Baskin, Tobias I.; Remillong, Elizabeth L.; Wilson, Jan E.
  • Functional Plant Biology, Vol. 28, Issue 6, p. 481
  • DOI: 10.1071/PP01047

Root Exudation and Rhizosphere Biology: Fig. 1.
journal, May 2003

  • Walker, Travis S.; Bais, Harsh Pal; Grotewold, Erich
  • Plant Physiology, Vol. 132, Issue 1
  • DOI: 10.1104/pp.102.019661

A unifying framework for dinitrogen fixation in the terrestrial biosphere
journal, June 2008

  • Houlton, Benjamin Z.; Wang, Ying-Ping; Vitousek, Peter M.
  • Nature, Vol. 454, Issue 7202
  • DOI: 10.1038/nature07028

Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25: Type III secretion in P. fluorescens
journal, September 2001


Discovery of new regulatory genes of lipopeptide biosynthesis in Pseudomonas fluorescens
journal, March 2014

  • Song, Chunxu; Aundy, Kumar; van de Mortel, Judith
  • FEMS Microbiology Letters, Vol. 356, Issue 2
  • DOI: 10.1111/1574-6968.12404

Effect of Plant Growth-promoting Rhizobacteria (PGPRs) on plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) under simulated seawater irrigation
journal, January 2012

  • Shen, Min; Jun Kang, Yi; Li Wang, Huan
  • The Journal of General and Applied Microbiology, Vol. 58, Issue 4
  • DOI: 10.2323/jgam.58.253

The regulation and plasticity of root hair patterning and morphogenesis
journal, May 2016

  • Salazar-Henao, Jorge E.; Vélez-Bermúdez, Isabel Cristina; Schmidt, Wolfgang
  • Development, Vol. 143, Issue 11
  • DOI: 10.1242/dev.132845

Twenty-One Genome Sequences from Pseudomonas Species and 19 Genome Sequences from Diverse Bacteria Isolated from the Rhizosphere and Endosphere of Populus deltoides
journal, October 2012

  • Brown, S. D.; Utturkar, S. M.; Klingeman, D. M.
  • Journal of Bacteriology, Vol. 194, Issue 21
  • DOI: 10.1128/JB.01243-12

Legacy of a half century of Athabasca oil sands development recorded by lake ecosystems
journal, January 2013

  • Kurek, J.; Kirk, J. L.; Muir, D. C. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 5
  • DOI: 10.1073/pnas.1217675110

Climate change effects on beneficial plant-microorganism interactions: Climate change and beneficial plant-microorganism interactions
journal, May 2010


Soil drying and nitrogen availability modulate carbon and water exchange over a range of annual precipitation totals and grassland vegetation types
journal, December 2009


The Incorporation of d-Glucosamine- 14 C into Root Tissues of Higher Plants
journal, March 1970


Role of Exopolysaccharides in Pseudomonas aeruginosa Biofilm Formation and Architecture
journal, June 2011

  • Ghafoor, Aamir; Hay, Iain D.; Rehm, Bernd H. A.
  • Applied and Environmental Microbiology, Vol. 77, Issue 15
  • DOI: 10.1128/AEM.00637-11

Genetic Interactions between Phytochrome A, Phytochrome B, and Cryptochrome 1 during Arabidopsis Development
journal, September 1998


Germination-Arrest Factor (GAF): Biological properties of a novel, naturally-occurring herbicide produced by selected isolates of rhizosphere bacteria
journal, September 2008


Role of root derived organic acids in the mobilization of nutrients from the rhizosphere
journal, October 1994

  • Jones, David L.; Darrah, Peter R.
  • Plant and Soil, Vol. 166, Issue 2
  • DOI: 10.1007/BF00008338

Detection of Root Mucilage Using an Anti-fucose Antibody
journal, March 2002


Predicting Ecological Roles in the Rhizosphere Using Metabolome and Transportome Modeling
journal, September 2015


Microbial co-operation in the rhizosphere
journal, May 2005

  • Barea, José-Miguel; Pozo, María José; Azcón, Rosario
  • Journal of Experimental Botany, Vol. 56, Issue 417
  • DOI: 10.1093/jxb/eri197

L-Glutamate as a Novel Modifier of Root Growth and Branching: What’s the Sensor?
journal, July 2007

  • Walch-Liu, Pia; Forde, Brian G.
  • Plant Signaling & Behavior, Vol. 2, Issue 4
  • DOI: 10.4161/psb.2.4.4016

Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r
journal, February 1997


Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors
journal, January 2011

  • Garbeva, Paolina; Silby, Mark W.; Raaijmakers, Jos M.
  • The ISME Journal, Vol. 5, Issue 6
  • DOI: 10.1038/ismej.2010.196

Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens
journal, January 2009

  • Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.
  • Genome Biology, Vol. 10, Issue 5
  • DOI: 10.1186/gb-2009-10-5-r51

Determination of low concentrations of organic phosphorus in soil solution
journal, July 1999

  • Martin, M.; Celi, L.; Barberis, E.
  • Communications in Soil Science and Plant Analysis, Vol. 30, Issue 13-14
  • DOI: 10.1080/00103629909370341

The effects of plant growth regulators and l-phenylalanine on phenolic compounds of sweet basil
journal, January 2015


Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion
journal, March 2015


Physiological and genetic characterization of rice nitrogen fixer PGPR isolated from rhizosphere soils of different crops
journal, February 2014

  • Habibi, Safiullah; Djedidi, Salem; Prongjunthuek, Kunlayakorn
  • Plant and Soil, Vol. 379, Issue 1-2
  • DOI: 10.1007/s11104-014-2035-7

Inoculation with Pseudomonas putida PCI2, a phosphate solubilizing rhizobacterium, stimulates the growth of tomato plants
journal, March 2014


Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays)
journal, October 2012


Metagenomic Sequencing of an In Vitro-Simulated Microbial Community
journal, April 2010


Rhamnose synthase activity is required for pathogenicity of the vascular wilt fungus Verticillium dahliae: Rhamnose is a Fungal Pathogenicity Factor
journal, June 2016

  • Santhanam, Parthasarathy; Boshoven, Jordi C.; Salas, Omar
  • Molecular Plant Pathology, Vol. 18, Issue 3
  • DOI: 10.1111/mpp.12401

Proline enhances growth, productivity and anatomy of two varieties of Lupinus termis L. grown under salt stress
journal, January 2016


Derivative Spectrophotometric Determination of Nitrate in Plant Tissue
journal, November 2003


Erratum: Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency
journal, July 2013

  • Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri
  • Journal of Plant Nutrition and Soil Science, Vol. 176, Issue 4
  • DOI: 10.1002/jpln.201390025

Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species
journal, February 2009


The impact of supplemental carbon sources on Arabidopsis thaliana growth, chlorophyll content and anthocyanin accumulation
journal, October 2009


Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective
journal, June 2009


Physiological and genetic characterization of rice nitrogen fixer PGPR isolated from rhizosphere soils of different crops
journal, February 2014

  • Habibi, Safiullah; Djedidi, Salem; Prongjunthuek, Kunlayakorn
  • Plant and Soil, Vol. 379, Issue 1-2
  • DOI: 10.1007/s11104-014-2035-7

Inoculation with Pseudomonas putida PCI2, a phosphate solubilizing rhizobacterium, stimulates the growth of tomato plants
journal, March 2014


Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays)
journal, October 2012


Germination-Arrest Factor (GAF): Biological properties of a novel, naturally-occurring herbicide produced by selected isolates of rhizosphere bacteria
journal, September 2008


The effects of plant growth regulators and l-phenylalanine on phenolic compounds of sweet basil
journal, January 2015


Proline enhances growth, productivity and anatomy of two varieties of Lupinus termis L. grown under salt stress
journal, January 2016


Plant assimilation of phosphorus from an insoluble organic form is improved by addition of an organic anion producing Pseudomonas sp.
journal, January 2014


Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns
journal, August 2002


Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors
journal, January 2011

  • Garbeva, Paolina; Silby, Mark W.; Raaijmakers, Jos M.
  • The ISME Journal, Vol. 5, Issue 6
  • DOI: 10.1038/ismej.2010.196

A unifying framework for dinitrogen fixation in the terrestrial biosphere
journal, June 2008

  • Houlton, Benjamin Z.; Wang, Ying-Ping; Vitousek, Peter M.
  • Nature, Vol. 454, Issue 7202
  • DOI: 10.1038/nature07028

Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5
journal, June 2005

  • Paulsen, Ian T.; Press, Caroline M.; Ravel, Jacques
  • Nature Biotechnology, Vol. 23, Issue 7
  • DOI: 10.1038/nbt1110

Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r
journal, February 1997


Legacy of a half century of Athabasca oil sands development recorded by lake ecosystems
journal, January 2013

  • Kurek, J.; Kirk, J. L.; Muir, D. C. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 5
  • DOI: 10.1073/pnas.1217675110

Determination of low concentrations of organic phosphorus in soil solution
journal, July 1999

  • Martin, M.; Celi, L.; Barberis, E.
  • Communications in Soil Science and Plant Analysis, Vol. 30, Issue 13-14
  • DOI: 10.1080/00103629909370341

