Auxin depletion from leaf primordia contributes to organ patterning

Stem cells are responsible for organogenesis, but it is largely unknown whether and how information from stem cells acts to direct organ patterning after organ primordia are formed. It has long been proposed that the stem cells at the plant shoot apex produce a signal, which promotes leaf adaxial-ab...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 111; no. 52; pp. 18769 - 18774
Main Authors Qi, Jiyan, Wang, Ying, Yu, Ting, Cunha, Alexandre, Wu, Binbin, Vernoux, Teva, Meyerowitz, Elliot, Jiao, Yuling
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 30.12.2014
National Acad Sciences
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Summary:Stem cells are responsible for organogenesis, but it is largely unknown whether and how information from stem cells acts to direct organ patterning after organ primordia are formed. It has long been proposed that the stem cells at the plant shoot apex produce a signal, which promotes leaf adaxial-abaxial (dorsoventral) patterning. Here we show the existence of a transient low auxin zone in the adaxial domain of early leaf primordia. We also demonstrate that this adaxial low auxin domain contributes to leaf adaxial-abaxial patterning. The auxin signal is mediated by the auxin-responsive transcription factor MONOPTEROS (MP), whose constitutive activation in the adaxial domain promotes abaxial cell fate. Furthermore, we show that auxin flow from emerging leaf primordia to the shoot apical meristem establishes the low auxin zone, and that this auxin flow contributes to leaf polarity. Our results provide an explanation for the hypothetical meristem-derived leaf polarity signal. Opposite to the original proposal, instead of a signal derived from the meristem, we show that a signaling molecule is departing from the primordium to the meristem to promote robustness in leaf patterning. Significance Stem cells not only initiate organs, but may also contribute to organ patterning, at least in the shoot apex of flowering plants: classical microsurgical experiments imply that the shoot apical meristem promotes development of the leaf adaxial side, i.e., the upper side. In this study, we show the existence of a transient low auxin zone in the adaxial side that contributes to adaxial development. We further find that this adaxial low auxin zone results from auxin transport from leaves to the shoot apex. Thus, it is not a positive signal from stem cells, but departure of a signaling molecule from primordia to stem cells, that delivers polarity information—opposite to what is generally assumed.
Bibliography:http://dx.doi.org/10.1073/pnas.1421878112
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PMCID: PMC4284573
Contributed by Elliot Meyerowitz, November 20, 2014 (sent for review August 14, 2014; reviewed by Yuval Eshed and Lars Østergaard)
Reviewers: Y.E., Weizmann Institute of Science; and L.Ø., John Innes Centre.
Author contributions: J.Q., Y.W., T.Y., B.W., and T.V. performed research; Y.W., E.M., and Y.J. designed research; A.C. and T.V. contributed new reagents/analytic tools; J.Q., Y.W., A.C., T.V., E.M., and Y.J. analyzed data; and T.V., E.M., and Y.J. wrote the paper.
1J.Q. and Y.W. contributed equally to this work.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1421878112