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Title: Robust biological nitrogen fixation in a model grass–bacterial association

Abstract

Summary Nitrogen‐fixing rhizobacteria can promote plant growth; however, it is controversial whether biological nitrogen fixation ( BNF ) from associative interaction contributes to growth promotion. The roots of Setaria viridis , a model C 4 grass, were effectively colonized by bacterial inoculants resulting in a significant enhancement of growth. Nitrogen‐13 tracer studies provided direct evidence for tracer uptake by the host plant and incorporation into protein. Indeed, plants showed robust growth under nitrogen‐limiting conditions when inoculated with an ammonium‐excreting strain of Azospirillum brasilense . 11 C‐labeling experiments showed that patterns in central carbon metabolism and resource allocation exhibited by nitrogen‐starved plants were largely reversed by bacterial inoculation, such that they resembled plants grown under nitrogen‐sufficient conditions. Adoption of S. viridis as a model should promote research into the mechanisms of associative nitrogen fixation with the ultimate goal of greater adoption of BNF for sustainable crop production.

Authors:
 [1];  [2];  [1];  [3];  [4];  [4];  [2];  [1];  [1];  [1];  [5];  [4]
  1. Department of Biochemistry and Molecular Biology Federal University of Paraná 81531‐980 Curitiba Brazil
  2. Department of Food Science and Technology Federal University of Santa Catarina 88034‐001 Florianópolis Brazil
  3. Department of Environmental Biology State University of New York College of Environmental Science and Forestry Syracuse NY 13210 USA
  4. Biological Environmental and Climate Sciences Department Brookhaven National Laboratory Building 901 Upton NY 11973 USA
  5. Divisions of Plant Science and Biochemistry C. S. Bond Life Science Center University of Missouri Columbia MO 65211 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1401375
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 81 Journal Issue: 6; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Pankievicz, Vânia C. S., do Amaral, Fernanda P., Santos, Karina F. D. N., Agtuca, Beverly, Xu, Youwen, Schueller, Michael J., Arisi, Ana Carolina M., Steffens, Maria. B. R., de Souza, Emanuel M., Pedrosa, Fábio O., Stacey, Gary, and Ferrieri, Richard A. Robust biological nitrogen fixation in a model grass–bacterial association. United Kingdom: N. p., 2015. Web. doi:10.1111/tpj.12777.
Pankievicz, Vânia C. S., do Amaral, Fernanda P., Santos, Karina F. D. N., Agtuca, Beverly, Xu, Youwen, Schueller, Michael J., Arisi, Ana Carolina M., Steffens, Maria. B. R., de Souza, Emanuel M., Pedrosa, Fábio O., Stacey, Gary, & Ferrieri, Richard A. Robust biological nitrogen fixation in a model grass–bacterial association. United Kingdom. https://doi.org/10.1111/tpj.12777
Pankievicz, Vânia C. S., do Amaral, Fernanda P., Santos, Karina F. D. N., Agtuca, Beverly, Xu, Youwen, Schueller, Michael J., Arisi, Ana Carolina M., Steffens, Maria. B. R., de Souza, Emanuel M., Pedrosa, Fábio O., Stacey, Gary, and Ferrieri, Richard A. Tue . "Robust biological nitrogen fixation in a model grass–bacterial association". United Kingdom. https://doi.org/10.1111/tpj.12777.
@article{osti_1401375,
title = {Robust biological nitrogen fixation in a model grass–bacterial association},
author = {Pankievicz, Vânia C. S. and do Amaral, Fernanda P. and Santos, Karina F. D. N. and Agtuca, Beverly and Xu, Youwen and Schueller, Michael J. and Arisi, Ana Carolina M. and Steffens, Maria. B. R. and de Souza, Emanuel M. and Pedrosa, Fábio O. and Stacey, Gary and Ferrieri, Richard A.},
abstractNote = {Summary Nitrogen‐fixing rhizobacteria can promote plant growth; however, it is controversial whether biological nitrogen fixation ( BNF ) from associative interaction contributes to growth promotion. The roots of Setaria viridis , a model C 4 grass, were effectively colonized by bacterial inoculants resulting in a significant enhancement of growth. Nitrogen‐13 tracer studies provided direct evidence for tracer uptake by the host plant and incorporation into protein. Indeed, plants showed robust growth under nitrogen‐limiting conditions when inoculated with an ammonium‐excreting strain of Azospirillum brasilense . 11 C‐labeling experiments showed that patterns in central carbon metabolism and resource allocation exhibited by nitrogen‐starved plants were largely reversed by bacterial inoculation, such that they resembled plants grown under nitrogen‐sufficient conditions. Adoption of S. viridis as a model should promote research into the mechanisms of associative nitrogen fixation with the ultimate goal of greater adoption of BNF for sustainable crop production.},
doi = {10.1111/tpj.12777},
journal = {The Plant Journal},
number = 6,
volume = 81,
place = {United Kingdom},
year = {Tue Mar 10 00:00:00 EDT 2015},
month = {Tue Mar 10 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/tpj.12777

