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Research Article

Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana

View ORCID ProfileElke Barbez, Kai Dünser, Angelika Gaidora, Thomas Lendl, and View ORCID ProfileWolfgang Busch
PNAS June 13, 2017 114 (24) E4884-E4893; first published May 30, 2017; https://doi.org/10.1073/pnas.1613499114
Elke Barbez
aGregor Mendel Institute, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria;
bDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, 1190 Vienna, Austria;
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  • ORCID record for Elke Barbez
  • For correspondence: wbusch@salk.edu elkebarbez@gmail.com
Kai Dünser
bDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, 1190 Vienna, Austria;
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Angelika Gaidora
aGregor Mendel Institute, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria;
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Thomas Lendl
aGregor Mendel Institute, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria;
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Wolfgang Busch
aGregor Mendel Institute, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria;
cPlant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037
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  • ORCID record for Wolfgang Busch
  • For correspondence: wbusch@salk.edu elkebarbez@gmail.com
  1. Edited by Mark Estelle, University of California at San Diego, La Jolla, CA, and approved May 8, 2017 (received for review August 12, 2016)

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Significance

Cellular growth in plants is constrained by cell walls; hence, loosening these structures is required for growth. The long-standing acid growth theory links auxin signaling, apoplastic pH homeostasis, and cellular expansion, providing a conceptual framework for cell expansion in plant shoots. Intriguingly, this model remains heavily debated for roots. Here, we present a fluorescent dye that allows for the correlation of cell size and apoplastic pH at a cellular resolution in Arabidopsis thaliana. This enabled us to elucidate a complex involvement of auxin in root apoplastic pH homeostasis, which is important for root cell expansion and gravitropic response. These findings shed light on the poorly understood acid growth mechanism in roots.

Abstract

Plant cells are embedded within cell walls, which provide structural integrity, but also spatially constrain cells, and must therefore be modified to allow cellular expansion. The long-standing acid growth theory postulates that auxin triggers apoplast acidification, thereby activating cell wall-loosening enzymes that enable cell expansion in shoots. Interestingly, this model remains heavily debated in roots, because of both the complex role of auxin in plant development as well as technical limitations in investigating apoplastic pH at cellular resolution. Here, we introduce 8-hydroxypyrene-1,3,6-trisulfonic acid trisodium salt (HPTS) as a suitable fluorescent pH indicator for assessing apoplastic pH, and thus acid growth, at a cellular resolution in Arabidopsis thaliana roots. Using HPTS, we demonstrate that cell wall acidification triggers cellular expansion, which is correlated with a preceding increase of auxin signaling. Reduction in auxin levels, perception, or signaling abolishes both the extracellular acidification and cellular expansion. These findings jointly suggest that endogenous auxin controls apoplastic acidification and the onset of cellular elongation in roots. In contrast, an endogenous or exogenous increase in auxin levels induces a transient alkalinization of the extracellular matrix, reducing cellular elongation. The receptor-like kinase FERONIA is required for this physiological process, which affects cellular root expansion during the gravitropic response. These findings pinpoint a complex, presumably concentration-dependent role for auxin in apoplastic pH regulation, steering the rate of root cell expansion and gravitropic response.

  • apoplastic pH
  • auxin
  • cellular expansion
  • root growth
  • root gravitropism

Footnotes

  • ↵1To whom correspondence may be addressed. Email: wbusch{at}salk.edu or elkebarbez{at}gmail.com.
  • Author contributions: E.B. and W.B. designed research; E.B., K.D., and A.G. performed research; T.L. contributed a new analytic tool; E.B., K.D., and A.G. analyzed data; and E.B. and W.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The raw data files of the presented experiments have been uploaded to the Dryad database, datadryad.org (doi: 10.5061/dryad.sq7s3).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1613499114/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Apoplastic pH regulation in A. thaliana roots
Elke Barbez, Kai Dünser, Angelika Gaidora, Thomas Lendl, Wolfgang Busch
Proceedings of the National Academy of Sciences Jun 2017, 114 (24) E4884-E4893; DOI: 10.1073/pnas.1613499114

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Apoplastic pH regulation in A. thaliana roots
Elke Barbez, Kai Dünser, Angelika Gaidora, Thomas Lendl, Wolfgang Busch
Proceedings of the National Academy of Sciences Jun 2017, 114 (24) E4884-E4893; DOI: 10.1073/pnas.1613499114
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