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The SlSHN2 transcription factor contributes to cuticle formation and epidermal patterning in tomato fruit.

ABSTRACT: Tomato (Solanum lycopersicum) is an established model for studying plant cuticle because of its thick cuticle covering and embedding the epidermal cells of the fruit. In this study, we screened an EMS mutant collection of the miniature tomato cultivar Micro-Tom for fruit cracking mutants and found a mutant displaying a glossy fruit phenotype. By using an established mapping-by-sequencing strategy, we identified the causal mutation in the SlSHN2 transcription factor that is specifically expressed in outer epidermis of growing fruit. The point mutation in the shn2 mutant introduces a K to N amino acid change in the highly conserved 'mm' domain of SHN proteins. The cuticle from shn2 fruit showed a ~ fivefold reduction in cutin while abundance and composition of waxes were barely affected. In addition to alterations in cuticle thickness and properties, epidermal patterning and polysaccharide composition of the cuticle were changed. RNAseq analysis further highlighted the altered expression of hundreds of genes in the fruit exocarp of shn2, including genes associated with cuticle and cell wall formation, hormone signaling and response, and transcriptional regulation. In conclusion, we showed that a point mutation in the transcriptional regulator SlSHN2 causes major changes in fruit cuticle formation and its coordination with epidermal patterning.

SUBMITTER: Bres C

PROVIDER: S-EPMC10515250 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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The SlSHN2 transcription factor contributes to cuticle formation and epidermal patterning in tomato fruit.

Bres Cécile C Petit Johann J Reynoud Nicolas N Brocard Lysiane L Marion Didier D Lahaye Marc M Bakan Bénédicte B Rothan Christophe C

Molecular horticulture 20220607 1

Tomato (Solanum lycopersicum) is an established model for studying plant cuticle because of its thick cuticle covering and embedding the epidermal cells of the fruit. In this study, we screened an EMS mutant collection of the miniature tomato cultivar Micro-Tom for fruit cracking mutants and found a mutant displaying a glossy fruit phenotype. By using an established mapping-by-sequencing strategy, we identified the causal mutation in the SlSHN2 transcription factor that is specifically expressed ...[more]

PMID: 37789465

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Project description:The fruit surface is a unique tissue with multiple roles influencing fruit development, post-harvest storage and quality, and consumer acceptability. Serving as the first line of protection against herbivores, pathogens, and abiotic stress, the surface can vary markedly among species, cultivars within species, and developmental stage. In this study we explore developmental changes and natural variation of cucumber (Cucumis sativus L.) fruit surface properties using two cucumber lines which vary greatly for these traits and for which draft genomes and a single nucleotide polymorphism (SNP) array are available: Chinese fresh market type, Chinese Long '9930' (CL9930), and pickling type, 'Gy14'. Thin-section samples were prepared from the mid-region of fruit harvested at 0, 4, 8, 12, 16, 20, 24 and 30 days post pollination (dpp), stained with Sudan IV and evaluated for cuticle thickness, depth of wax intercalation between epidermal cells, epidermal cell size and shape, and number and size of lipid droplets. 'Gy14' is characterized by columnar shaped epidermal cells, a 2-3 fold thicker cuticular layer than CL9930, increased cuticular intercalations between cells and a larger number and larger sized lipid droplets. In both lines maximal deposition of cuticle and increase in epidermal size coincided with exponential fruit growth and was largely completed by approximately 16 dpp. Phenotyping and quantitative trait locus mapping (QTL) of fruit sampled from an F7:F8 Gy14 × CL9930 recombinant inbred line (RIL) population identified QTL regions on chromosomes 1, 4 and 5. Strong QTL for epidermal cell height, cuticle thickness, intercalation depth, and diameter of lipid droplets co-localized on chromosome 1. SSR markers on chromosome 1 were used to screen for recombinants in an extended RIL population to refine the QTL region. Further fine mapping by KASP assay combined with gene expression profiling suggested a small number of candidate genes. Tissue specificity, developmental analysis of expression, allelic diversity and gene function implicate the regulatory factor CsSHINE1/WIN1 as a source of natural variation for cucumber fruit epidermal traits.

