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A novel role of BELL1-like homeobox genes, PENNYWISE and POUND-FOOLISH, in floral patterning

Abstract

Flowers are determinate shoots comprised of perianth and reproductive organs displayed in a whorled phyllotactic pattern. Floral organ identity genes display region-specific expression patterns in the developing flower. In Arabidopsis, floral organ identity genes are activated by LEAFY (LFY), which functions with region-specific co-regulators, UNUSUAL FLORAL ORGANS (UFO) and WUSCHEL (WUS), to up-regulate homeotic genes in specific whorls of the flower. PENNYWISE (PNY) and POUND-FOOLISH (PNF) are redundant functioning BELL1-like homeodomain proteins that are expressed in shoot and floral meristems. During flower development, PNY functions with a co-repressor complex to down-regulate the homeotic gene, AGAMOUS (AG), in the outer whorls of the flower. However, the function of PNY as well as PNF in regulating floral organ identity in the central whorls of the flower is not known. In this report, we show that combining mutations in PNY and PNF enhance the floral patterning phenotypes of weak and strong alleles of lfy, indicating that these BELL1-like homeodomain proteins play a role in the specification of petals, stamens and carpels during flower development. Expression studies show that PNY and PNF positively regulate the homeotic genes, APETALA3 and AG, in the inner whorls of the flower. Moreover, PNY and PNF function in parallel with LFY, UFO and WUS to regulate homeotic gene expression. Since PNY and PNF interact with the KNOTTED1-like homeodomain proteins, SHOOTMERISTEMLESS (STM) and KNOTTED-LIKE from ARABIDOPSIS THALIANA2 (KNAT2) that regulate floral development, we propose that PNY/PNF-STM and PNY/PNF-KNAT2 complexes function in the inner whorls to regulate flower patterning events.

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Abbreviations

SAM:

Shoot apical meristem

KNOX:

Knotted1-like homeobox

BLH:

BELL1-like homeobox

PNY:

PENNYWISE

PNF:

POUND-FOOLISH

LFY:

LEAFY

UFO:

UNUSUAL FLORAL ORGANS

WUS:

WUSCHEL

AP3:

APETALA3

AG:

AGAMOUS

STM:

SHOOTMERISTEMLESS

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Acknowledgments

We thank Dr. Xuemei Chen for the pCIT565 and pD793 plamids, Dr. Jeff Long for the pDW22.1 plasmid, and Dr. G. Venugopala Reddy for the pBSWUS plasmid. We also thank Drs. Patricia Springer, Xuemei Chen and Susan Byrd for critical reading of this manuscript. We are thankful to the anonymous reviewers for their helpful comments. We are grateful to Dr. Patricia Springer for microscopy help for the in situ images and Dr. David Carter at the Genome Core Facility for help with the SEM. This research was supported by the National Science Foundation grant number IOB-0615774.

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Correspondence to Harley M. S. Smith.

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Yu, L., Patibanda, V. & Smith, H.M.S. A novel role of BELL1-like homeobox genes, PENNYWISE and POUND-FOOLISH, in floral patterning. Planta 229, 693–707 (2009). https://doi.org/10.1007/s00425-008-0867-1

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Keywords

  • Arabidopsis
  • Development
  • Meristem
  • Homeodomain
  • Flower
  • Patterning