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Effects of Cultivar and Cropping Type on the Growth and Yield of Female and Male Asparagus Plants

Authors:
Satoru MotokiFaculty of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Kazuki OkadaGraduate School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Shumpei ImaiGraduate School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Takumi TaguchiGraduate School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Akira KannoGraduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-Ku, Sendai, Miyagi 980-8577, Japan

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Abstract

Asparagus (Asparagus officinalis L.) is a dioecious perennial plant. Male plants have a higher yield than female plants; therefore, all-male cultivars are more commonly produced. In contrast, female plants have a higher spear weight than that of male plants. To increase profitability, selective cultivation of only female plants would increase the yield of asparagus with a thick spear, which has a higher unit price. However, the effects of cultivar and cropping type on the growth and yield of male and female asparagus plants have rarely been examined. This study compared the growth and yield of female and male plants of three cultivars grown under various cropping types: a rootstock planting forcing culture; a long-term harvest production system in an open field; and a semi-forcing culture. As a measurement of growth, the rootstock weight was significantly higher for female plants compared with that of male plants with the rootstock planting forcing culture. Regarding yield measurements, the spear weight and yield were not significantly different with the rootstock planting forcing culture. However, with the long-term harvest production system in the open field and semi-forcing cultures, the weight and yield of female plants were equivalent to or significantly higher than those of male plants, regardless of the cultivar, except during some harvest periods. These results indicated that the selective production of female plants may be advantageous in terms of growing heavier spears with a higher unit price in a long-term harvest production system in the open field and semi-forcing cultures in Japan. Additionally, the development of a simple and low-cost method for sex identification would be beneficial.

In Japan, asparagus (Asparagus officinalis L.) cropping types can be divided as follows: open field culture; semi-forcing culture; and rootstock planting forcing culture (RPFC) (Motoki 2003, 2016). With open field and semi-forcing cultures, three types of cultivation exist depending on the harvest period: a conventional production system; two-season harvest production system; and long-term harvest production system (LHPS) (Motoki 2003, 2016). The conventional production system includes harvesting in spring only. With the two-season harvest production system, the harvest is stopped to establish mother ferns at some point during the spring harvest; then the appropriate number of mother ferns is established for the summer–autumn harvest. The LHPS involves harvesting continuously from spring to summer–autumn without stopping the harvest after the establishment of mother ferns. LHPS in a semi-forcing culture is a greenhouse-based cropping system in which the greenhouse is closed to keep the inside of the greenhouse warm before the spring harvest, and the window on the gable face and side ventilator of the greenhouse are opened as the outside temperature increases. Because it can be harvested 2 to 3 months earlier than that in the open field culture, and because the harvest period can be set to last longer, the yield per unit area is higher than that in the LHPS in the open field culture. Additionally, rain protection reduces stem blight caused by Phomopsis asparagi (Sacc.), which can be a problem in the open field culture. Therefore, LHPS has been introduced and intensively cultivated, mainly in warm regions of Japan (Motoki 2003, 2016). The RPFC is a cropping type developed in Japan; rootstocks are grown in open fields for 1 or 2 years and are dug up in autumn and placed in hot beds in a plastic greenhouse. Thereafter, the spears are harvested from December to March (the off-crop season of asparagus in Japan) (Koizumi et al. 2003; Motoki 2003, 2016). With RPFC, it is suitable to use cultivars with shallow dormancy and a high yield of thick spears.

Asparagus is a dioecious plant. Because male plants do not produce fruits or seedlings that could become weeds, all-male asparagus cultivars can be bred by crossing between a super male plant and female plants as parents for pollination (Sneep 1953); therefore, all-male asparagus is cultivated widely (Motoki 2016). In contrast, female plants produce fruits, which remove some nutrients from the plant. The seeds of the fruits can also fall and produce seedlings that become weeds, which can subsequently infect the culture, spread disease, and cause crop damage. However, previous studies found that spear weight is higher for female plants than for male plants (Hamasaki and Jinno 2019; Ikeuchi and Kobayakawa 1999; Koizumi et al. 2003; Robbins and Jones 1925; Uragami et al. 2016). Recently, thick spears have become valued for their size and eating quality; therefore, they are traded at a high price (Motoki 2003, 2016; Motoki et al. 2011). Therefore, cultivation of only female plants could result in a higher yield of asparagus with a thick spear, which would have a higher unit price and would, in turn, increase the profitability of asparagus farming.

