SHINE Transcription Factors Act Redundantly to Pattern the Archetypal Surface of Arabidopsis Flower Organs

Abstract

Floral organs display tremendous variation in their exterior that is essential for organogenesis and the interaction with the environment. This diversity in surface characteristics is largely dependent on the composition and structure of their coating cuticular layer. To date, mechanisms of flower organ initiation and identity have been studied extensively, while little is known regarding the regulation of flower organs surface formation, cuticle composition, and its developmental significance. Using a synthetic microRNA approach to simultaneously silence the three SHINE (SHN) clade members, we revealed that these transcription factors act redundantly to shape the surface and morphology of Arabidopsis flowers. It appears that SHNs regulate floral organs' epidermal cell elongation and decoration with nanoridges, particularly in petals. Reduced activity of SHN transcription factors results in floral organs' fusion and earlier abscission that is accompanied by a decrease in cutin load and modified cell wall properties. SHN transcription factors possess target genes within four cutin- and suberin-associated protein families including, CYP86A cytochrome P450s, fatty acyl-CoA reductases, GSDL-motif lipases, and BODYGUARD1-like proteins. The results suggest that alongside controlling cuticular lipids metabolism, SHNs act to modify the epidermis cell wall through altering pectin metabolism and structural proteins. We also provide evidence that surface formation in petals and other floral organs during their growth and elongation or in abscission and dehiscence through SHNs is partially mediated by gibberellin and the DELLA signaling cascade. This study therefore demonstrates the need for a defined composition and structure of the cuticle and cell wall in order to form the archetypal features of floral organs surfaces and control their cell-to-cell separation processes. Furthermore, it will promote future investigation into the relation between the regulation of organ surface patterning and the broader control of flower development and biological functions.

Author Summary

The cuticular layer that covers all aerial parts of plants plays a vital role not only in the interaction with environment but also in plant development and growth. Despite the recent significant achievements in the identification of structural genes involved in cuticle biosynthesis and secretion, little is known regarding the regulation of metabolic pathways generating cuticular constituents, more specifically wax and cutin. The Arabidopsis AP2-type transcription factor SHINE1/WAX INDUCER1 (SHN1/WIN1) was the first assigned regulator of a cuticle-related metabolic pathway; nevertheless, its mode of action and biological function remain uncertain due to redundancy with two additional clade members. Here, by co-silencing all three SHN clade members using an artificial microRNAs approach, we demonstrated that SHN transcription factors act redundantly in patterning reproductive organ surface, modulating processes associated with cell elongation, adhesion, and separation, which secure the proper function of these organs. It appears that SHN transcription factors act directly on downstream cutin and cell wall–modifying genes. These factors are likely part of the genetic network controlling floral organ development. Thus, SHN transcription factors link together cuticle assembly, cell wall remodeling, and flower development to form the archetypal surface of floral organs mediating plant reproduction through pollination and seed dispersal.