QTL and transcriptomic analyses implicate cuticle transcription factor SHINE as a source of natural variation for epidermal traits in cucumber fruit

Authors: RETT-CADMAN, STEPHANIE - Michigan State University; COLLE, MARIVI - Michigan State University; MANSFELD, BEN - Michigan State University; BARRY, CORNELIUS - Michigan State University; WANG, YUHUI - University Of Wisconsin; Weng, Yiqun; GAO, LEI - Cornell University; FEI, ZHANGJUN - Cornell University; GRUMET, REBECCA - Michigan State University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/28/2019
Publication Date: 11/27/2019
Citation: Rett-Cadman, S., Colle, M., Mansfeld, B.N., Barry, C., Wang, Y., Weng, Y., Gao, L., Fei, Z., Grumet, R. 2019. QTL and transcriptomic analyses implicate cuticle transcription factor SHINE as a source of natural variation for epidermal traits in cucumber fruit. Frontiers in Plant Science. 10:1536. https://doi.org/10.3389/fpls.2019.01536.
DOI: https://doi.org/10.3389/fpls.2019.01536

Interpretive Summary: Background information: The fruit surface is a unique tissue impacting fruit development, protection against herbivores, pathogens, and abiotic stresses, post-harvest storage and quality, and consumer acceptability. Epidermal cell structure can influence fruit firmness and susceptibility to damage, while cuticle structure and waxiness can modify external appearance, rate of water loss, susceptibility to cracking, and material penetration into the fruit surface. Much of our understanding of epidermal cell structure and cuticle development is derived from mutant or overexpression analyses in model systems; little is known about factors driving variation in natural populations. Findings: In this study we explore developmental changes and natural variation of cucumber fruit surface properties using two cucumber lines: Chinese Long line 9930 and US pickling cucumber line Gy14 which vary greatly for these traits. Thin-section samples were prepared from the mid-region of fruit harvested at different times after pollination for microscopic observations. We found that Gy14 is characterized by columnar shaped epidermal cells, thicker cuticular layer, 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. We conducted QL analysis for fruit epidermal features, and identified strong QTL for epidermal cell height, cuticle thickness, intercalation depth, and diameter of lipid droplets that were co-localized on chromosome 1. Multiple evidence from 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. Why it is important? We identified the regulatory factor CsSHINE1/WIN1 as a source of natural variation for cucumber fruit epidermal traits. As epidermal properties influence both consumer preferences and longevity in the market chain, allelic variation in CsSHN1 may provide a valuable target for breeders developing varieties to meet desired fruit quality characteristics. Who cares? Results from this study are of interest to plant geneticists to understand the molecular mechanism of fruit skin development. Cucumber breeders may take advantage of the findings to develop varieties to meet desired fruit quality characteristics.

Technical Abstract: 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.