Several previous studies have compared the differences between the sexes of asparagus in terms of spear weight and yield; however, few studies have made such comparisons for 1-year-old plants (Koizumi et al. 2003; Robbins and Jones 1925; Uragami et al. 2016) and for cropping types other than open field culture (Hamasaki and Jinno 2019; Ikeuchi and Kobayakawa 1999). Additionally, previous studies have mainly tested relatively older breeds of asparagus cultivars (Motoki 2016), including Mary Washington (Robbins and Jones 1925), Washington (Robbins and Jones 1925), Palometto (Robbins and Jones 1925), and UC157 (Hamasaki and Jinno 2019; Ikeuchi and Kobayakawa 1999; Koizumi et al. 2002, 2003; Uragami et al. 2016), even though new cultivars with characteristics suitable for RPFC, such as Early California and Taiho-Wase, have been bred (Motoki 2016) and are grown widely in production regions. Asparagus cultivars can be classified into diploid green asparagus and tetraploid purple asparagus (Motoki 2003, 2016). Purple asparagus is superior to green asparagus in terms of rutin, polyphenol, ascorbic acid, and sugar contents (Maeda et al. 2005; Motoki 2003, 2016). There has been an increase in the production area of purple asparagus in Japan (Motoki 2016), and the demand for purple asparagus is expected to continue to grow. However, the growth and yield differences between the sexes of new asparagus cultivars and purple asparagus have not been studied in detail; therefore, it is necessary to investigate possible strategies to improve profitability in these cases.

In the present study, sex differences in the growth and yield of 1-year-old green asparagus cultivars Early California and UC157 grown in RPFC were investigated to determine which of the cultivars is more suitable for RPFC. Additionally, using a LHPS, this study examined yield differences between the sexes of 2- to 4-year-old asparagus cultivars, specifically green asparagus UC157 and purple asparagus Pacific Purple, in open field and semi-forcing cultures to determine whether the female purple asparagus plants have advantages over the male plants in terms of profitability. UC157 is the cultivar with the largest production area in Japan (Motoki 2003, 2016); therefore, it was used as a control for each cropping type.

Materials and Methods

Sex identification of asparagus.

The sex of asparagus plants was determined according to the method of Kanno et al. (2014). Total DNA was extracted from 100 mg of cladophyll (Honda and Hirai 1990), and a polymerase chain reaction was performed using the primers MSSTS710 (Kanno et al. 2014) and Asp1-T7sp (Nakayama et al. 2006), which were used to distinguish the sex of the plants. Specifically, the sex was determined based on a male-specific amplified fragment in the polymerase chain reaction and later confirmed by examining the morphology of the flowers that bloomed after planting.

Growth and yield differences between female and male plants in RPFC (1-year-old plants).

