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Journal of Plant Growth Regulation

, Volume 33, Issue 2, pp 328–339 | Cite as

Carbon-11 Reveals Opposing Roles of Auxin and Salicylic Acid in Regulating Leaf Physiology, Leaf Metabolism, and Resource Allocation Patterns that Impact Root Growth in Zea mays

  • Beverly Agtuca
  • Elisabeth Rieger
  • Katharina Hilger
  • Lihui Song
  • Christelle A. M. Robert
  • Matthias Erb
  • Abhijit Karve
  • Richard A. FerrieriEmail author
Article

Abstract

Auxin (IAA) is an important regulator of plant development and root differentiation. Although recent studies indicate that salicylic acid (SA) may also be important in this context by interfering with IAA signaling, comparatively little is known about its impact on the plant’s physiology, metabolism, and growth characteristics. Using carbon-11, a short-lived radioisotope (t 1/2 = 20.4 min) administered as 11CO2 to maize plants (B73), we measured changes in these functions using SA and IAA treatments. IAA application decreased total root biomass, though it increased lateral root growth at the expense of primary root elongation. IAA-mediated inhibition of root growth was correlated with decreased 11CO2 fixation, photosystem II (PSII) efficiency, and total leaf carbon export of 11C-photoassimilates and their allocation belowground. Furthermore, IAA application increased leaf starch content. On the other hand, SA application increased total root biomass, 11CO2 fixation, PSII efficiency, and leaf carbon export of 11C-photoassimilates, but it decreased leaf starch content. IAA and SA induction patterns were also examined after root-herbivore attack by Diabrotica virgifera to place possible hormone crosstalk into a realistic environmental context. We found that 4 days after infestation, IAA was induced in the midzone and root tip, whereas SA was induced only in the upper proximal zone of damaged roots. We conclude that antagonistic crosstalk exists between IAA and SA which can affect the development of maize plants, particularly through alteration of the root system’s architecture, and we propose that the integration of both signals may shape the plant’s response to environmental stress.

Keywords

Carbon-11 PET imaging Auxin Salicylic acid Hormone crosstalk Root–herbivore interactions 

Notes

Acknowledgments

This article has been authored by Brookhaven Science Associates, LLC under contract number DE-AC02-98CH10886 with the U.S. Department of Energy (DOE), which supported R. A. Ferrieri in this effort. Additional support was provided by a DOE training grant through the University of Missouri and Brookhaven National Laboratory (Grant No. DE-SC0002040), which supported L. Song; the DOE SULI Program, which supported B. Agtuca; the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) Bonn, which supported E. Rieger and K. Hilger; a Marie Curie Intra-European Fellowship (Grant No. 273107), which supported M. Erb; a Swiss National Foundation Fellowship (Grant No. 140196), which supported C. Robert; and a USDA-DOE (Grant No. 2012-BNL-MO094-BUDG), which supported A. Karve. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a nonexclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The authors give a special thanks to M. Schueller for his assistance in isotope production and to D. Alexoff for his assistance in image analysis. Finally, the authors thank the USDA for supplying germplasm accessions of the B73 line through their National Plant Germplasm Service.

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Copyright information

© Springer Science+Business Media New York (outside the USA) 2013

Authors and Affiliations

  • Beverly Agtuca
    • 1
  • Elisabeth Rieger
    • 2
  • Katharina Hilger
    • 2
  • Lihui Song
    • 3
  • Christelle A. M. Robert
    • 4
    • 5
  • Matthias Erb
    • 4
  • Abhijit Karve
    • 6
  • Richard A. Ferrieri
    • 6
    Email author
  1. 1.State University of New York College of Environmental Science and ForestrySyracuseUSA
  2. 2.Fachbereich ChemieJohannes Gutenberg UniversitätMainzGermany
  3. 3.Plant Sciences Division, Department of Chemistry, Bond Life Sciences CenterUniversity of MissouriColumbiaUSA
  4. 4.Root-Herbivore Interactions GroupMax Planck Institute for Chemical EcologyJenaGermany
  5. 5.Department of BiochemistryMax Planck Institute for Chemical EcologyJenaGermany
  6. 6.Biosciences DepartmentBrookhaven National LaboratoryUptonUSA

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