HANABA TARANU (HAN) Bridges Meristem and Organ Primordia Boundaries through PINHEAD, JAGGED, BLADE-ON-PETIOLE2 and CYTOKININ OXIDASE 3 during Flower Development in Arabidopsis.

Lian Ding,Jianyu Zhao,Shuangshuang Yan,Juan Zhang,Li Jiang,Qian Wang,Xiaolan Zhang,Kang Ning,Xiaofeng Liu,Wensheng Zhao,Xing Wang Deng

doi:10.1371/journal.pgen.1005479

Abstract

Shoot organ primordia are initiated from the shoot apical meristem and develop into leaves during the vegetative stage, and into flowers during the reproductive phase. Between the meristem and the newly formed organ primordia, a boundary with specialized cells is formed that separates meristematic activity from determinate organ growth. Despite interactions that have been found between boundary regulators with genes controlling meristem maintenance or primordial development, most boundary studies were performed during embryogenesis or vegetative growth, hence little is known about whether and how boundaries communicate with meristem and organ primordia during the reproductive stage. We combined genetic, molecular and biochemical tools to explore interactions between the boundary gene HANABA TARANU (HAN) and two meristem regulators BREVIPEDICELLUS (BP) and PINHEAD (PNH), and three primordia-specific genes PETAL LOSS (PTL), JAGGED (JAG) and BLADE-ON-PETIOLE (BOP) during flower development. We demonstrated the key role of HAN in determining petal number, as part of a set of complex genetic interactions. HAN and PNH transcriptionally promote each other, and biochemically interact to regulate meristem organization. HAN physically interacts with JAG, and directly stimulates the expression of JAG and BOP2 to regulate floral organ development. Further, HAN directly binds to the promoter and intron of CYTOKININ OXIDASE 3 (CKX3) to modulate cytokinin homeostasis in the boundary. Our data suggest that boundary-expressing HAN communicates with the meristem through the PNH, regulates floral organ development via JAG and BOP2, and maintains boundary morphology through CKX3 during flower development in Arabidopsis.

Highlights

Leaves and flowers originate from the shoot apical meristem (SAM), which contains pluripotent stem cells and resides at the tip of each stem
Previous studies showed that boundary genes interact with meristem regulators and primordia genes during embryogenesis or leaf development
Whether and how boundaries communicate with meristem and organ primordia during flower development remains largely unknown

Summary

Introduction

Leaves and flowers originate from the shoot apical meristem (SAM), which contains pluripotent stem cells and resides at the tip of each stem. Primordia are initiated from the peripheral zone of the SAM in a predictable pattern, and develop into leaves during the vegetative stage, and into flowers during the reproductive phase. Each flower consists of four concentric whorls of organ types: the protective sepals, the showy petals, the male stamens, and the female carpels [1]. Between the meristem and newly formed leaf or flower primordia, a boundary forms with specialized cells that separate meristematic activity from determinate organ growth [2]. M-O (meristem-organ) boundaries separate leaf and flower primordia from the SAM, whereas O-O (organ-organ) boundaries develop between individual floral organs and create space between them [2, 7]

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