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Works referenced in this record:

The Transcriptome of Rhizobacteria-Induced Systemic Resistance in Arabidopsis
journal, August 2004

  • Verhagen, Bas W. M.; Glazebrook, Jane; Zhu, Tong
  • Molecular Plant-Microbe Interactions, Vol. 17, Issue 8
  • DOI: 10.1094/MPMI.2004.17.8.895

Early colonization pattern of maize (Zea mays L. Poales, Poaceae) roots by Herbaspirillum seropedicae (Burkholderiales, Oxalobacteraceae)
journal, January 2008


Soybean nodule gas permeability, nitrogen fixation and dirunal cycles in soil temperature
journal, July 1988


Partitioning of New Carbon as 11C in Nicotiana tabacum Reveals Insight into Methyl Jasmonate Induced Changes in Metabolism
journal, September 2010


Effect of nitrogen compounds on nitrogenase activity in Herbaspirillum seropedicae SMR1
journal, September 1997

  • Klassen, G.; Pedrosa, F. O.; Souza, E. M.
  • Canadian Journal of Microbiology, Vol. 43, Issue 9
  • DOI: 10.1139/m97-129

Comparison of Benefit to Sugarcane Plant Growth and 15 N 2 Incorporation Following Inoculation of Sterile Plants with Acetobacter diazotrophicus Wild-Type and Nif¯ Mutant Strains
journal, March 2001

  • Sevilla, Myrna; Burris, Robert H.; Gunapala, Nirmala
  • Molecular Plant-Microbe Interactions, Vol. 14, Issue 3
  • DOI: 10.1094/MPMI.2001.14.3.358

Responses of agronomically important crops to inoculation with Azospirillum
journal, January 2001

  • Dobbelaere, Sofie; Croonenborghs, Anja; Thys, Amber
  • Functional Plant Biology, Vol. 28, Issue 9
  • DOI: 10.1071/PP01074

Setaria viridis : A Model for C 4 Photosynthesis
journal, August 2010

  • Brutnell, Thomas P.; Wang, Lin; Swartwood, Kerry
  • The Plant Cell, Vol. 22, Issue 8
  • DOI: 10.1105/tpc.110.075309

Carbon Dioxide Enrichment Inhibits Nitrate Assimilation in Wheat and Arabidopsis
journal, May 2010


Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses.
journal, April 1994


Contribution of biological nitrogen fixation to Elephant grass (Pennisetum purpureum Schum.)
journal, September 2011

  • de Morais, Rafael F.; Quesada, Diego M.; Reis, Veronica M.
  • Plant and Soil, Vol. 356, Issue 1-2
  • DOI: 10.1007/s11104-011-0944-2

Evidence for the endophytic colonization of Phaseolus vulgaris(common bean) roots by the diazotroph Herbaspirillum seropedicae
journal, March 2011


Herbaspirillum, an endophytic diazotroph colonizing vascular tissue 3Sorghum bicolor L. Moench
journal, March 1997

