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.

Wax Layers onCosmos bipinnatusPetals Contribute Unequally to Total Petal Water Resistance

“…Phaseolus vulgaris (Steinmüller and Tevini, 1985), Medicago truncatula (Zhang et al, 2005), and Pisum sativum (Gniwotta et al, 2005; the composition of V. faba leaf wax has not been reported yet). Arabidopsis flower wax is dominated by C 29 alkane (Shi et al, 2011), shorter than the prevalent C 31 homolog in leaves (Jenks et al, 1995) but similar to inflorescence stems and siliques (Todd et al, 1999). Overall, there appears to be a fairly widespread compositional pattern in flower waxes, in many species characterized by the presence of shorter chain lengths than on vegetative organs.…”

“…Noteworthy exceptions are detailed analyses of petal waxes for Crataegus monogyna and three cultivars of Rubus idaeus (Griffiths et al, 2000), Antirrhinum majus (Goodwin et al, 2003), Vicia faba (Griffiths et al, 1999), Cistus albidus (Hennig et al, 1988), Petunia hybrida (King et al, 2007), Arabidopsis (Arabidopsis thaliana; Shi et al, 2011), and Rosa damascena (Stoianova-Ivanova et al, 1971). Selected compound classes have been investigated for some more species, including selected Ericaceae (Salasoo, 1989), Rosaceae (Wollrab, 1969a(Wollrab, , 1969b, and Asteraceae (Akihisa et al, 1998) species.…”

Transcriptional analysis of cell wall and cuticle related genes during fruit development of two sweet cherry cultivars with contrasting levels of cracking tolerance

“…Although expression levels of PaWINB are higher in 'Kordia' only in the initial stage of fruit growth development ( Figure 3C), its action may influence a subsequent activity of other genes related to the synthesis of cuticular waxes such as WS and PaCER6. In addition, SHN transcription factors can affect the expression of various cell wall-modifying genes, increasing the amount of cellulose and simultaneously decreasing lignin levels, suggesting a close coordination between the cuticle and the synthesis of cell wall polysaccharides (Shi et al, 2011;Ambavaram et al, 2011). This might suggest that the tolerant 'Kordia', besides presenting a higher gene expression related to the synthesis of cuticular waxes may also have a higher activity of cell wall modification enzymes which could provide greater exocarp flexibility preventing the appearance of micro fractures during the expansion phases of fruit development.…”

Physical Interaction of Floral Organs Controls Petal Morphogenesis in Arabidopsis

“…The outer layer of the cutin is covered with cuticular wax, a complex of C 20 to C 60 aliphatics, aldehydes, ketones, and wax esters, coating the outermost surface of the plant body (Pollard et al, 2008). A series of Arabidopsis mutants defective in cuticle synthesis and secretion show the biological roles of cuticles as a barrier to biotic or abiotic stresses, osmotic stress, water loss, and damage from UV radiation, and in preventing the fusion of leaves and floral organs (Yephremov et al, 1999;Pruitt et al, 2000;Krolikowski et al, 2003;Aharoni et al, 2004;Kurdyukov et al, 2006;Bessire et al, 2007;Shi et al, 2011;Wang et al, 2011). Some mutants are known to be involved in petal morphogenesis: Lack of nanoridges of petals, due to a mutation in DEFECTIVE IN CUTICULAR RIDGES (DCR, encoding a BAHD acyltransferase), CYP77A6 (cytochrome P450 family), GLYCEROL-3-PHOSPHATE ACYLTRANSFERASE6 (GPAT6), or PERMEABLE CUTICLE1 (PEC1), result in increased permeability of petals to a dye and cause organ fusion (Li-Beisson et al, 2009;Panikashvili et al, 2009;Bessire et al, 2011).…”