The Epidermis-Specific Extracellular BODYGUARD Controls Cuticle Development and Morphogenesis inArabidopsis

Abstract

The outermost epidermal cell wall is specialized to withstand pathogens and natural stresses, and lipid-based cuticular polymers are the major barrier against incursions. The Arabidopsis thaliana mutant bodyguard (bdg), which exhibits defects characteristic of the loss of cuticle structure not attributable to a lack of typical cutin monomers, unexpectedly accumulates significantly more cell wall-bound lipids and epicuticular waxes than wild-type plants. Pleiotropic effects of the bdg mutation on growth, viability, and cell differentiation are also observed. BDG encodes a member of the a/b-hydrolase fold protein superfamily and is expressed exclusively in epidermal cells. Using Strep-tag epitope-tagged BDG for mutant complementation and immunolocalization, we show that BDG is a polarly localized protein that accumulates in the outermost cell wall in the epidermis. With regard to the appearance and structure of the cuticle, the phenotype conferred by bdg is reminiscent of that of transgenic Arabidopsis plants that express an extracellular fungal cutinase, suggesting that bdg may be incapable of completing the polymerization of carboxylic esters in the cuticular layer of the cell wall or the cuticle proper. We propose that BDG codes for an extracellular synthase responsible for the formation of cuticle. The alternative hypothesis proposes that BDG controls the proliferation/differentiation status of the epidermis via an unknown mechanism.

Arabidopsis LTPG Is a Glycosylphosphatidylinositol-Anchored Lipid Transfer Protein Required for Export of Lipids to the Plant Surface

“…Alkanes of other chain lengths were not significantly different from the wild type. Besides this cuticular wax phenotype, ltpg-1 mutants were indistinguishable from the wild type and displayed no organ fusions, unlike some other mutants with cuticle defects (Kurdyukov et al, 2006;Bird et al, 2007).…”

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).…”

Analyses of Tomato Fruit Brightness Mutants Uncover Both Cutin-Deficient and Cutin-Abundant Mutants and a New Hypomorphic Allele of GDSL Lipase

“…However, the most striking result is that the dull fruit aspect of tomato cuticle mutants appears primarily due to different epidermal cell differentiation. The relationship between epidermal cell differentiation and cuticle development is now well established and genes controlling both cell morphogenesis and cuticle synthesis have been identified (Kurdyukov et al, 2006;Javelle et al, 2011;Oshima et al, 2013). More indirect effects may also arise from perturbations in fruit cell division and development that affect cuticle formation in tomato fruit (Czerednik et al, 2012).…”