Abstract
Summary The leaf outer epidermal cell wall acts as a barrier against pathogen attack and desiccation, and as such is covered by a cuticle, composed of waxes and the polymer cutin. Cutin monomers are formed by the transfer of fatty acids to glycerol by glycerol‐3‐phosphate acyltransferases, which facilitate their transport to the surface.The extent to which cutin monomers affect leaf cell wall architecture and barrier properties is not known. We report a dual functionality of pathogen‐inducible GLYCEROL‐3‐PHOSPHATE ACYLTRANSFERASE 6 (GPAT6) in controlling pathogen entry and cell wall properties affecting dehydration in leaves.Silencing of Nicotiana benthamiana NbGPAT6a increased leaf susceptibility to infection by the oomycetes Phytophthora infestans and Phytophthora palmivora, whereas overexpression of NbGPAT6a‐GFP rendered leaves more resistant. A loss‐of‐function mutation in tomato SlGPAT6 similarly resulted in increased susceptibility of leaves to Phytophthora infection, concomitant with changes in haustoria morphology. Modulation of GPAT6 expression altered the outer wall diameter of leaf epidermal cells. Moreover, we observed that tomato gpat6‐a mutants had an impaired cell wall–cuticle continuum and fewer stomata, but showed increased water loss.This study highlights a hitherto unknown role for GPAT6‐generated cutin monomers in influencing epidermal cell properties that are integral to leaf–microbe interactions and in limiting dehydration.
Highlights
Most epidermal cells of the aerial parts of vascular plants are covered by a hydrophobic extracellular lipid barrier, known as the cuticle, which is composed of polymeric cutin and waxes (Yeats & Rose, 2013)
We first identified all GPATs encoded in the tomato and N. benthamiana genomes and grouped them based on their phylogenetic relationship to the better characterized A. thaliana homologues (Fig. S1; Methods S1)
This revealed the presence of three N. benthamiana genes grouping with AtGPAT1/2/3 that probably contribute to storage lipid biosynthesis (Zheng et al, 2003), and three genes associated with AtGPAT5/7 that may be involved in suberin biosynthesis (Beisson et al, 2007)
Summary
Most epidermal cells of the aerial parts of vascular plants are covered by a hydrophobic extracellular lipid barrier, known as the cuticle, which is composed of polymeric cutin and waxes (Yeats & Rose, 2013). Cutin biosynthesis involves the esterification of oxygenated 16- or 18-carbon fatty acids to glycerol (Beisson et al, 2012) through the action of glycerol-3-phosphate acyltransferases (GPAT4, GPAT6 and GPAT8). These enzymes have specificity for the second carbon of the glycerol (sn-2 position) (Yang et al., 2012) and exhibit phosphatase activity that removes the phosphate group from glycerol-3-phosphate (Yang et al, 2010). GPAT6 is involved in cutin synthesis in A. thaliana petals (Li-Beisson et al, 2009) and tomato (Solanum lycopersicum) fruit (Petit et al, 2016) and was found to have multiple functions in stamen development and fertility (Li et al, 2012). A glossy fruit mutant of the tomato cv Micro-Tom with increased total wax load, but lower amounts of total cutin in fruit cuticles, and a much thinner cuticle (Petit et al, 2014), were discovered to be a result of a point mutation in the GPAT6 gene
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