Effects of Maleic Hydrazide Treatment on the Size and Number of Cells and Sugar Accumulation in the Fruit of Melons (Cucumis melo L.)

in HortScience

The relationships between the size and the number of cells and sugar accumulation in melon fruit have been examined. Maleic hydrazide (MH) was used to investigate the relationships. Although cell size was markedly larger in MH-treated fruit than in untreated fruit in the early stages of fruit development, the number of cells in MH-treated fruit was less than in untreated fruit in latter fruit development. Sucrose, glucose, and fructose content were higher in MH-treated fruit than in untreated fruit. It is therefore suggested that sucrose accumulation in fruit subjected to MH treatment is accelerated as a result of early cell enlargement and that sucrose content increases further as a result of the decrease in the number of cells in the fruit during late development.

Abstract

The relationships between the size and the number of cells and sugar accumulation in melon fruit have been examined. Maleic hydrazide (MH) was used to investigate the relationships. Although cell size was markedly larger in MH-treated fruit than in untreated fruit in the early stages of fruit development, the number of cells in MH-treated fruit was less than in untreated fruit in latter fruit development. Sucrose, glucose, and fructose content were higher in MH-treated fruit than in untreated fruit. It is therefore suggested that sucrose accumulation in fruit subjected to MH treatment is accelerated as a result of early cell enlargement and that sucrose content increases further as a result of the decrease in the number of cells in the fruit during late development.

Sucrose is the most important factor determining the sweetness of melon fruit. The rate of sucrose accumulation in melon fruit increases during the latter half of the fruit development as the result of cell enlargement (Kano, 2002). In addition, sucrose accumulation has been demonstrated to occur in response to cellular enlargement if cell size is increased by auxin treatment during early fruit development (Kano, 2002) as well as in response to heating fruits (Kano, 2006). Conversely, sucrose accumulation in melon fruit can be suppressed by mechanical restriction resulting from relative decreases in the number of large cells associated with such treatment (Kano, 2004a) or by treatment with plant growth inhibitors (Kano, 2004b). Sucrose accumulation is suppressed in Japanese pears as a result of an increase in the number of small cells that result from 2-chloro-4-pyridyl-N-phenylurea treatment (Kano, 2003). Thus, it is considered that increased sucrose accumulation is associated with a higher number of large cells relative to small cells in the fruit. Most of the imported sugars accumulate in the vacuole of sink-tissue storage cells (Leigh et al., 1979; Yamaki and Ino, 1992). Cell size during the latter stage of fruit development is mostly equal to that of the vacuole because vacuoles in peaches force the cytoplasm to the outside of the mesocarp cells in the middle stages of fruit development (Ishida et al., 1973). Taken together, these findings suggest that the occurrence of lots of large cells is associated with increased sucrose content. The treatment of seeds with maleic hydrazine (MH) was found to increase cell size and vacuolation in wheat seedlings (Mendhulkar, 2000), and low concentrations of MH have been shown to increase cell length in algae (Gupta and Kumar, 1970). Furthermore, the inhibition of sprouting in onion has been demonstrated by MH treatment (Benkeblia, 2004; Benkeblia et al., 2002; El-Otmani et al., 2003) as a result of its effects on inhibiting cell division (Marcano, et al., 2004; Zilkah, et al.,1981), Thus, MH treatment has the effect of both accelerating cell enlargement as well as inhibiting cell division. Consequently, I hypothesized that sucrose content increases in melon fruit with early cell enlargement and with a cessation in cell division after an inflexion point.

I therefore treated melon fruit with MH to clarify the relationship between the size and the number of cells and sugar accumulation in the fruit.

Materials and Methods

Plant materials.

Earl's Knight Natsukei No.2 (Cucumis melo L.) melon seeds were planted in a seedbed on 20 Mar. 2004 with nursery plants spaced at 40-cm intervals in a plastic film greenhouse on 20 Apr. 2004. The flowers that opened on ≈14 June were used in this experiment. Only one fruit was borne on about the 12th node of each plant and the main stems were pinched at the 20th node. Three fruits were used in each treatment. The fruits on the 30th day after anthesis (DAA), considered to be the time when sucrose accumulation is initiated, were thoroughly sprayed with an MH solution at 2000 mg·L−1. The three fruits that were collected and weighed at 40 and 50 DAA for the control and MH treatments, respectively, were used for cell size and sugar analyses.