Detection of Root Mucilage Using an Anti-fucose Antibody
journal, March 2002


Microbial co-operation in the rhizosphere
journal, May 2005

  • Barea, José-Miguel; Pozo, María José; Azcón, Rosario
  • Journal of Experimental Botany, Vol. 56, Issue 417
  • DOI: 10.1093/jxb/eri197

Biological costs and benefits to plant–microbe interactions in the rhizosphere
journal, May 2005

  • Morgan, J. A. W.; Bending, G. D.; White, P. J.
  • Journal of Experimental Botany, Vol. 56, Issue 417
  • DOI: 10.1093/jxb/eri205

Root Exudation and Rhizosphere Biology: Fig. 1.
journal, May 2003

  • Walker, Travis S.; Bais, Harsh Pal; Grotewold, Erich
  • Plant Physiology, Vol. 132, Issue 1
  • DOI: 10.1104/pp.102.019661

Genetic Interactions between Phytochrome A, Phytochrome B, and Cryptochrome 1 during Arabidopsis Development
journal, September 1998


The Incorporation of d-Glucosamine- 14 C into Root Tissues of Higher Plants
journal, March 1970


Discovery of new regulatory genes of lipopeptide biosynthesis in Pseudomonas fluorescens
journal, March 2014

  • Song, Chunxu; Aundy, Kumar; van de Mortel, Judith
  • FEMS Microbiology Letters, Vol. 356, Issue 2
  • DOI: 10.1111/1574-6968.12404

Soil drying and nitrogen availability modulate carbon and water exchange over a range of annual precipitation totals and grassland vegetation types
journal, December 2009


Rhamnose synthase activity is required for pathogenicity of the vascular wilt fungus Verticillium dahliae: Rhamnose is a Fungal Pathogenicity Factor
journal, June 2016

  • Santhanam, Parthasarathy; Boshoven, Jordi C.; Salas, Omar
  • Molecular Plant Pathology, Vol. 18, Issue 3
  • DOI: 10.1111/mpp.12401

Lysopine and Octopine Promote Crown-Gall Tumor Growth in vivo
journal, October 1970


PslD Is a Secreted Protein Required for Biofilm Formation by Pseudomonas aeruginosa
journal, April 2006


An improved, high-quality draft genome sequence of the Germination-Arrest Factor-producing Pseudomonas fluorescens WH6
journal, January 2010


Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens
journal, January 2009

  • Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.
  • Genome Biology, Vol. 10, Issue 5
  • DOI: 10.1186/gb-2009-10-5-r51

The regulation and plasticity of root hair patterning and morphogenesis
journal, May 2016

  • Salazar-Henao, Jorge E.; Vélez-Bermúdez, Isabel Cristina; Schmidt, Wolfgang
  • Development, Vol. 143, Issue 11
  • DOI: 10.1242/dev.132845

Nicotinamide as a plant growth regulator isolated from rice hulls.
journal, January 1975

  • Takeuchi, Setsuo; Kono, Yoshiki; Kawarada, Akira
  • Agricultural and Biological Chemistry, Vol. 39, Issue 4
  • DOI: 10.1271/bbb1961.39.859

Metagenomic Sequencing of an In Vitro-Simulated Microbial Community
journal, April 2010


Predicting Ecological Roles in the Rhizosphere Using Metabolome and Transportome Modeling
journal, September 2015


Genetic diversity of siderophore-producing bacteria of tobacco rhizosphere
journal, January 2009


Transient Induction of a Peroxidase Gene in Medicago truncatula Precedes Infection by Rhizobium meliloti
journal, January 1995

  • Cook, Douglas; Dreyer, Dale; Bonnet, Dominique
  • The Plant Cell, Vol. 7, Issue 1
  • DOI: 10.2307/3869836

Effect of Plant Growth-promoting Rhizobacteria (PGPRs) on plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) under simulated seawater irrigation
journal, January 2012

  • Shen, Min; Jun Kang, Yi; Li Wang, Huan
  • The Journal of General and Applied Microbiology, Vol. 58, Issue 4
  • DOI: 10.2323/jgam.58.253

Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion
journal, March 2015


The stimulatory effects of L-tryptophan and plant growth promoting rhizobacteria (PGPR) on soil health and physiology of wheat
journal, January 2015


L-Glutamate as a Novel Modifier of Root Growth and Branching: What’s the Sensor?
journal, July 2007

  • Walch-Liu, Pia; Forde, Brian G.
  • Plant Signaling & Behavior, Vol. 2, Issue 4
  • DOI: 10.4161/psb.2.4.4016

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