Plants can use protein as a nitrogen source without assistance from other organisms

  1. Chanyarat Paungfoo-Lonhienne*,
  2. Thierry G. A. Lonhienne,
  3. Doris Rentsch,
  4. Nicole Robinson*,
  5. Michael Christie,
  6. Richard I. Webb§,
  7. Harshi K. Gamage*,
  8. Bernard J. Carroll,
  9. Peer M. Schenk*, and
  10. Susanne Schmidt*,
  1. *School of Integrative Biology,
  2. ARC Centre of Excellence for Integrative Legume Research, School of Molecular and Microbial Sciences, and School of Land Crop and Food Sciences, and
  3. §Centre for Microscopy and Microanalysis, University of Queensland, Queensland 4072, Australia; and
  4. Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland
  1. Edited by Peter Vitousek, Stanford University, Stanford, CA, and approved January 25, 2008 (received for review December 21, 2007)

Abstract

Nitrogen is quantitatively the most important nutrient that plants acquire from the soil. It is well established that plant roots take up nitrogen compounds of low molecular mass, including ammonium, nitrate, and amino acids. However, in the soil of natural ecosystems, nitrogen occurs predominantly as proteins. This complex organic form of nitrogen is considered to be not directly available to plants. We examined the long-held view that plants depend on specialized symbioses with fungi (mycorrhizas) to access soil protein and studied the woody heathland plant Hakea actites and the herbaceous model plant Arabidopsis thaliana, which do not form mycorrhizas. We show that both species can use protein as a nitrogen source for growth without assistance from other organisms. We identified two mechanisms by which roots access protein. Roots exude proteolytic enzymes that digest protein at the root surface and possibly in the apoplast of the root cortex. Intact protein also was taken up into root cells most likely via endocytosis. These findings change our view of the spectrum of nitrogen sources that plants can access and challenge the current paradigm that plants rely on microbes and soil fauna for the breakdown of organic matter.

Footnotes

  • To whom correspondence should be addressed. E-mail: susanne.schmidt{at}uq.edu.au
  • Author contributions: C.P.-L. and T.G.A.L. contributed equally to this work; B.J.C., P.M.S., and S.S. contributed equally to this work; C.P.-L., T.G.A.L., D.R., B.J.C., P.M.S., and S.S. designed research; C.P.-L., T.G.A.L., N.R., M.C., R.I.W., and H.K.G. performed research; C.P.-L., T.G.A.L., B.J.C., and S.S. contributed new reagents/analytic tools; C.P.-L., T.G.A.L., D.R., N.R., R.I.W., B.J.C., P.M.S., and S.S. analyzed data; and C.P.-L., T.G.A.L., D.R., N.R., B.J.C., P.M.S., and S.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0712078105/DC1.

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