Unraveling Cuticle Formation, Structure, and Properties by Using Tomato Genetic Diversity

The tomato (Solanum lycopersicum) fruit has a thick, astomatous cuticle that has become a model for the study of cuticle formation, structure, and properties in plants. Tomato is also a major horticultural crop and a long-standing model for research in genetics, fruit development, and disease resistance. As a result, a wealth of genetic resources and genomic tools have been established, including collections of natural and artificially induced genetic diversity, introgression lines of genome fragments from wild relatives, high-quality genome sequences, phenotype and gene expression databases, and efficient methods for genetic transformation and editing of target genes. This mini-review reports the considerable progresses made in recent years in our understanding of cuticle by using and generating genetic diversity for cuticle-associated traits in tomato. These include the synthesis of the main cuticle components (cutin and waxes), their role in the structure and properties of the cuticle, their interaction with other cell wall polymers as well as the regulation of cuticle formation. It also addresses the opportunities offered by the untapped germplasm diversity available in tomato and the current strategies available to exploit them.

Peridermal fruit skin formation in Actinidia sp. (kiwifruit) is associated with genetic loci controlling russeting and cuticle formation

Background The skin (exocarp) of fleshy fruit is hugely diverse across species. Most fruit types have a live epidermal skin covered by a layer of cuticle made up of cutin while a few create an outermost layer of dead cells (peridermal layer). Results In this study we undertook crosses between epidermal and peridermal skinned kiwifruit, and showed that epidermal skin is a semi-dominant trait. Furthermore, backcrossing these epidermal skinned hybrids to a peridermal skinned fruit created a diverse range of phenotypes ranging from epidermal skinned fruit, through fruit with varying degrees of patches of periderm (russeting), to fruit with a complete periderm. Quantitative trait locus (QTL) analysis of this population suggested that periderm formation was associated with four loci. These QTLs were aligned either to ones associated with russet formation on chromosome 19 and 24, or cuticle integrity and coverage located on chromosomes 3, 11 and 24. Conclusion From the segregation of skin type and QTL analysis, it appears that skin development in kiwifruit is controlled by two competing factors, cuticle strength and propensity to russet. A strong cuticle will inhibit russeting while a strong propensity to russet can create a continuous dead skinned periderm.

Evolutionary assembly of cooperating cell types in an animal chemical defense system

A long-standing challenge in biology is explaining how the functions of multicellular organs emerge from the underlying evolution of cell types. We deconstructed evolution of an organ novelty: a rove beetle gland that secretes a defensive cocktail. We show that gland function was pieced together via assembly of two cell types that manufacture distinct compounds. One cell type forms a chemical reservoir in the beetle's abdomen and produces alkane and ester compounds. We demonstrate that this cell type is a hybrid of cuticle cells and ancient pheromone and adipocyte-like cells, and executes its function via a mosaic of enzymes sourced from each parental cell type. The second cell type synthesizes noxious benzoquinones using a chimeric pathway derived from conserved cellular energy and cuticle formation pathways. We present evidence that evolution of each cell type was shaped by coevolution between the two cell types: the benzoquinones produced by the second cell type dissolve in solvents produced by the first, yielding a potent secretion that confers adaptive value onto the gland as a whole. Our findings illustrate how cooperation between cell types can arise, generating new, organ-level behaviors.

Differential regulation of triterpene biosynthesis induced by an early failure in cuticle formation in apple

Waxy apple cuticles predominantly accumulate ursane-type triterpenes, but the profile shifts with the induction of skin russeting towards lupane-type triterpenes. We previously characterised several key enzymes in the ursane-type and lupane-type triterpene pathways, but this switch in triterpene metabolism associated with loss of cuticle integrity is not fully understood. To analyse the relationship between triterpene biosynthesis and russeting, we used microscopy, RNA-sequencing and metabolite profiling during apple fruit development. We compared the skin of three genetically-close clones of ‘Golden Delicious’ (with waxy, partially russeted and fully russeted skin). We identified a unique molecular profile for the russet clone, including low transcript abundance of multiple cuticle-specific metabolic pathways in the early stages of fruit development. Using correlation analyses between gene transcription and metabolite concentration we found MYB transcription factors strongly associated with lupane-type triterpene biosynthesis. We showed how their transcription changed with the onset of cuticle cracking followed by russeting and that one factor, MYB66, was able to bind the promoter of the oxidosqualene cyclase OSC5, to drive the production of lupeol derivatives. These results provide insights into the breakdown of cuticle integrity leading to russet and how this drives MYB-regulated changes to triterpene biosynthesis.

First mass spectrometric report of cryptocyanin, a moulting protein from the mud crab Scylla serrata (Forskål, 1775) (Decapoda: Brachyura: Portunidae) in India

The mud crab Scylla serrata (Forskål, 1775) is a highly abundant and economically important species throughout coastal India. Cryptocyanin plays an important role during the moult cycle of brachyuran crabs, and the presence of cryptocyanin and haemocyanin in oocytes, embryos, and zoeas of various species suggests that cryptocyanin is available from the very early stage of cuticle formation in development. Cryptocyanin is highly similar to haemocyanin in structure, but it is a copper-free enzyme that lacks an oxygen-binding capacity. Cryptocyanin has furthermore been reported as an important factor in immunity in crustaceans. The precise molecular weight of the cryptocyanin protein from gill tissues of S. serrata (79.11 kDa) is reported with the help of the matrix-assisted laser desorption/ionization mass spectrophotometry (MALDI-MS) technique.