Switchgrass Rhizosphere Metabolite Chemistry Driven by Nitrogen Availability

Smercina, Darian N.; Bowsher, Alan W.; Evans, Sarah E.; Friesen, Maren L.; Eder, Elizabeth K.; Hoyt, David W.; Tiemann, Lisa K.

doi:10.1094/PBIOMES-09-19-0055-FI

Switchgrass Rhizosphere Metabolite Chemistry Driven by Nitrogen Availability

Journal Article · Thu Apr 16 00:00:00 EDT 2020 · Phytobiomes Journal

DOI:https://doi.org/10.1094/PBIOMES-09-19-0055-FI· OSTI ID:1637665

^[1]; ^[2]; Evans, Sarah E. ^[3]; Friesen, Maren L. ^[4]; Eder, Elizabeth K. ^[5]; Hoyt, David W. ^[5]; Tiemann, Lisa K. ^[2]

Michigan State Univ., East Lansing, MI (United States); Michigan State University Department of Plant, Soil and Microbial Sciences
Michigan State Univ., East Lansing, MI (United States)
Michigan State Univ., Hickory Corner, MI (United States)
Washington State Univ., Pullman, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Plants and soil microorganisms interact closely in the rhizosphere where plants may exchange carbon (C) for functional benefits from the microbial community. For example, the bioenergy crop, switchgrass (Panicum virgatum) is thought to exchange root-exuded C for nitrogen (N) fixed by diazotrophs (free-living N-fixers). However, this interaction is not well characterized and it is not known how or if switchgrass responds to diazotrophs or their activity. To explore this question, we assessed rhizosphere metabolite chemistry of switchgrass grown in a hydroponic system under two N levels and under inoculated or uninoculated conditions. Plants were grown with the inoculum Azotobacter vinelandii DJ for 3 days before harvest. We found switchgrass root exudate chemistry to be driven by N availability. Total metabolite concentrations were generally greater under high N versus low N and unaffected by inoculation. Examination of rhizosphere chemical fingerprints indicates metabolite chemistry was also driven strongly by N availability with a greater relative abundance of carbohydrates under high N and greater relative abundance of organic acids under low N. We also found evidence of changes in rhizosphere chemical fingerprints by inoculation treatment. However, we found little evidence of N treatment and inoculation interaction effects that suggests this response is not directly mediated by N availability.

View Accepted Manuscript (DOE)

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0014108; SC0018409; FC02-07ER64494; AC02-05CH11231; AC05-76RL01830

OSTI ID:: 1637665

Alternate ID(s):: OSTI ID: 1806283

Journal Information:: Phytobiomes Journal, Journal Name: Phytobiomes Journal Journal Issue: 1 Vol. 5; ISSN 2471-2906

Publisher:: American Phytopathological Society (APS)Copyright Statement

Country of Publication:: United States

Language:: English

References (35)