Measurements of cell number and size in the fruit.

Two ≈10-mm thick disks were cut from each of the three fruit from the control and MH-treated plants; one disk was excised from the fruit at the maximum transverse diameter toward the calyx end for cell analysis, whereas another was excised from the maximum transverse diameter toward the peduncle end for sugar analysis. Using a sharp table knife, a sample measuring ≈10 mm × 10 mm was removed from the disk with 5 mm straddling the maximum diameter line across each disk (Fig. 1). Rectangular parallelepipeds (hereafter RP), each measuring 7 mm, were serially sampled across the diameter of the disk using the same sharp table knife. Except for the RP containing seeds and the RPs at both ends containing the epidermis, all of the RPs along the 7-mm-long strips through the diameter of the fruit body were 8 and 9 and 12 and 12 at 40 and 50 DAA, respectively. All of the RPs obtained from fruit from each treatment were dehydrated by treatment using a series of alcohol concentrations (70%, 80%, 90%, and 100%) before being embedded in paraffin. Seven 10-μm-thick sections were prepared from these paraffin blocks, and the clearest section from each RP treatment was examined under a microscope. As shown in Figure 2, the maximum diameters of individual cells along the maximum transverse diameters of the RPs were measured. Cell size was calculated by dividing the total cell diameter measured in each RP from the three fruits or all RPs of three fruits by the number of cells of each RP of three fruits or the number of cells of all RPs of three fruits.

Fig. 1.
Fig. 1.

An illustration of the collection of rectangular parallelepiped (RP) parts for the determination of the size and number of cells and sugar content in melon fruits. This is an example for the untreated fruit on 40 d after anthesis.

Citation: HortScience horts 42, 6; 10.21273/HORTSCI.42.6.1357

Fig. 2.
Fig. 2.

An illustration of the measurement of the size and the number of cells of melon fruits 40 d after anthesis. White dots indicate the actual cells measured.

Citation: HortScience horts 42, 6; 10.21273/HORTSCI.42.6.1357

Sugar analysis.

The RPs from the disk taken from the maximum transverse diameter toward the peduncle end were used for sugar analysis. With exception of those RPs containing the seeds and both epidermal layers, all of the RPs were wrapped in cheesecloth and squeezed using pincers to extract the juice. The juice was diluted 10 times with distilled water before being centrifuged at 8000 × g for 15 min and filtered through a 0.45-μm filter. Then, 20 μL of filtrate was analyzed by high-performance liquid chromatography (LXC-10ADvp; Shimadzu, Kyoto, Japan) fitted with a refractive index detector (RID-10A; Shimadzu) equipped with Shim-pack SCR-101C (Shimadzu) at 0.8 mL·min−1 at 80 °C. Standard solutions of sucrose, glucose, and fructose at 20,000 mg·L−1 were injected into the high-performance liquid chromatograph before injection of the filtrates. Mean sucrose, glucose, and fructose content in each RP was calculated by dividing the total sucrose, glucose, and fructose content of each RP from three fruits by three. Mean sucrose, glucose, and fructose content in whole fruits was then estimated by dividing the total sucrose, glucose, and fructose content of all RPs from three fruits by the total number of PRs from the three fruit.

Results

The weights of MH-treated fruit at 40 and 50 DAA were not observed to differ from those of the untreated fruit (Fig. 3).

Fig. 3.
Fig. 3.

Effect of maleic hydrazide treatment on fruit growth. Maleic hydrazide was treated 30 d after anthesis. Vertical bars are sd (n = 3). ns, nonsignificant differences at P < 0.05 by t test.

