Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root

Riccardo Di Mambro, Micol De Ruvo, Elena Pacifici, Elena Salvi, Rosangela Sozzani, Philip N. Benfey, Wolfgang Busch, Ondrej Novak, Karin Ljung, Luisa Di Paola, Athanasius F. M. Marée, Paolo Costantino, Verônica A. Grieneisen, and Sabrina Sabatini
PNAS first published August 22, 2017 https://doi.org/10.1073/pnas.1705833114

  1. Edited by Sarah Hake, University of California, Berkeley, CA, and approved June 26, 2017 (received for review April 11, 2017)

Significance

The maintenance of boundaries between neighboring groups of distinct cell types is vital during development of multicellular organisms, as groups of cells with distinct functions must be kept physically separated to guarantee correct control of organ and body growth and function. In the Arabidopsis root, the transition zone is a developmental boundary in the meristem that separates dividing from differentiating cells. Here, we infer that a well-defined and tightly controlled minimum of the hormone auxin acts as a signal to establish the position of the transition zone by controlling the developmental switch from cell division to cell differentiation. We provide the mechanistic and genetic basis of how another hormone, cytokinin, controls and positions this auxin minimum, thus regulating root size.

Abstract

In multicellular organisms, a stringent control of the transition between cell division and differentiation is crucial for correct tissue and organ development. In the Arabidopsis root, the boundary between dividing and differentiating cells is positioned by the antagonistic interaction of the hormones auxin and cytokinin. Cytokinin affects polar auxin transport, but how this impacts the positional information required to establish this tissue boundary, is still unknown. By combining computational modeling with molecular genetics, we show that boundary formation is dependent on cytokinin’s control on auxin polar transport and degradation. The regulation of both processes shapes the auxin profile in a well-defined auxin minimum. This auxin minimum positions the boundary between dividing and differentiating cells, acting as a trigger for this developmental transition, thus controlling meristem size.

Footnotes

  • ↵1R.D.M. and M.D.R. contributed equally to this work.

  • ↵2Present address: Dipartimento di Biologia, Università di Pisa, 56126 Pisa, Italy.

  • ↵3To whom correspondence may be addressed. Email: veronica.grieneisen{at}jic.ac.uk or sabrina.sabatini{at}uniroma1.it.

  • Author contributions: V.A.G. and S.S. conceived the research; R.D.M. and M.D.R. planned experiments; R.D.M. performed experiments; R.D.M., M.D.R., and A.F.M.M. planned simulations; M.D.R. and A.F.M.M. performed simulations; A.F.M.M. developed the code for simulations; M.D.R. and A.F.M.M. implemented the code for simulations; R.S., P.N.B., and W.B. performed ChIP-chip experiments; E.P. and E.S. cloned genes; O.N. and K.L. performed auxin measurement; L.D.P. discussed experiments; P.C. discussed experiments; R.D.M., M.D.R., A.F.M.M., V.A.G., and S.S. discussed and interpreted all results; and R.D.M., M.D.R., A.F.M.M., V.A.G., and S.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (accession no. GSE70595). The code and the scripts that generated all simulation outputs (graphs and images) are available on Bitbucket (https://bitbucket.org/mareelab/transitionzone).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1705833114/-/DCSupplemental.

  1. Riccardo Di Mambroa,1,2,
  2. Micol De Ruvoa,b,c,1,
  3. Elena Pacificia,
  4. Elena Salvia,
  5. Rosangela Sozzanid,
  6. Philip N. Benfeye,f,
  7. Wolfgang Buschg,
  8. Ondrej Novakh,
  9. Karin Ljungh,
  10. Luisa Di Paolab,
  11. Athanasius F. M. Maréec,
  12. Paolo Costantinoa,
  13. Verônica A. Grieneisenc,3, and
  14. Sabrina Sabatinia,i,3
  1. aDipartimento di Biologia e Biotecnologie, Laboratory of Functional Genomics and Proteomics of Model Systems, Università di Roma, Sapienza, 00185 Rome, Italy;
  2. bUnit of Chemical-Physics Fundamentals in Chemical Engineering, Department of Engineering, Università Campus Bio-Medico di Roma, 00128 Rome, Italy;
  3. cComputational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom;
  4. dDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695;
  5. eDepartment of Biology, Duke University, Durham, NC 27708;
  6. fHoward Hughes Medical Institute, Duke University, Durham, NC 27708;
  7. gGregor Mendel Institute, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria;
  8. hUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden;
  9. iIstituto Pasteur-Fondazione Cenci Bolognetti, 00100 Rome, Italy