Data from: Switchgrass rhizosphere metabolite chemistry driven by nitrogen availability Smercina, Darian; Bowsher, Alan W.; Evans, Sarah E. Dryad https://doi.org/10.5061/dryad.9zw3r229b	dataset	January 2020
Carbon flow in the rhizosphere: carbon trading at the soil–root interface Jones, D. L.; Nguyen, C.; Finlay, R. D. Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-009-9925-0	journal	February 2009
The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists Baldani, José Ivo; Reis, Veronica Massena; Videira, Sandy Sampaio Plant and Soil, Vol. 384, Issue 1-2 https://doi.org/10.1007/s11104-014-2186-6	journal	July 2014
Optimization of the 15N2 incorporation and acetylene reduction methods for free-living nitrogen fixation Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L. Plant and Soil, Vol. 445, Issue 1-2 https://doi.org/10.1007/s11104-019-04307-3	journal	October 2019
Amino acids and vitamins produced by azotobacter vinelandii atcc 12837 in chemically-defined media and dialysed soil media Gonzalez-Lopez, J.; Salmeron, V.; Moreno, J. Soil Biology and Biochemistry, Vol. 15, Issue 6 https://doi.org/10.1016/0038-0717(83)90037-8	journal	January 1983
Mapping the site(s) of MgATP and MgADP interaction with the nitrogenase of Azotobacter vinelandii. Lysine 15 of the iron protein plays a major role in MgATP interaction. Seefeldt, L. C.; Morgan, T. V.; Dean, D. R. Journal of Biological Chemistry, Vol. 267, Issue 10 https://doi.org/10.1016/S0021-9258(19)50480-X	journal	April 1992
Regulation of lysine catabolism in higher plants Arruda, Paulo; Kemper, Edson L.; Papes, Fabio Trends in Plant Science, Vol. 5, Issue 8 https://doi.org/10.1016/S1360-1385(00)01688-5	journal	August 2000
Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.) Roley, Sarah S.; Xue, Chao; Hamilton, Stephen K. Soil Biology and Biochemistry, Vol. 129 https://doi.org/10.1016/j.soilbio.2018.11.006	journal	February 2019
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Trends in Plant Science, Vol. 23, Issue 1 https://doi.org/10.1016/j.tplants.2017.09.003	journal	January 2018
Regulation of lysine catabolism in higher plants Arruda, Paulo; Kemper, Edson L.; Papes, Fabio Trends in Plant Science, Vol. 5, Issue 8 https://doi.org/10.1016/s1360-1385(00)01688-5	journal	August 2000
Targeted Profiling: Quantitative Analysis of ¹ H NMR Metabolomics Data Weljie, Aalim M.; Newton, Jack; Mercier, Pascal Analytical Chemistry, Vol. 78, Issue 13 https://doi.org/10.1021/ac060209g	journal	July 2006
The role of root exudates and allelochemicals in the rhizosphere Bertin, Cecile; Yang, Xiaohan; Weston, Leslie A. Plant and Soil, Vol. 256, Issue 1 https://doi.org/10.1023/A:1026290508166	journal	September 2003
The role of root exudates and allelochemicals in the rhizosphere Bertin, Cecile; Yang, Xiaohan; Weston, Leslie A. Plant and Soil, Vol. 256, Issue 1 https://doi.org/10.1023/a:1026290508166	journal	September 2003
Root exudate metabolomes change under drought and show limited capacity for recovery Gargallo-Garriga, Albert; Preece, Catherine; Sardans, Jordi Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30150-0	journal	August 2018
The role of glycine betaine in the protection of plants from stress: clues from transgenic plants: Role of betaine in stress tolerance Sakamoto, A.; Murata, N. Plant, Cell & Environment, Vol. 25, Issue 2 https://doi.org/10.1046/j.0016-8025.2001.00790.x	journal	February 2002
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales Borton, Mikayla A.; Hoyt, David W.; Roux, Simon Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1800155115	journal	June 2018
Nucleic acids in the culture fluids of Rhodopseudomonas capsulatus and other heterotrophic bacteria Katayama, Tadashi; Kobayashi, Michiharu; Okuda, Azuma Soil Science and Plant Nutrition, Vol. 13, Issue 4 https://doi.org/10.1080/00380768.1967.10431982	journal	July 1967
The Biology and Agronomy of Switchgrass for Biofuels Parrish, David J.; Fike, John H. Critical Reviews in Plant Sciences, Vol. 24, Issue 5-6 https://doi.org/10.1080/07352680500316433	journal	September 2005
Nitrogen fertilization challenges the climate benefit of cellulosic biofuels Ruan, Leilei; Bhardwaj, Ajay K.; Hamilton, Stephen K. Environmental Research Letters, Vol. 11, Issue 6 https://doi.org/10.1088/1748-9326/11/6/064007	journal	June 2016
The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism: Purine catabolism in ABA-mediated stress tolerance Watanabe, Shunsuke; Matsumoto, Mayumi; Hakomori, Yuki Plant, Cell & Environment, Vol. 37, Issue 4 https://doi.org/10.1111/pce.12218	journal	November 2013
Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes Robertson, G. Philip; Hamilton, Stephen K.; Barham, Bradford L. Science, Vol. 356, Issue 6345 https://doi.org/10.1126/science.aal2324	journal	June 2017
Diversity of Nitrogen-Fixing Bacteria Associated with Switchgrass in the Native Tallgrass Prairie of Northern Oklahoma Bahulikar, Rahul A.; Torres-Jerez, Ivone; Worley, Eric Applied and Environmental Microbiology, Vol. 80, Issue 18 https://doi.org/10.1128/AEM.02091-14	journal	July 2014
Erratum for Smercina et al., “To Fix or Not To Fix: Controls on Free-Living Nitrogen Fixation in the Rhizosphere” Smercina, Darian N.; Evans, Sarah E.; Friesen, Maren L. Applied and Environmental Microbiology, Vol. 85, Issue 22 https://doi.org/10.1128/AEM.02103-19	journal	November 2019
Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa Wargo, Matthew J. Applied and Environmental Microbiology, Vol. 79, Issue 7 https://doi.org/10.1128/AEM.03565-12	journal	January 2013
The Amino Acid Valine Is Secreted in Continuous-Flow Bacterial Biofilms Valle, J.; Da Re, S.; Schmid, S. Journal of Bacteriology, Vol. 190, Issue 1 https://doi.org/10.1128/JB.01405-07	journal	November 2007
Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa Wargo, Matthew J. Applied and Environmental Microbiology, Vol. 79, Issue 7 https://doi.org/10.1128/aem.03565-12	journal	January 2013
The Amino Acid Valine Is Secreted in Continuous-Flow Bacterial Biofilms Valle, J.; Da Re, S.; Schmid, S. Journal of Bacteriology, Vol. 190, Issue 1 https://doi.org/10.1128/jb.01405-07	journal	November 2007
Functional Ecology of Free-Living Nitrogen Fixation: A Contemporary Perspective Reed, Sasha C.; Cleveland, Cory C.; Townsend, Alan R. Annual Review of Ecology, Evolution, and Systematics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev-ecolsys-102710-145034	journal	December 2011
Bacterial Osmoregulation: A Paradigm for the Study of Cellular Homeostasis Wood, Janet M. Annual Review of Microbiology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102815	journal	October 2011
Small RNAs: A New Paradigm in Plant-Microbe Interactions Weiberg, Arne; Wang, Ming; Bellinger, Marschal Annual Review of Phytopathology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-phyto-102313-045933	journal	August 2014
N EW I NSIGHTS INTO THE R EGULATION AND F UNCTIONAL S IGNIFICANCE OF L YSINE M ETABOLISM IN P LANTS Galili, Gad Annual Review of Plant Biology, Vol. 53, Issue 1 https://doi.org/10.1146/annurev.arplant.53.091401.110929	journal	June 2002
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105159	journal	June 2006
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient Roley, Sarah S.; Duncan, David S.; Liang, Di PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0197320	journal	June 2018
Metabolite Profiling of Root Exudates of Common Bean under Phosphorus Deficiency Tawaraya, Keitaro; Horie, Ryota; Saito, Saki Metabolites, Vol. 4, Issue 3 https://doi.org/10.3390/metabo4030599	journal	July 2014
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Elsevier https://doi.org/10.5167/uzh-148899	text	January 2018

Cited By (1)

Data from: Switchgrass rhizosphere metabolite chemistry driven by nitrogen availability Smercina, Darian; Bowsher, Alan W.; Evans, Sarah E. Dryad https://doi.org/10.5061/dryad.9zw3r229b	dataset	January 2020