FIDDLEHEAD , a gene required to suppress epidermal cell interactions in Arabidopsis , encodes a putative lipid biosynthetic enzyme

Abstract

In plants, the outer epidermal cell wall and cuticle presents a semipermeable barrier that maintains the external integrity of the plant and regulates the passage of various classes of molecules into and out of the organism. During vegetative development, the epidermal cells remain relatively inert, failing to respond to wounding or grafting. During reproductive development and fertilization, however, the epidermis is developmentally more labile and participates in two types of contact-mediated cell interactions: organ fusion and pollen hydration. Here we describe the isolation and characterization of one gene whose product normally functions in blocking both types of epidermal cell interactions during vegetative development: the FIDDLEHEAD gene. As suggested by previous biochemical analyses, the gene encodes a protein that is probably involved in the synthesis of long-chain lipids found in the cuticle and shows similarity to a large class of genes encoding proteins related to ␤-ketoacyl-CoA synthases and chalcone synthases. In situ hybridization reveals an epidermal pattern of expression consistent with a role for this protein in the synthesis of lipid components that are thought to localize extracellularly and probably modify the properties of the cuticle.

Functional conservation and maintenance of expression pattern of FIDDLEHEAD-like genes in Arabidopsis and Antirrhinum

“…GFP fluorescence was detected exclusively in the epidermis of various organs of the transgenic plants ( Figure 6). There was no indication of the expression of FDH in phloem or other nonepidermal cells, conversely to what has been reported previously (Pruitt et al, 2000). The expression pattern was equivalent to that revealed by in situ hybridization with a FDH probe in wild-type Arabidopsis (Yephremov et al, 1999), confirming that the promoter fragment carried all cis-acting elements required for normal expression.…”

“…The FDH gene belongs to the FAE1 family, the members of which encode known and putative b-ketoacyl-CoA synthases expressed during seed development and in the epidermis (Yephremov et al, 1999;Pruitt et al, 2000). This plant gene family contains multiple sequences, including 21 predicted proteins encoded in the complete Arabidopsis genome (Lechelt-Kunze et al, 2003).…”

“…Using in situ hybridization, FDH transcripts have been detected in protodermis cells and in the epidermis of vegetative organs and floral organs, including carpels prior to fusion (Yephremov et al, 1999) and ovules (Pruitt et al, 2000). To investigate the regulatory DNA sequences in the FDH promoter, a 1122-bp region upstream of the FDH coding sequence was fused to GFP, and its expression was studied in 11 independent families of transgenic plants.…”

“…Orchestration of a number of pathways and cell-cell communication are necessary for proper differentiation of protodermal cells (Van Den Berg et al, 1997;Huelskamp and Schnittger, 1998). In Arabidopsis, studies on the FIDDLEHEAD (FDH), HIGH CARBON DIOXIDE (HIC), LACERATA (LCR) and WAX2/YORE-YORE genes have revealed a role for fatty acid metabolism in this process (Yephremov et al, 1999;Pruitt et al, 2000;Wellesen, 2001;Chen et al, 2003;Kurata et al, 2003). The FDH and HIC genes code for putative b-ketoacylCoA synthases of the FATTY ACID ELONGA-TION1 (FAE1) gene family, which consists of 21 genes in Arabidopsis (Lechelt-Kunze et al, 2003).…”

“…The epidermis-specific FDH gene is implicated in the control of a barrier function associated with the outermost cell walls of the epidermis (Lolle et al, 1997;Yephremov et al, 1999;Pruitt et al, 2000). Suppression of this function in fdh mutants results in ectopic organ fusions, and allows wildtype pollen to germinate on the leaf epidermis of fdh mutants (Lolle et al, 1992;Lolle and Cheung, 1993).…”