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Title: A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization

Abstract

The complex interactions between plants and their microbiome can have a profound effect on the health and productivity of the plant host. A better understanding of the microbial mechanisms that promote plant health and stress tolerance will enable strategies for improving the productivity of economically-important plants. Pantoea sp. YR343 is a motile, rod-shaped bacterium isolated from the roots of Populus deltoides that possesses the ability to solubilize phosphate and produce the phytohormone indole-3-acetic acid. Pantoea sp. YR343 readily colonizes plant roots and does not appear to be pathogenic when applied to the leaves or roots of selected plant hosts. To better understand the molecular mechanisms involved in plant association and rhizosphere survival by Pantoea sp. YR343, we constructed a mutant in which the crtB gene encoding phytoene synthase was deleted. Phytoene synthase is responsible for converting geranylgeranyl pyrophosphate to phytoene, an important precursor to the production of carotenoids. As predicted, the ΔcrtB mutant is defective in carotenoid production, and shows increased sensitivity to oxidative stress. Moreover, we find that the ΔcrtB mutant is impaired in biofilm formation and production of indole-3-acetic acid. Finally we demonstrate that the ΔcrtB mutant shows reduced colonization of plant roots. Taken together, these data suggestmore » that carotenoids are important for plant association and/or rhizosphere survival in Pantoea sp. YR343.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [2];  [2];  [3];  [1];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  2. Univ. of Notre Dame, IN (United States). Department of Chemical and Biomolecular Engineering
  3. Univ. of Pretoria, Pretoria (South Africa)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1248782
Grant/Contract Number:  
AC05-00OR22725; SC0006642
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Pantoea; carotenoids; crtB; indole-3-acetic acid; poplar; rhizosphere; zeaxanthin

Citation Formats

Bible, Amber, Fletcher, Sarah J, Pelletier, Dale A, Schadt, Christopher Warren, Jawdy, Sara, Weston, David, Engle, Nancy L., Tschaplinski, Timothy J., Masyuko, Rachel, Polisetti, Sneha, Bohn, Paul W., Coutinho, Teresa, Doktycz, Mitchel John, and Morrell-Falvey, Jennifer L. A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00491.
Bible, Amber, Fletcher, Sarah J, Pelletier, Dale A, Schadt, Christopher Warren, Jawdy, Sara, Weston, David, Engle, Nancy L., Tschaplinski, Timothy J., Masyuko, Rachel, Polisetti, Sneha, Bohn, Paul W., Coutinho, Teresa, Doktycz, Mitchel John, & Morrell-Falvey, Jennifer L. A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization. United States. doi:10.3389/fmicb.2016.00491.
Bible, Amber, Fletcher, Sarah J, Pelletier, Dale A, Schadt, Christopher Warren, Jawdy, Sara, Weston, David, Engle, Nancy L., Tschaplinski, Timothy J., Masyuko, Rachel, Polisetti, Sneha, Bohn, Paul W., Coutinho, Teresa, Doktycz, Mitchel John, and Morrell-Falvey, Jennifer L. Mon . "A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization". United States. doi:10.3389/fmicb.2016.00491. https://www.osti.gov/servlets/purl/1248782.
@article{osti_1248782,
title = {A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization},
author = {Bible, Amber and Fletcher, Sarah J and Pelletier, Dale A and Schadt, Christopher Warren and Jawdy, Sara and Weston, David and Engle, Nancy L. and Tschaplinski, Timothy J. and Masyuko, Rachel and Polisetti, Sneha and Bohn, Paul W. and Coutinho, Teresa and Doktycz, Mitchel John and Morrell-Falvey, Jennifer L.},
abstractNote = {The complex interactions between plants and their microbiome can have a profound effect on the health and productivity of the plant host. A better understanding of the microbial mechanisms that promote plant health and stress tolerance will enable strategies for improving the productivity of economically-important plants. Pantoea sp. YR343 is a motile, rod-shaped bacterium isolated from the roots of Populus deltoides that possesses the ability to solubilize phosphate and produce the phytohormone indole-3-acetic acid. Pantoea sp. YR343 readily colonizes plant roots and does not appear to be pathogenic when applied to the leaves or roots of selected plant hosts. To better understand the molecular mechanisms involved in plant association and rhizosphere survival by Pantoea sp. YR343, we constructed a mutant in which the crtB gene encoding phytoene synthase was deleted. Phytoene synthase is responsible for converting geranylgeranyl pyrophosphate to phytoene, an important precursor to the production of carotenoids. As predicted, the ΔcrtB mutant is defective in carotenoid production, and shows increased sensitivity to oxidative stress. Moreover, we find that the ΔcrtB mutant is impaired in biofilm formation and production of indole-3-acetic acid. Finally we demonstrate that the ΔcrtB mutant shows reduced colonization of plant roots. Taken together, these data suggest that carotenoids are important for plant association and/or rhizosphere survival in Pantoea sp. YR343.},
doi = {10.3389/fmicb.2016.00491},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {4}
}