  • James, E. K.; Olivares, F. L.; Baldani, J. I.
  • Journal of Experimental Botany, Vol. 48, Issue 3
  • DOI: 10.1093/jxb/48.3.785

Biological nitrogen fixation associated with sugar cane and rice: Contributions and prospects for improvement
journal, July 1995

  • Boddey, R. M.; de Oliveira, O. C.; Urquiaga, S.
  • Plant and Soil, Vol. 174, Issue 1-2
  • DOI: 10.1007/BF00032247

Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes
journal, September 2006

  • Cannon, S. B.; Sterck, L.; Rombauts, S.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 40
  • DOI: 10.1073/pnas.0603228103

DEGseq: an R package for identifying differentially expressed genes from RNA-seq data
journal, October 2009


Optimizing [13N]N2 radiochemistry for nitrogen-fixation in root nodules of legumes
journal, June 2010

  • Kasel, Mirjam C. K.; Schueller, Michael J.; Ferrieri, Richard A.
  • Journal of Labelled Compounds and Radiopharmaceuticals, Vol. 53, Issue 9
  • DOI: 10.1002/jlcr.1786

Comparison of automated pre-column and post-column analysis of amino acid oligomers
journal, January 1987


Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a Root-Associated Nitrogen-Fixing Bacterium
journal, January 1986

  • Baldani, J. I.; Baldani, V. L. D.; Seldin, L.
  • International Journal of Systematic Bacteriology, Vol. 36, Issue 1
  • DOI: 10.1099/00207713-36-1-86

Nitrogen Fixation in Wheat Provided by Klebsiella pneumoniae 342
journal, October 2004

  • Iniguez, A. Leonardo; Dong, Yuemei; Triplett, Eric W.
  • Molecular Plant-Microbe Interactions, Vol. 17, Issue 10
  • DOI: 10.1094/MPMI.2004.17.10.1078

N 2 Fixation by Azospirillum brasilense and Its Incorporation into Host Setaria italica
journal, September 1983


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

Biological nitrogen fixation in non-legume plants
journal, March 2013

  • Santi, Carole; Bogusz, Didier; Franche, Claudine
  • Annals of Botany, Vol. 111, Issue 5
  • DOI: 10.1093/aob/mct048

16S Ribosomal DNA Characterization of Nitrogen-Fixing Bacteria Isolated from Banana (Musa spp.) and Pineapple (Ananas comosus (L.) Merril)
journal, May 2001


Nitrogen fixation in endophytic and associative symbiosis
journal, March 2000


Infection and Colonization of Sugar Cane and Other Graminaceous Plants by Endophytic Diazotrophs
journal, January 1998


Does GABA increase the efficiency of symbiotic N 2 fixation in legumes?
journal, January 2011


Endophytic Herbaspirillum seropedicae expresses nif genes in gramineous plants
journal, July 2003

  • Roncato-Maccari, Lauren D. B.; Ramos, Humberto J. O.; Pedrosa, Fabio O.
  • FEMS Microbiology Ecology, Vol. 45, Issue 1
  • DOI: 10.1016/S0168-6496(03)00108-9

A nonradioactive assay method for determination of enzymatic activity of d-ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)
journal, August 2002

  • Chakrabarti, Subhra; Bhattacharya, Sumana; Bhattacharya, Sanjoy K.
  • Journal of Biochemical and Biophysical Methods, Vol. 52, Issue 3
  • DOI: 10.1016/S0165-022X(02)00072-6

Products of Dark CO 2 Fixation in Pea Root Nodules Support Bacteroid Metabolism
journal, May 1990

  • Rosendahl, Lis; Vance, Carroll P.; Pedersen, Walther B.
  • Plant Physiology, Vol. 93, Issue 1
  • DOI: 10.1104/pp.93.1.12

Life in grasses: diazotrophic endophytes
journal, April 1998


Radio-Metabolite Analysis of Carbon-11 Biochemical Partitioning to Non-Structural Carbohydrates for Integrated Metabolism and Transport Studies
journal, April 2013