Citation: HortScience horts 42, 6; 10.21273/HORTSCI.42.6.1357

The number of RPs with mean cell size larger than 250 μm at 40 DAA numbered three in the MH-treated fruit batch compared with one in the untreated fruit, and the number of RPs with a mean cell size exceeding 250 μm at 50 DAA was six in MH-treated fruit and eight in the untreated fruit (Table 1). Mean cell size for all RPs from MH-treated fruit at 40 DAA was 247 μm, whereas the fruit at 50 DAA did not differ between the two treatments. Although the number of RPs with more than 25 cells was eight in both treatments at 40 DAA, at 50 DAA, the number of RPs with more than 25 cells was one in MH-treated fruit compared with 10 in the untreated fruit (Table 2). The mean number of cells for all RPs at 40 DAA was 27 in both treatments, but the number at 50 DAA was 23 in MH-treated fruit, which was five less than that found in the untreated fruit.

Table 1.

Effects of maleic hydrazide (MH) treatment on cell size (μm) in each rectangular parellepiped (RP) and in all the RPs.

Table 1.
Table 2.

Effects of maleic hydrazide (MH) treatment on mean number of cells in each rectangular parelleepiped (RP) and mean number of cells in all the RPs and total number of cells in the fruit.

Table 2.

The number of RPs with sucrose contents greater than 40 g·L−1 at 40 DAA was six in MH-treated fruit compared with one in the untreated fruit (Table 3). The number of RPs with sucrose contents greater than 80 g·L−1 at 50 DAA was 5 in MH-treated fruit, compared with none in the untreated fruit. Mean sucrose, glucose, and fructose contents at 40 and 50 DAA were 10 to 15 g·L−1, 4 g·L−1, and 3 g·L−1 larger in MH-treated fruit compared with the untreated fruit, respectively.

Table 3.

Effects of maleic hydrazide (MH) treatment on sugar content (g·L−1) in each rectangular parellepiped (RP) and mean content in all the RPs.

Table 3.

However, it does not always follow that the sucrose content in RPs of MH-treated fruit with larger cells at 40 DAA is greater than that found in RPs of untreated fruit with smaller cells at 40 DAA (Tables 1 and 3). In fact, the sucrose content of RPs from MH-treated fruit with a smaller number of cells at 50 DAA is always higher than that found in RPs with a large number of cells in the untreated fruit (Tables 2 and 3).

Discussion

Cell size at 40 DAA was markedly greater in MH-treated fruit compared with untreated fruit. The MH treatment of seeds was found to increase cell size and vacuolation in wheat seedlings (Mendhulkar, 2000). Similarly, treatment with low concentrations of MH increases cell length in algae (Gupta and Kumar, 1970). Taken together, these results lend support to the hypothesis that the increase in cell size in MH-treated fruit at 40 DAA is attributable to the stimulation of cell enlargement by MH itself. Sucrose content was greater in MH-treated fruit at 40 DAA than in untreated fruit. Generally, the small vacuoles of meristematic cells increase in size and gradually coalesce as the cells enlarge and age (Esau, 1964). Most of the imported sugars accumulate in the vacuole of sink-tissue storage cells (Leigh et al., 1979; Yamaki and Ino, 1992). The mean cell volume of strawberry fruit increases slowly during active cell division, but rises rapidly and linearly for 10 d after cell division stops (Guiwen and Breen, 1992) with sucrose content in the vacuoles of strawberry fruit increasing from 25 to 35 DAA (Ofosu-Anim and Yamaki, 1994). Sucrose accumulates rapidly in the larger cells of melon fruit (Kano, 2002) because cell enlargement during early melon development results in dramatically increased sucrose content as a result of the increased duration of sucrose accumulation before harvesting (Kano, 2005). The treatment of various crops with MH has also been demonstrated to increase leaf carbohydrate content (Currier et al., 1951; Derridj et al., 1986), especially Gossypium herbaceum (McIlrath, 1950), Zea mays (Naylor, 1951) and Nicotiana tabacum (Seltmann and Nichols, 1984). Given these results, it is reasonable to assume that the sucrose accumulation in the cells of melon fruits treated with MH increases as a result of the early enlargement of vacuoles by rapid cell enlargement.