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Works referenced in this record:

REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
journal, June 2004


A New Leaf Blotch Disease of Sudangrass Caused by Pantoea ananas and Pantoea stewartii
journal, September 2000


Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence
journal, July 2011

  • Barret, Matthieu; Morrissey, John P.; O’Gara, Fergal
  • Biology and Fertility of Soils, Vol. 47, Issue 7
  • DOI: 10.1007/s00374-011-0605-x

Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents
journal, January 2012

  • Beneduzi, Anelise; Ambrosini, Adriana; Passaglia, Luciana M. P.
  • Genetics and Molecular Biology, Vol. 35, Issue 4 suppl 1
  • DOI: 10.1590/S1415-47572012000600020

Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA)
journal, December 2008

  • Brady, Carrie; Cleenwerck, Ilse; Venter, Stephanus
  • Systematic and Applied Microbiology, Vol. 31, Issue 6-8
  • DOI: 10.1016/j.syapm.2008.09.004

Biological Control of Pseudomonas syringae pv. syringae , the Causal Agent of Basal Kernel Blight of Barley, by Antagonistic Pantoea agglomerans
journal, April 2000


How carotenoids protect bacterial photosynthesis
journal, October 2000

  • Cogdell, Richard J.; Howard, Tina D.; Bittl, Robert
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402
  • DOI: 10.1098/rstb.2000.0696

Bacterial Blight and Dieback of Eucalyptus Species, Hybrids, and Clones in South Africa
journal, January 2002


Genome Sequence of Pantoea ananatis LMG20103, the Causative Agent of Eucalyptus Blight and Dieback
journal, March 2010

  • De Maayer, P.; Chan, W. Y.; Venter, S. N.
  • Journal of Bacteriology, Vol. 192, Issue 11
  • DOI: 10.1128/Jb.00060–10

Carotenes and carotenoids in natural biological samples: a Raman spectroscopic analysis
journal, October 2009

  • de Oliveira, Vanessa E.; Castro, Harlem V.; Edwards, Howell G. M.
  • Journal of Raman Spectroscopy, Vol. 41, Issue 6
  • DOI: 10.1002/jrs.2493

Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper
journal, January 2012

  • del Amor, Francisco M.; Cuadra-Crespo, Paula
  • Functional Plant Biology, Vol. 39, Issue 1
  • DOI: 10.1071/FP11173

Carotenoids’ influence on radiotolerance of Pantoea agglomerans , a plant pathogen
journal, September 2008


The carotenoids as anti-oxidants — a review
journal, December 1997

  • Edge, R.; McGarvey, D. J.; Truscott, T. G.
  • Journal of Photochemistry and Photobiology B: Biology, Vol. 41, Issue 3
  • DOI: 10.1016/S1011-1344(97)00092-4

Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates
journal, May 2006


Chemistry of singlet oxygen. VII. Quenching by .beta.-carotene
journal, October 1968

  • Foote, Christopher S.; Denny, Robert W.
  • Journal of the American Chemical Society, Vol. 90, Issue 22
  • DOI: 10.1021/ja01024a061