  • Babst, Benjamin A.; Karve, Abhijit A.; Judt, Tatjana
  • Plant and Cell Physiology, Vol. 54, Issue 6
  • DOI: 10.1093/pcp/pct045

Endophytic Bacteria and Their Potential Applications
journal, November 2002

  • Lodewyckx, Cindy; Vangronsveld, Jaco; Porteous, Fiona
  • Critical Reviews in Plant Sciences, Vol. 21, Issue 6
  • DOI: 10.1080/0735-260291044377

Regulation of nitrogen fixation (nif) genes of Azospirillum brasilense by nifA and ntr (gln) type gene products
journal, June 1984


Endophytic Expression of nif Genes of Azoarcus sp. Strain BH72 in Rice Roots
journal, September 1999

  • Egener, Tanja; Hurek, Thomas; Reinhold-Hurek, Barbara
  • Molecular Plant-Microbe Interactions, Vol. 12, Issue 9
  • DOI: 10.1094/MPMI.1999.12.9.813

Potential roles for the glnB and ntrYX genes in Azospirillum brasilense
journal, July 2001


Azospirillum -plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003)
journal, August 2004

  • Bashan, Yoav; Holguin, Gina; de-Bashan, Luz E.
  • Canadian Journal of Microbiology, Vol. 50, Issue 8
  • DOI: 10.1139/w04-035

How close are we to nitrogen-fixing cereals?
journal, October 2010


Close Association of Azospirillum and Diazotrophic Rods with Different Root Zones of Kallar Grass
journal, January 1986

  • Reinhold, Barbara; Hurek, Thomas; Niemann, Ernst-Georg
  • Applied and Environmental Microbiology, Vol. 52, Issue 3
  • DOI: 10.1128/aem.52.3.520-526.1986

Infection of mottled stripe disease-susceptible and resistant sugar cane varieties by the endophytic diazotroph Herbaspirillum
journal, April 1997


Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties
journal, April 2002


Azoarcus Grass Endophytes Contribute Fixed Nitrogen to the Plant in an Unculturable State
journal, March 2002

  • Hurek, Thomas; Handley, Linda L.; Reinhold-Hurek, Barbara
  • Molecular Plant-Microbe Interactions, Vol. 15, Issue 3
  • DOI: 10.1094/MPMI.2002.15.3.233

Infection and Colonization of Rice Seedlings by the Plant Growth-Promoting Bacterium Herbaspirillum seropedicae Z67
journal, September 2002

  • James, Euan K.; Gyaneshwar, Prasad; Mathan, Natarajan
  • Molecular Plant-Microbe Interactions, Vol. 15, Issue 9
  • DOI: 10.1094/MPMI.2002.15.9.894

Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus
journal, January 1994

  • James, E. K.; Reis, V. M.; Olivares, F. L.
  • Journal of Experimental Botany, Vol. 45, Issue 6
  • DOI: 10.1093/jxb/45.6.757

Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes
journal, June 2008


Use of carbon-11 in Populus shows that exogenous jasmonic acid increases biosynthesis of isoprene from recently fixed carbon
journal, May 2005


Excretion of ammonium by Azospirillum brasilense mutants resistant to ethylenediamine
journal, July 1991

  • Machado, H. B.; Funayama, S.; Rigo, L. U.
  • Canadian Journal of Microbiology, Vol. 37, Issue 7
  • DOI: 10.1139/m91-092

Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses
journal, March 2011

  • Li, P.; Brutnell, T. P.
  • Journal of Experimental Botany, Vol. 62, Issue 9
  • DOI: 10.1093/jxb/err096

Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions
journal, September 2011

  • Walker, Vincent; Couillerot, Olivier; Von Felten, Andreas
  • Plant and Soil, Vol. 356, Issue 1-2
  • DOI: 10.1007/s11104-011-0960-2

Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms
journal, February 2009

  • Richardson, Alan E.; Barea, José-Miguel; McNeill, Ann M.
  • Plant and Soil, Vol. 321, Issue 1-2
  • DOI: 10.1007/s11104-009-9895-2