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Repression of BLADE-ON-PETIOLE genes by KNOX homeodomain protein BREVIPEDICELLUS is essential for differentiation of secondary xylem in Arabidopsis root

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Abstract

Main conclusion

Repression of boundary genes by KNOTTED1-like homeodomain transcription factor BREVIPEDICELLUS promotes the differentiation of phase II secondary xylem in Arabidopsis roots.

Plant growth and development relies on the activity of meristems. Boundaries are domains of restricted growth that separate forming organs and the meristem. Class I KNOX homeodomain transcription factors are important regulators of meristem maintenance. Members of this class including BREVIDICELLUS also called KNOTTED-LIKE FROM ARABIDOPSIS THALIANA1 (BP/KNAT1) fulfill this function in part by spatially regulating boundary genes. The vascular cambium is a lateral meristem that allows for radial expansion of organs during secondary growth. We show here that BP/KNAT1 repression of boundary genes plays a crucial role in root secondary growth. In particular, exclusion of BLADE-ON-PETIOLE1/2 (BOP1/2) and other members of this module from xylem is required for the differentiation of lignified fibers and vessels during the xylem expansion phase of root thickening. These data reveal a previously undiscovered role for boundary genes in the root and shed light on mechanisms controlling wood development in trees.

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Abbreviations

ATH1:

ARABIDOPSIS THALIANA HOMEOBOX GENE1

BP:

BREVIPEDICELLUS

BOP:

BLADE-ON-PETIOLE

PNY:

PENNYWISE

PNF:

POUND-FOOLISH

SAM:

Shoot apical meristem

TALE:

Three amino acid loop extension

KNOX:

KNOTTED1-like homeobox

KNAT:

KNOTTED-like from Arabidopsis thaliana

BELL:

BELL1-like

HCl:

Hydrochloric acid

Col:

Columbia

GA:

Gibberellin

GUS:

β-Glucuronidase

ARK:

ARBORKNOX

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Acknowledgements

This work was supported by a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant (No. 327195) to SRH and NSERC Undergraduate Summer Research Assistantships to NW. The IJPB benefits from the support of the Labex Saclay Plant Sciences (ANR-10-LABX-0040-SPS). Thank you to Jean-Christophe Palauqui for critical reading of the manuscript.

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    1. Department of Biology and Institute of Biochemistry, Carleton University, 1125 Colonel By Drive, Ottawa, ON, K1S 5B6, Canada

      Natalie Woerlen, Gamalat Allam, Adina Popescu, Laura Corrigan & Shelley R. Hepworth

    2. Institut Jean-Pierre Bourgin, UMR1318, INRA, Agro Paris Tech, CNRS, Université Paris-Saclay, RD10, 78026, Versailles Cedex, France

      Natalie Woerlen, Adina Popescu & Véronique Pautot

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    1. Natalie Woerlen
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    Correspondence to Shelley R. Hepworth.

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    G. Allam and A. Popescu contributed equally to this work.

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    Woerlen, N., Allam, G., Popescu, A. et al. Repression of BLADE-ON-PETIOLE genes by KNOX homeodomain protein BREVIPEDICELLUS is essential for differentiation of secondary xylem in Arabidopsis root. Planta 245, 1079–1090 (2017). https://doi.org/10.1007/s00425-017-2663-2

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