Reactive oxygen species as signals that modulate plant stress responses and programmed cell death
journal, January 2006

  • Gechev, Tsanko S.; Van Breusegem, Frank; Stone, Julie M.
  • BioEssays, Vol. 28, Issue 11
  • DOI: 10.1002/bies.20493

Raman spectroscopic study of the heterogeneity of microcolonies of a pigmented bacterium
journal, January 2006

  • Goodwin, James R.; Hafner, Louise M.; Fredericks, Peter M.
  • Journal of Raman Spectroscopy, Vol. 37, Issue 9
  • DOI: 10.1002/jrs.1523

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

Carotenoids as modulators of lipid membrane physical properties
journal, May 2005

  • Gruszecki, Wiesław I.; Strzałka, Kazimierz
  • Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1740, Issue 2
  • DOI: 10.1016/j.bbadis.2004.11.015

New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Pantoea stewartii subsp. stewartii Exhibits Surface Motility, Which is a Critical Aspect of Stewart's Wilt Disease Development on Maize
journal, October 2008

  • Herrera, Carmen M.; Koutsoudis, Maria D.; Wang, Xiaolei
  • Molecular Plant-Microbe Interactions, Vol. 21, Issue 10
  • DOI: 10.1094/MPMI-21-10-1359

Singlet oxygen quenching ability of naturally occurring carotenoids
journal, February 1994

  • Hirayama, Osamu; Nakamura, Kyoko; Hamada, Syoko
  • Lipids, Vol. 29, Issue 2
  • DOI: 10.1007/BF02537155

Regulation of membrane lipid fluidity in Acholeplasma laidlawii: Effect of carotenoid pigment content
journal, June 1974


CAROTENOIDS OF Erwinia herbicola AND AN Escherichia coli HB101 STRAIN CARRYING THE Erwinia herbicola CAROTENOID GENE CLUSTER
journal, July 1991


Organic Acids, Sugars, and l -Tryptophane in Exudates of Vegetables Growing on Stonewool and Their Effects on Activities of Rhizosphere Bacteria
journal, March 2006

  • Kamilova, Faina; Kravchenko, Lev V.; Shaposhnikov, Alexander I.
  • Molecular Plant-Microbe Interactions, Vol. 19, Issue 3
  • DOI: 10.1094/MPMI-19-0250

Hopanoid Biosynthesis and Function in Bacteria
journal, April 1999


Antioxidant functions of carotenoids
journal, January 1989


Actions of Carotenoids in Biological Systems
journal, July 1993


Indole-3-acetic acid biosynthetic pathway and aromatic amino acid aminotransferase activities in Pantoea dispersa strain GPK
journal, March 2013

  • Kulkarni, G. B.; Nayak, A. S.; Sajjan, S. S.
  • Letters in Applied Microbiology, Vol. 56, Issue 5
  • DOI: 10.1111/lam.12053

The Oxidative Burst in Plant Disease Resistance
journal, June 1997


Microbial Carotenoids
journal, October 1972


Functional microdomains in bacterial membranes
journal, August 2010


Resonance Raman spectroscopy of carotenoids and carotenoid-containing systems
journal, January 1985


A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
journal, July 1962


Reactive Oxygen Species during Plant-microorganism Early Interactions
journal, February 2010


Bacterial biosynthesis of indole-3-acetic acid
journal, March 1996

  • Patten, Cheryl L.; Glick, Bernard R.
  • Canadian Journal of Microbiology, Vol. 42, Issue 3
  • DOI: 10.1139/m96-032

A General System for Studying Protein−Protein Interactions in Gram-Negative Bacteria
journal, August 2008

  • Pelletier, Dale A.; Hurst, Gregory B.; Foote, Linda J.
  • Journal of Proteome Research, Vol. 7, Issue 8
  • DOI: 10.1021/pr8001832

The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms
journal, February 2008

  • Raaijmakers, Jos M.; Paulitz, Timothy C.; Steinberg, Christian
  • Plant and Soil, Vol. 321, Issue 1-2
  • DOI: 10.1007/s11104-008-9568-6