Project description:Two important biophysical properties, the thermal and UV-Vis screening capacity, of isolated tomato fruit cuticle membranes (CM) have been studied by differential scanning calorimetry (DSC) and UV-Vis spectrometry, respectively. A first order melting, corresponding to waxes, and a second order glass transition (T g ) thermal events have been observed. The glass transition was less defined and displaced toward higher temperatures along the fruit ripening. In immature and mature green fruits, the CM was always in the viscous and more fluid state but, in ripe fruits, daily and seasonal temperature fluctuations may cause the transition between the glassy and viscous states altering the mass transfer between the epidermal plant cells and the environment. CM dewaxing reduced the T g value, as derived from the role of waxes as fillers. T g reduction was more intense after polysaccharide removal due to their highly interwoven distribution within the cutin matrix that restricts the chain mobility. Such effect was amplified by the presence of phenolic compounds in ripe cuticle membranes. The structural rigidity induced by phenolics in tomato CMs was directly reflected in their mechanical elastic modulus. The heat capacity (Cp rev ) of cuticle membranes was found to depend on the developmental stage of the fruits and was higher in immature and green stages. The average Cp rev value was above the one of air, which confers heat regulation capacity to CM. Cuticle membranes screened the UV-B light by 99% irrespectively the developmental stage of the fruit. As intra and epicuticular waxes contributed very little to the UV screening, this protection capacity is attributed to the absorption by cinnamic acid derivatives. However, the blocking capacity toward UV-A is mainly due to the CM thickness increment during growth and to the absorption by flavone chalconaringenin accumulated during ripening. The build-up of phenolic compounds was found to be an efficient mechanism to regulate both the thermal and UV screening properties of cuticle membranes.

Project description:BackgroundFruit maturation and ripening are genetically regulated processes that involve a complex interplay of plant hormones, growth regulators and multiple biological and environmental factors. Tomato (Solanum lycopersicum) has been used as a model of biological and genetic studies on the regulation of specific ripening pathways, including ethylene, carotenoid and cell wall metabolism. This model has also been used to investigate the functions of upstream signalling and transcriptional regulators. Thus far, many ripening-associated transcription factors that influence fruit development and ripening have been reported. NAC transcription factors are plant specific and play important roles in many stages of plant growth and development, such as lateral root formation, secondary cell wall synthesis, and embryo, floral organ, vegetative organ and fruit development.ResultsTissue-specific analysis by quantitative real-time PCR showed that SlNAC1 was highly accumulated in immature green fruits; the expression of SlNAC1 increased with fruit ripening till to the highest level at 7 d after the breaker stage. The overexpression of SlNAC1 resulted in reduced carotenoids by altering carotenoid pathway flux and decreasing ethylene synthesis mediated mainly by the reduced expression of ethylene biosynthetic genes of system-2, thus led to yellow or orange mature fruits. The results of yeast one-hybrid experiment demonstrated that SlNAC1 can interact with the regulatory regions of genes related lycopene and ethylene synthesis. These results also indicated that SlNAC1 inhibited fruit ripening by affecting ethylene synthesis and carotenoid accumulation in SlNAC1 overexpression lines. In addition, the overexpression of SlNAC1 reduced the firmness of the fruits and the thickness of the pericarp and produced more abscisic acid, resulting in the early softening of fruits. Hence, in SlNAC1 overexpression lines, both ethylene-dependent and abscisic acid-dependent pathways are regulated by SlNAC1 in fruit ripening regulatory network.ConclusionsSlNAC1 had a broad influence on tomato fruit ripening and regulated SlNAC1 overexpression tomato fruit ripening through both ethylene-dependent and abscisic acid-dependent pathways. Thus, this study provided new insights into the current model of tomato fruit ripening regulatory network.

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The SlSHN2 transcription factor contributes to cuticle formation and epidermal patterning in tomato fruit.

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The SlSHN2 transcription factor contributes to cuticle formation and epidermal patterning in tomato fruit.

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