Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss

Abstract

SUMMARYPlant cuticles are broadly composed of two major components: polymeric cutin and a mixture of waxes, which infiltrate the cutin matrix and also accumulate on the surface, forming an epicuticular layer. Although cuticles are thought to play a number of important physiological roles, with the most important being to restrict water loss from aerial plant organs, the relative contributions of cutin and waxes to cuticle function are still not well understood. Tomato (Solanum lycopersicum) fruits provide an attractive experimental system to address this question as, unlike other model plants such as Arabidopsis, they have a relatively thick astomatous cuticle, providing a poreless uniform material that is easy to isolate and handle. We identified three tomato mutants, cutin deficient 1 (cd1), cd2 and cd3, the fruit cuticles of which have a dramatic (95-98%) reduction in cutin content and substantially altered, but distinctly different, architectures. This cutin deficiency resulted in an increase in cuticle surface stiffness, and in the proportions of both hydrophilic and multiply bonded polymeric constituents. Furthermore, our data suggested that there is no correlation between the amount of cutin and the permeability of the cuticle to water, but that cutin plays an important role in protecting tissues from microbial infection. The three cd mutations were mapped to different loci, and the cloning of CD2 revealed it to encode a homeodomain protein, which we propose acts as a key regulator of cutin biosynthesis in tomato fruit.

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

“…fruit growth, visual aspect, cracking, water loss, resistance to pathogens, and postharvest shelf-life) are highly dependent on fruit cuticle (Bargel and Neinhuis, 2005;Saladié et al, 2007;Matas et al, 2009;Domínguez et al, 2011;Parsons et al, 2012). An increasing number of studies highlight the possibilities offered by tomato for analyzing cuticle architecture, mechanical properties, and permeability (López-Casado et al, 2007;Saladié et al, 2007;MintzOron et al, 2008;Buda et al, 2009;Isaacson et al, 2009;Wang et al, 2011) and for discovering genes contributing to cuticle synthesis and regulation (Hovav et al, 2007;Mintz-Oron et al, 2008;Girard et al, 2012;Nadakuduti et al, 2012;Yeats et al, 2012b;Shi et al, 2013). Nevertheless, to further our understanding of the relationships between cuticle composition and architecture and cuticle properties and performance in plants, new tomato cuticle mutants are highly needed (Domínguez et al, 2011).…”

“…Less straightforward than TILLING, this approach relies first on the phenotypic characterization of the mutant trait and then on the identification of the mutation through map-based cloning, combined (or not) with the candidate gene approach or, more recently, through whole-genome sequencing (Abe et al, 2012;Just et al, 2013). Using this strategy, new cuticle-related genes involved in cuticle regulation (the cd2 HD-ZIP IV mutant; Isaacson et al, 2009), cutin monomer biosynthesis (the cyp86A9 mutant; Shi et al, 2013), and cutin polymerization (the cutin synthase mutant; Yeats et al, 2012b) were recently uncovered in tomato EMS mutant collections. However, when considering the large number of candidate genes involved in the regulation, synthesis, and transport processes necessary for cuticle formation (Matas et al, 2011;Yeats and Rose, 2013), very few tomato cuticle mutants have been described to date (Kimbara et al, 2012;Nadakuduti et al, 2012;Shi et al, 2013).…”

“…Interestingly, one of the three fruit cutin-deficiency (cd1) mutants identified in the M82 tomato mutant collection (Menda et al, 2004;Isaacson et al, 2009) was recently identified as a SlGDSL2 truncation mutant (Yeats et al, 2012b). The discovery of SlGDSL2 mutations by two independent screenings of unrelated tomato mutant collections in M82 and 'Micro-Tom' is probably not a mere coincidence.…”

“…The thick and easy-to-isolate peel from tomato has long been used for studying the biomechanical properties of plant cuticle (Domínguez et al, 2011). In recent years, the increased availability of tomato genomic resources, including saturated genetic linkage maps, markers, and very recently the tomato genomic sequence (Tomato Genome Consortium, 2012), offered unprecedented possibilities for exploiting tomato as a model for studying plant cuticle (Hovav et al, 2007;Adato et al, 2009;Isaacson et al, 2009;Girard et al, 2012;Yeats et al, 2012b;Shi et al, 2013). To fully explore the relationships between cuticle composition and cuticle properties and to discover new genes and functions, new sources of genetic variability affecting tomato genes involved in wax, cutin, and suberin synthesis and regulation are required.…”

EliA is required for inducing the stearyl alcohol-mediated expression of secretory proteins and production of polyester in Ralstonia sp. NT80

“…In the natural environment, land plants use fatty alcohols, such as palmityl and stearyl alcohols, to form waxes, which provide protection against desiccation, bacterial attacks and UV radiation (Buschhaus & Jetter, 2011;Isaacson et al, 2009). Lipases (EC 3.1.1.3) catalyse hydrolysis not only of glycerides formed from glycerol and long-chain fatty acids but also of various esters including polyesters.…”