A fewer number of cells were found in MH-treated fruit at 50 DAA compared with the untreated fruit. After reaching the inflection point, before which fruit growth is primarily the result of cell division, any increase in melon size is the result of cell enlargement only. In the fruits of Cucurbits, this usually occurs when the fruit diameter is ≈20 mm (Masuda, 1970; Sinnott, 1939). Cell division in the tissues near the exocarp in the fruit of Lagenaria vulgaris continues until the middle stages of fruit growth (Sinnott, 1939) with cellular multiplication continuing until harvest in the fruit of the avocado (Schroeder, 1953). In this study, the total number of cells in the untreated fruit increased from 217 to 282 at 40 to 50 DAA, respectively (refer to Table 2). Consequently, slower rates of cell division, not as active as before the inflection point, are likely to continue during the mid to latter development stages in melon fruit. Therefore, the gradual decrease in cell number response to MH treatment only becomes apparent during the mid to latter stages of fruit development when some time has elapsed. Moreover, sucrose content was considerably higher in MH-treated fruit than in the untreated fruit 50 DAA. No cell division was observed during the latter stages of fruit development as a result of MH treatment, resulting in the production of fewer large cells and thus, smaller sucrose sink for the whole fruit. Consequently, the constant and active sucrose accumulation in large cells, which are fewer in number in MH-treated fruit, has the effect of further increasing sucrose content.

However, a clear relationship between cell size and sucrose content was not observed in RPs from untreated fruit and MH-treated fruit at 40 and 50 DAA. Although numerous vascular bundles develop in the mesocarp and endocarp of melon fruit, they change in number and diameter as a result of differential growth in the fruit (Kanahama and Saito, 1987). This is likely to be the reason for the apparent absence of any relationship between cell size and sucrose content of the RPs examined.

The following conclusion can be drawn from the results observed in MH-treated fruits: sucrose accumulation is promoted as a result of early cell enlargement associated with MH treatment and the concomitant decrease in the number of cells in the fruit during late development, which results in a further increase in sucrose content.

Literature Cited

  • BenkebliaN.2004Effect of maleic hydrazine on respiratory parameters of stored onion bulbs (Allium cepa L.)Bra. J. Plant Physiol.164752

  • BenkebliaN.VaroquauxP.ShiomiN.SakaiH.2002Storage technology of onion bulbs cv. Rouge Amposta: Effects of irradiation, maleic hydrazide and carbamate isopropyl N-phenyl (CIP) on respiration rate and carbohydratesInter. J. Food Sci. Tech.37169175

    • Search Google Scholar
    • Export Citation
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  • DerridjS.FialaV.JolivetE.1986Increase of European corn borer (Ostrinia nubilalis) oviposition induced by a treatment of maize plants with maleic hydrazide: Role of leaf carbohydrate contentEntomol. Exp. Appl.41305310

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  • El-OtmaniM.NdiaveA.Ait-OubahouA.KaananeA.2003Effects of preharvest foliar application of maleic hydrazide and storage conditions on onion quality postharvestActa Hort.628615622

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    • Export Citation
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  • GuiwenW.C.BreenP.J.1992Cell count and size in relation to fruit size among strawberry cultivarsJ. Amer. Soc. Hort. Soc.117946950

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    • Search Google Scholar
    • Export Citation
  • KanoY.2002Relationship between sucrose accumulation and cell size in 4-CPA-treated melon fruits (Cucumis melo L.)J. Hort. Sci. Biotechnol.77546550

    • Search Google Scholar
    • Export Citation
  • KanoY.2003Effect of GA and CPPU treatments on cell size and type of sugars accumulated in Japanese pear fruitJ. Hort. Sci. Biotechnol.78331334

    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • KanoY.2004bEffect of SADH treatment on cell size and kind of sugars accumulated in melon fruitsJ. Hort. Sci. Biotech.791417

  • KanoY.2005Comparison of the effects of 4-CPA and CPPU treatment on melon cell size and sugar accumulationEnviron. Control Biol.43147154

