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SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis

Abstract

Leaves of flowering plants are determinate organs produced by pluripotent structures termed shoot apical meristems. Once specified, leaves differentiate an adaxial (upper) side specialized for light capture, and an abaxial (lower) side specialized for gas exchange. A functional relationship between meristem activity and the differentiation of adaxial leaf fate has been recognized for over fifty years, but the molecular basis of this interaction is unclear. In Arabidopsis thaliana, activity of the class I KNOX (KNOTTED1-like homeobox) genes SHOOTMERISTEMLESS (STM) and BREVIPEDICELLUS (BP) is required for meristem function but excluded from leaves1,2,3, whereas members of the HD-Zip III (class III homeodomain leucine zipper) protein family function to promote both meristem activity and adaxial leaf fate4,5,6. Here we show that the zinc-finger protein SERRATE acts in a microRNA (miRNA) gene-silencing pathway to regulate expression of the HD-Zip III gene PHABULOSA (PHB) while also limiting the competence of shoot tissue to respond to KNOX expression. Thus, SERRATE acts to coordinately regulate meristem activity and leaf axial patterning.

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Figure 1: se alleles condition defects in leaf axial patterning and increased meristem size.
Figure 2: SE regulates PHB expression.
Figure 3: SE functions in a miRNA gene-silencing pathway.
Figure 4: SE antagonises KNOX activity.

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Acknowledgements

We are indebted to K. Barton and B. Reinhart for providing plasmids 35S::PHB (pJM2) and 35S::PHB-1D (pMKB2) and for sharing data before publication. For helpful discussions and seed storks we thank N. Ori and S. Hake (bp-9 seeds) and Y. Eshed and J. Bowman (phb-6; phv-5; rev-9/ + seeds). We also thank M. Prigge for se-1 Ler seeds, R. Sablowski for STMGR seeds and J. Langdale for comments on the manuscript, the Arabidopsis Biological Resource Center and Syngenta for se-3 and se-2 seeds respectively, and J. Baker for photography. Finally, we thank A. Bird and I. Henderson for advice on bisulphite sequencing. This work was funded by a BBSRC grant to M.T. S.P.G. is the recipient of a Sainsbury Studentship from the Gatsby Charitable Foundation and A.H. is the recipient of a University of Oxford Glasstone Research Fellowship.

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Correspondence to Miltos Tsiantis.

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Supplementary information

Supplemntary Figure S1

A schematic of the SE genomic locus indicating the positions of lesions in se mutant alleles, and contains information regarding transcripts produced by these alleles. (DOC 31 kb)

Supplementary Figure S2

RT-PCR and RNA gel blot analysis of expression of various transcripts in se-3 and Col, and contains descriptions of PCR conditions and primer sequences. (DOC 302 kb)

Supplementary Figure S3

A histogram reflecting the cytosine methylation status of a region of the PHB genomic locus in se-3 and Col. Clones generated from se-3 show reduced levels of CpG methylation. (PDF 77 kb)

Supplementary Figure S4

Gene expression analysis of the gibberellic acid biosynthetic gene GA5, demonstrating that this gene is similarly regulated in a KNOX gain-of-function line, a dominant phb mutant, and se-1. (DOC 137 kb)

Supplementary Methods

Experimental procedures used in generation of the supporting online material not included in the main methods section. (DOC 28 kb)

Supplementary Table S1

A sequence alignment of all clones analysed for generating bisulphite sequencing data presented in Supplementary Figure S3. (DOC 39 kb)

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Grigg, S., Canales, C., Hay, A. et al. SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437, 1022–1026 (2005). https://doi.org/10.1038/nature04052

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