Effect of pollination on cell division, cell enlargement, and endogenous hormones in fruit development in a gynoecious cucumber

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Abstract

To study the effect of pollination on fruit development in gynoecious and parthenocarpic cucumbers (Cucumis sativus L. cv. NK × AN8), the number of cells, cell size, mitotic index, histone H4 gene expression, and concentrations of endogenous cytokinins and auxin were compared in fruits that had developed from pollinated and non-pollinated flowers. Fresh weight was more in the pollinated group 4–12 days after anthesis (DAA) in both winter and spring, and 2–6 DAA in the summer. In winter, mitotic index increased from anthesis to 2 DAA and then decreased gradually in the pollinated group but immediately after anthesis in the non-pollinated group. Histone H4 gene in the pericarp zone was expressed more strongly during the period from pre-anthesis to 2 DAA in the pollinated group in summer. Concentrations of zeatin, isopentenyladenine, and indole-3-acetic acid (IAA) were higher in the non-pollinated group 2 and 4 DAA and peaked 4 DAA in spring whereas isopentenyladenine and IAA showed no distinct peaks in the pollinated group. These results are incompatible with the idea that pollination activates cell division by stimulating the synthesis of cytokinins and auxin in cucumber fruits.

Introduction

Gynoecious and multi-pistillate types of cucumbers bear two times as many pistillate flowers as mono-pistillate type cucumbers do within a short period (Hikosaka and Sugiyama, 2004). Competition for the photoassimilate among fruits is intense in multi-pistillate type cultivars because many fruits develop simultaneously; the competition restricts the growth of fruits that develop later, leading to fruit abortion. It is well known that pollination reduces fruit abortion because pollination increases the levels of indole-3-acetic acid (IAA), zeatin, and gibberellin (GA), which are essential to fruit development (Sjut and Bangerth, 1981, Nagar and Raja Rao, 1986, Kim et al., 1992, Lewis et al., 1996, Ben-Cheikh et al., 1997, Yu et al., 2001b, Cowan et al., 2005). Kim et al. (1992) reported that (1) concentration of IAA in cucumber ovaries in a parthenocarpic cultivar was twice as high as that in ovaries of a non-parthenocarpic cultivar; (2) exogenously applied naphthaleneacetic acid (NAA) and N-(2-chloro-4-pyridil)-N′-phenylurea (CPPU) increased endogenous IAA; and (3) NAA and CPPU application could increase fruit-set in non-pollinated fruits. Therefore, the authors considered that auxin acts as a trigger to induce parthenocarpy. On the other hand, Takeno et al. (1992) found that application of 6N-benzyladenine (BA) stimulated cell division in cucumber fruits developing from non-pollinated flowers in both parthenocarpic and non-parthenocarpic cultivars but did not increase IAA concentrations in such fruits in either cultivar at 3 DAA. Therefore, the authors concluded that exogenous application of cytokinin led to parthenocarpy because it was the higher concentration of cytokinin, not that of auxin, that could stimulate cell division in a non-parthenocarpic cultivar.

Fruit size increases because of increase in both the number and size of cells. The period in which cell division occurs has been well studied in many fruits such as European parthenocarpic cucumber (Marcelis and Baan Hofman-Eijer, 1993), tomato (Bohner and Bangerth, 1988), Lagenaria leucantha (Yu et al., 2001a, Li et al., 2003), and blueberry (Cano-Medrano and Darnell, 1997). In cucumber, cell division occurs about a week after anthesis whereas cell elongation occurs throughout fruit development, although cell size increases markedly only after cell division begins to decline (Marcelis and Baan Hofman-Eijer, 1993).

Takeno et al. (1992) reported that in non-parthenocarpic cultivars, the concentration of IAA was higher in cucumber fruits that had developed from non-pollinated flowers than in those developed from pollinated flowers, although pollination had no effect on the concentration in parthenocarpic cultivars. Yu et al. (2001b) compared auxin and cytokinin concentrations between fruits treated with CPPU and those developed from pollinated flowers in L. leucantha and found that the concentration of IAA was higher in the latter group, whereas that of cytokinin was more or less the same in both. In cucumber, however, the effect of pollination on cytokinin concentration throughout fruit development has to be studied for a better understanding of the effect of pollination on fruit-set and cell division. Therefore, we tried to clarify the effect of pollination on cell division, cell enlargement, and endogenous cytokinin and auxin levels in parthenocarpic and gynoecious cucumbers.

Section snippets

Plant materials

Seeds of cucumber (Cucumis sativus L. cv. NK × AN8), which is of gynoecious, parthenocarpic, and plural-pistillate type (1–2 pistillate flowers per node), were sown on 15 October 2004 (Experiment 1), 19 May 2005 (Experiment 2), and 15 February 2005 (Experiment 3). The seeds were obtained from the Nihon Horticultural Production Institute (Matsudo, Japan). Single plants with three fully expanded leaves were transplanted into 20 l plastic containers filled with the growth medium (Soil Mix, Sakata

Fruit growth, cell division, and cell enlargement (Experiment 1)

Fruit fresh weight increased logarithmically 2 DAA and beyond in the case of pollinated flowers and 4 DAA and beyond in that of non-pollinated flowers (Fig. 1A). Fresh weight 4 DAA and beyond of fruits from pollinated flowers was significantly greater than that of fruits developing from non-pollinated flowers whereas the increase in the log of fresh weight with time (slope of the line) was almost the same in both (0.208 ± 0.008 vs. 0.204 ± 0.005).

The number of cells in each fruit did not differ

Discussion

Cell expansion phase is considered to either follow or associate the cell division phase in developing fruits. In Experiment 1, mitotic indices were significantly higher in the pollinated group 2 DAA and the number of cells was greater, although not significantly, 4 DAA. Furthermore, the histone H4 gene was expressed more strongly in the pollinated group 2 DAA, resulting in greater number of cells 2 DAA in Experiment 2. These results suggest that pollination stimulated cell division during the

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