    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
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  • MendhulkarV.D.2000Effect of maleic hydrazide on somatic cells and nuclear size in Triticum aestivum LinnAdvances in Plant Sciences. Acad. Plant Sci. Muzaffarnager India.13567572

    • Search Google Scholar
    • Export Citation
  • NaylorA.W.1951Accumulation of sucrose in maize following treatment with maleic hydrazideArch. Biochem. Biophys.33340342

  • Ofosu-AnimJ.YamakiS.1994Sugar content, compartmentation, and efflux in strawberry tissueJ. Amer. Soc. Hort. Sci.11910241028

  • SchroederC.A.1953Growth and development of the Fuerte avocado fruitJ. Amer. Soc. Hort. Sci.61103109

  • SeltmannH.NicholsB.C.1984Agronomic, physical and visual characteristics of hand suckered on maleic hydrazide treated flue-cured and burley tobaccosAgron. J.76375378

    • Search Google Scholar
    • Export Citation
  • SinnottE.W.1939A developmental analysis of the relation between cell size and fruit size in CucurbitsAmer. J. Bot.26179189

  • YamakiS.InoM.1992Alteration of cellular compartmentation and membrane permeability to sugars in immature and mature apple fruitJ. Amer. Soc. Hort. Sci.117951954

    • Search Google Scholar
    • Export Citation
  • ZilkahS.OsbandM.E.McCaffreyR.1981Effect of inhibitors of plant cell division on mammalian tumor cells in vitroCancer Res.4118791883

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Contributor Notes

I thank Ms. S. Tasaka and Ms. M. Maeguchi for their technical assistance. E-mail gansho@ishikawa-pu.ac.jp.

Article Sections

Article Figures

  • View in gallery

    An illustration of the collection of rectangular parallelepiped (RP) parts for the determination of the size and number of cells and sugar content in melon fruits. This is an example for the untreated fruit on 40 d after anthesis.

  • View in gallery

    An illustration of the measurement of the size and the number of cells of melon fruits 40 d after anthesis. White dots indicate the actual cells measured.

  • View in gallery

    Effect of maleic hydrazide treatment on fruit growth. Maleic hydrazide was treated 30 d after anthesis. Vertical bars are sd (n = 3). ns, nonsignificant differences at P < 0.05 by t test.

Article References

  • BenkebliaN.2004Effect of maleic hydrazine on respiratory parameters of stored onion bulbs (Allium cepa L.)Bra. J. Plant Physiol.164752

  • BenkebliaN.VaroquauxP.ShiomiN.SakaiH.2002Storage technology of onion bulbs cv. Rouge Amposta: Effects of irradiation, maleic hydrazide and carbamate isopropyl N-phenyl (CIP) on respiration rate and carbohydratesInter. J. Food Sci. Tech.37169175

    • Search Google Scholar
    • Export Citation
  • CurrierH.B.DayB.E.CraftsA.S.1951Some effects of maleic hydrazide on plantsBot. Gaz.112272280

  • DerridjS.FialaV.JolivetE.1986Increase of European corn borer (Ostrinia nubilalis) oviposition induced by a treatment of maize plants with maleic hydrazide: Role of leaf carbohydrate contentEntomol. Exp. Appl.41305310

    • Search Google Scholar
    • Export Citation
  • El-OtmaniM.NdiaveA.Ait-OubahouA.KaananeA.2003Effects of preharvest foliar application of maleic hydrazide and storage conditions on onion quality postharvestActa Hort.628615622

    • Search Google Scholar
    • Export Citation
  • EsauK.1964Vacuoles2325Plant anatomyJohn Wiley & Sons, IncNew York, London, Sydney

  • GuiwenW.C.BreenP.J.1992Cell count and size in relation to fruit size among strawberry cultivarsJ. Amer. Soc. Hort. Soc.117946950

  • GuptaR.S.KumarH.D.1970The effect of maleic hydrazide on growth and mutation of a blue-green algaArch. Microbiol.70330339

