Fleshy fruits are highly prized for nutritional content, flavor, fragrance, and appearance. While most fruits are eaten when ripe, a subset, including many that for culinary purposes are viewed as vegetables, are consumed immature. Cucumbers (Cucumis sativus), which are used as fresh product and processed into pickles, are typically harvested at the middle or end of the exponential growth phase, 1–2 weeks post-pollination, and approximately 2–3 weeks prior to fruit maturation.
Early fruit development is typified by phases of cell division and expansion [1
]. In cucumber fruit, which develop from an enlarged inferior ovary, cell division occurs most rapidly prior to anthesis and then continues more slowly in the first 0–5 days post anthesis [2
]. This phase largely overlaps with the period of highest respiration [4
]. Fruit elongation begins almost immediately after pollination, with the most rapid increase occurring approximately 4–12 days post pollination (dpp) [6
]. The rapid increase in cell size mirrors the rapid increase in fruit length, with obvious increase in vacuolization of mesocarp cells, and thickening in epidermal cell walls occurring between 8 and 16 dpp [6
]. Cell division and expansion are largely completed by 12–16 dpp, with some variation depending on cultivar and season [4
In addition to cell division and expansion, early development also includes specialized tissue and organ development and interaction with the abiotic and biotic environment. For example, developing cucumber fruit exhibit a distinct change in susceptibility to the soil-borne, oomycete pathogen, Phytophthora capsici
; young fruit are highly susceptible, while older fruit are resistant [8
]. There is a sharp transition in susceptibility that occurs at approximately 10–12 dpp coinciding with the end of the period of rapid fruit elongation. This age-related resistance suggests additional kinds of developmental changes occurring in the young cucumber fruit.
Although a limited number of studies have examined gene expression during early fruit development, a picture reflecting cell division and expansion is beginning to emerge based on transcriptomic studies of apple, cucumber, grape, tomato and watermelon. Among the enriched categories associated with tomato fruit set, were genes associated with protein biosynthesis, histones, nucleosome and chromosome assembly and cell cycle, suggesting a profile reflective of active cell division [10
]. In contrast, various water, sugar and organic acid transport-associated genes were under-represented, but then increased with the transition from cell division to cell expansion. Highly expressed categories of genes expressed in expanding cucumber, as well as apple, grape, tomato, melon and watermelon fruits, included cytoskeleton and cell wall modifying genes such as tubulins, expansins, endo-1,2-B-glucanase, beta glucosidases, pectate lyases, and pectin methylesterases, and transport associated genes such as aquaporins, vacuolar H+ATPases, and phloem-associated proteins [6
]. The most highly represented transcripts in rapidly expanding cucumber fruit (8 dpp) also were strongly enriched for defense related homologs including, lipid, latex, and defense-related genes, e.g., chitinase, thionin, hevein, snakin, peroxidase, catalase, thioredoxin, and dehydrins [6
The early stages of fruit development, including fruit set and exponential growth, are clearly essential for all fruits. However, despite their importance as determinants of fruit size and yield, there has been little detailed analysis of this phase of development. Most studies to date, including recent transcriptomic studies, have focused on late development, or a broad range of developmental stages, with only a single snapshot during early development eg., [19
]. In this study we combined morphological characterization with transcriptome analysis to provide new insight into important early fruit developmental stages and processes. Our observations, performed at five time points during the period from fruit set through the end of exponential fruit growth, indicate that this is a dynamic period of cucumber fruit development involving an array of internal and external morphological, physiological, and transcriptomic changes that act in concert with phases of active cell division, expansion, and response to the environment. Relative to anthesis and early fruit set, the period of peak- and late-exponential growth includes a large portion of highly represented transcripts, either of unknown function, or without homologs in Arabidopsis, suggesting unique factors contributing to the rapid growth phase in cucurbits. The end of exponential growth was marked by a shift in transcriptome profile characterized by abiotic and biotic stress related genes and significant enrichment for transcription factor gene homologs associated with stress response and development, suggesting that the interval between expansive growth and ripening may include a programmed transition toward enhanced defense.