  1. Edited by Sarah Hake, University of California, Berkeley, CA, and approved June 26, 2017 (received for review April 11, 2017)

Significance

The maintenance of boundaries between neighboring groups of distinct cell types is vital during development of multicellular organisms, as groups of cells with distinct functions must be kept physically separated to guarantee correct control of organ and body growth and function. In the Arabidopsis root, the transition zone is a developmental boundary in the meristem that separates dividing from differentiating cells. Here, we infer that a well-defined and tightly controlled minimum of the hormone auxin acts as a signal to establish the position of the transition zone by controlling the developmental switch from cell division to cell differentiation. We provide the mechanistic and genetic basis of how another hormone, cytokinin, controls and positions this auxin minimum, thus regulating root size.

Abstract

In multicellular organisms, a stringent control of the transition between cell division and differentiation is crucial for correct tissue and organ development. In the Arabidopsis root, the boundary between dividing and differentiating cells is positioned by the antagonistic interaction of the hormones auxin and cytokinin. Cytokinin affects polar auxin transport, but how this impacts the positional information required to establish this tissue boundary, is still unknown. By combining computational modeling with molecular genetics, we show that boundary formation is dependent on cytokinin’s control on auxin polar transport and degradation. The regulation of both processes shapes the auxin profile in a well-defined auxin minimum. This auxin minimum positions the boundary between dividing and differentiating cells, acting as a trigger for this developmental transition, thus controlling meristem size.

  • plant hormones
  • cell differentiation
  • root meristem
  • computational modeling

Footnotes

  • ↵1R.D.M. and M.D.R. contributed equally to this work.

  • ↵2Present address: Dipartimento di Biologia, Università di Pisa, 56126 Pisa, Italy.

  • ↵3To whom correspondence may be addressed. Email: veronica.grieneisen{at}jic.ac.uk or sabrina.sabatini{at}uniroma1.it.

  • Author contributions: V.A.G. and S.S. conceived the research; R.D.M. and M.D.R. planned experiments; R.D.M. performed experiments; R.D.M., M.D.R., and A.F.M.M. planned simulations; M.D.R. and A.F.M.M. performed simulations; A.F.M.M. developed the code for simulations; M.D.R. and A.F.M.M. implemented the code for simulations; R.S., P.N.B., and W.B. performed ChIP-chip experiments; E.P. and E.S. cloned genes; O.N. and K.L. performed auxin measurement; L.D.P. discussed experiments; P.C. discussed experiments; R.D.M., M.D.R., A.F.M.M., V.A.G., and S.S. discussed and interpreted all results; and R.D.M., M.D.R., A.F.M.M., V.A.G., and S.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (accession no. GSE70595). The code and the scripts that generated all simulation outputs (graphs and images) are available on Bitbucket (https://bitbucket.org/mareelab/transitionzone).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1705833114/-/DCSupplemental.

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Auxin minimum triggers cell differentiation
Riccardo Di Mambro, Micol De Ruvo, Elena Pacifici, Elena Salvi, Rosangela Sozzani, Philip N. Benfey, Wolfgang Busch, Ondrej Novak, Karin Ljung, Luisa Di Paola, Athanasius F. M. Marée, Paolo Costantino, Verônica A. Grieneisen, Sabrina Sabatini
Proceedings of the National Academy of Sciences Aug 2017, 201705833; DOI: 10.1073/pnas.1705833114
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