  • IshidaM.InabaA.SobajimaY.1973Physiological studies on the growth and development of peach fruits. I. Anatomical changes during the development of peach fruitsSci. Rep. Kyoto Pref. Univ. Agr. No.2518

    • Search Google Scholar
    • Export Citation
  • KanahamaK.SaitoS.1987Vascular system and carpel arrangement in the fruits of melon, cucumber and Luffa acutangula RoxbJ. Jpn. Soc. Hort. Sci.55476483

    • Search Google Scholar
    • Export Citation
  • KanoY.2002Relationship between sucrose accumulation and cell size in 4-CPA-treated melon fruits (Cucumis melo L.)J. Hort. Sci. Biotechnol.77546550

    • Search Google Scholar
    • Export Citation
  • KanoY.2003Effect of GA and CPPU treatments on cell size and type of sugars accumulated in Japanese pear fruitJ. Hort. Sci. Biotechnol.78331334

    • Search Google Scholar
    • Export Citation
  • KanoY.2004aEffect of mechanical restriction of fruit enlargement on cell size and sucrose accumulation in melon fruits (Cucumis melo L.)Acta Hort.662369372

    • Search Google Scholar
    • Export Citation
  • KanoY.2004bEffect of SADH treatment on cell size and kind of sugars accumulated in melon fruitsJ. Hort. Sci. Biotech.791417

  • KanoY.2005Comparison of the effects of 4-CPA and CPPU treatment on melon cell size and sugar accumulationEnviron. Control Biol.43147154

    • Search Google Scholar
    • Export Citation
  • KanoY.2006Effect of heating fruit on cell size and sugar accumulation in melon fruit (Cucumis melo L.)HortScience4114

  • LeighR.A.ApreeT.FulerW.A.BonfieldJ.1979The location of acid invertase and sucrose in vacuoles isolated from storage roots of red beet (Beta vulgaris L.)Biochem. J.1785357

    • Search Google Scholar
    • Export Citation
  • MarcanoL.CarruyoI.Del. CampoA.MontielX.2004Cytotoxicity and mode of action of maleic hydrazide in root tips of Allium cepa LEnviron. Res. Acad. Press. Orlando FL USA.94221226

    • Search Google Scholar
    • Export Citation
  • MasudaT.19706. Effects of some environments on cell division in the fruit flesh6978Studies on the development of melon fruitsKyoto UniversityKyoto, JapanPhD Diss.

    • Search Google Scholar
    • Export Citation
  • McIlrathW.J.1950Response of the cotton plant to maleic hydrazideAmer. J. Bot.37816819

  • MendhulkarV.D.2000Effect of maleic hydrazide on somatic cells and nuclear size in Triticum aestivum LinnAdvances in Plant Sciences. Acad. Plant Sci. Muzaffarnager India.13567572

    • Search Google Scholar
    • Export Citation
  • NaylorA.W.1951Accumulation of sucrose in maize following treatment with maleic hydrazideArch. Biochem. Biophys.33340342

  • Ofosu-AnimJ.YamakiS.1994Sugar content, compartmentation, and efflux in strawberry tissueJ. Amer. Soc. Hort. Sci.11910241028

  • SchroederC.A.1953Growth and development of the Fuerte avocado fruitJ. Amer. Soc. Hort. Sci.61103109

  • SeltmannH.NicholsB.C.1984Agronomic, physical and visual characteristics of hand suckered on maleic hydrazide treated flue-cured and burley tobaccosAgron. J.76375378

    • Search Google Scholar
    • Export Citation
  • SinnottE.W.1939A developmental analysis of the relation between cell size and fruit size in CucurbitsAmer. J. Bot.26179189

  • YamakiS.InoM.1992Alteration of cellular compartmentation and membrane permeability to sugars in immature and mature apple fruitJ. Amer. Soc. Hort. Sci.117951954

    • Search Google Scholar
    • Export Citation
  • ZilkahS.OsbandM.E.McCaffreyR.1981Effect of inhibitors of plant cell division on mammalian tumor cells in vitroCancer Res.4118791883

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