Resonance Raman studies of bacterial reaction centers
journal, June 1990


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


Molecular biology of cellulose production in bacteria
journal, May 2002


New functional assignment of the carotenogenic genes crtB and crtE with constructs of these genes from Erwinia species
journal, January 1992


Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis
journal, November 2000


Potential of NIR-FT-Raman spectroscopy in natural carotenoid analysis
journal, January 2005

  • Schulz, H.; Baranska, M.; Baranski, R.
  • Biopolymers, Vol. 77, Issue 4
  • DOI: 10.1002/bip.20215

Diversity of Carotenoid Synthesis Gene Clusters from Environmental Enterobacteriaceae Strains
journal, December 2005


Production of indole-3-acetic acid, aromatic amino acid aminotransferase activities and plant growth promotion by Pantoea agglomerans rhizosphere isolates
journal, July 2007

  • Sergeeva, Elena; Hirkala, Danielle L. M.; Nelson, Louise M.
  • Plant and Soil, Vol. 297, Issue 1-2
  • DOI: 10.1007/s11104-007-9314-5

A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013


Rhizosphere Bacterial Signalling: A Love Parade Beneath Our Feet
journal, January 2004

  • Somers, E.; Vanderleyden, J.; Srinivasan, M.
  • Critical Reviews in Microbiology, Vol. 30, Issue 4
  • DOI: 10.1080/10408410490468786

Indole-3-acetic acid in microbial and microorganism-plant signaling
journal, July 2007


Analysis of the gene cluster encoding carotenoid biosynthesis in Erwinia herbicola Eho13
journal, February 1994


Reactive Oxygen Species Signaling in Response to Pathogens: Figure 1.
journal, June 2006

  • Torres, Miguel Angel; Jones, Jonathan D. G.; Dangl, Jeffery L.
  • Plant Physiology, Vol. 141, Issue 2
  • DOI: 10.1104/pp.106.079467

MBDS Solvent: An Improved Method for Assessment of Biofilms
journal, January 2013

  • Tram, Greg; Korolik, Victoria; Day, Christopher J.
  • Advances in Microbiology, Vol. 03, Issue 02
  • DOI: 10.4236/aim.2013.32030

Natural Infestation of Onion Seed by Pantoea ananatis , Causal Agent of Center Rot
journal, February 2002


Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae
journal, June 2015

  • Walterson, Alyssa M.; Stavrinides, John
  • FEMS Microbiology Reviews, Vol. 39, Issue 6
  • DOI: 10.1093/femsre/fuv027

Microarray Analysis of the Gene Expression Profile Induced by the Endophytic Plant Growth-Promoting Rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis
journal, May 2005

  • Wang, Yanqing; Ohara, Yumiko; Nakayashiki, Hitoshi
  • Molecular Plant-Microbe Interactions, Vol. 18, Issue 5
  • DOI: 10.1094/MPMI-18–0385

Pseudomonas fluorescens Induces Strain-Dependent and Strain-Independent Host Plant Responses in Defense Networks, Primary Metabolism, Photosynthesis, and Fitness
journal, June 2012

  • Weston, David J.; Pelletier, Dale A.; Morrell-Falvey, Jennifer L.
  • Molecular Plant-Microbe Interactions, Vol. 25, Issue 6
  • DOI: 10.1094/MPMI-09-11-0253

Oxidative burst: an early plant response to pathogen infection
journal, March 1997

  • Wojtaszek, Przemysław
  • Biochemical Journal, Vol. 322, Issue 3
  • DOI: 10.1042/bj3220681

Genetic organization of the cellulose synthase operon in Acetobacter xylinum.
journal, October 1990

  • Wong, H. C.; Fear, A. L.; Calhoon, R. D.
  • Proceedings of the National Academy of Sciences, Vol. 87, Issue 20
  • DOI: 10.1073/pnas.87.20.8130

    Works referencing / citing this record:

    Characterization of two Pantoea strains isolated from extra-virgin olive oil
    journal, July 2018


    Characterization of two Pantoea strains isolated from extra-virgin olive oil
    journal, July 2018