The following experiment was conducted in an open field in Numata City, Gunma Prefecture, Japan (lat. 36°39′N, long. 139°08′E; 550 m altitude; andosols) during 2 years (based on the year of planting): in 2014 with ‘Early California’ and in 2016 with ‘Early California’ and ‘UC157’. In 2014, the seeds were sown on 5 Feb, potted on 17 Apr, and planted on 1 Jun. In 2016, the seeds were sown on 8 Jan, potted on 5 Apr, and planted on 25 Apr. In both planting years, the seeds were sown in 200-hole cell trays and potted in 9-cm polyethylene pots. Asparagus plants were planted in a single row with a ridge width of 1.4 m and planting distance of 0.4 m (17,860 plants/ha). The test area was divided into three replicates, with each containing ten plants. The ridges were formed mechanically, and their surfaces were covered with 0.02-mm-thick black plastic mulch (Mikado Kako Co., Ltd., Chiba, Japan) during the growing period. Chemical fertilizer (220N–230P–200K) was applied before planting, and supplemental fertilizer (56N–56P–56K and 68N–64K) was applied from July to September in both planting years. Other cultural practices followed the methods of Motoki (2003, 2016). The aboveground plant parts were measured on 16 Nov 2014 and 15 Nov 2016, and the effective stem number, ineffective stem number, stem diameter (mm), and stem length (cm) were measured. To measure the underground part of plants, rootstocks were dug up on 25 Nov 2014 and 22 Nov 2016, and the rootstock weight (g) and storage root Brix (°Brix) were measured; the latter was measured using a refractometer (PR–201α; ATAGO Co., Ltd., Tokyo, Japan). The dug-up rootstock was cultivated in an abandoned construction tunnel (length, ≈740 m; width, 6.9 m; and height, 5 m) in accordance with the methods of previous studies (Motoki 2003; Motoki et al. 2013). The tunnel was located in Sakaki Town, Nagano Prefecture (lat. 36°45′N, long. 138°20′E; 460 m altitude). The temperature and humidity in the tunnel were maintained at ≈16 °C ± 1 °C and 90%, respectively, throughout the year, and it was completely dark inside; therefore, asparagus were harvested as white asparagus (Fig. 1). In the experiments beginning in 2014 and 2016, yield was measured for 114 d from 13 Dec 2014 to 5 Apr 2015, and for 75 d from 7 Dec 2016 to 19 Feb 2017, respectively. Spears were divided according to the following grades: 2L = ≥28 g; L = 12 to 27 g; M = 7 to 11 g; S = 4 to 6 g; others <4 g; and malformation (Motoki et al. 2011). Malformed spears, those with disease, or those infested with insects above the ground were cut off. Harvesting was conducted two to three times per week until there were no more sprouts of spears of the M class standard (7–11 g per spear weight). The spears were cut to 25 cm, and the spear number and spear weight were determined to calculate the yield.

Fig. 1.
Fig. 1.

Test area and sprouting status of white asparagus in the rootstock planting forcing culture.

Citation: HortScience 57, 11; 10.21273/HORTSCI16786-22

Growth and yield differences between female and male plants grown using a LHPS in open field and semi-forcing cultures (2- to 4-year-old plants).

The following experiment was conducted in an open field and a plastic greenhouse at Meiji University in Kawasaki City, Kanagawa Prefecture, Japan (lat. 35°36′N, long. 139°32′E; 65 m altitude; andosols) over 4 years from 2014 to 2017. The cultivars tested were the green asparagus ‘UC157’ and purple asparagus ‘Pacific Purple’. Seeds were sown in 200-hole cell trays on 5 Feb. 2014, potted in 9-cm polyethylene pots on 17 Apr. 2014, and planted on 4 June 2014. Asparagus plants were planted in a single row with a ridge width of 1.5 m and a planting distance of 0.3 m (22,000 plants/ha). Two specific sections were defined for female and male plants, and the test area was divided into three replicates, with each containing six plants per cropping type. The ridges were formed mechanically and their surfaces were covered with 0.02-mm-thick white-on-black plastic mulch (Okura Ind. Co., Ltd., Kagawa, Japan) during the growing period of 1-year-old plants. An insect-proof net (1-mm mesh size) was placed over the opening of the plastic greenhouse to prevent the entry of pollinating insects. Chemical fertilizer (150N–150P–150K) was applied before planting the 1-year-old plants and before the sprouting of the 2- to 4-year-old plants. Harvesting began with 2-year-old plants and was conducted three times per week (Table 1). The establishment of mother ferns for sprouting was conducted such that it aligned with the end of the spring harvest of ‘UC157’, and these were harvested in the autumn when the plants no longer sprout spears. In accordance with the study of Motoki (2003), there were three to four mother ferns per plant. Malformed and diseased spears or those infested with insects above the ground were removed. The spears of ‘UC157’ were cut to 25 cm, and the number and weight of spears were measured to determine the yield. The adherence of male flowers of ‘Pacific Purple’ was confirmed during the harvest of the 2-year-old plants for some of the plants that were previously determined to be female. Therefore, replicated trials were no longer possible for this cultivar. Therefore, the spring harvest of 2-year-old ‘Pacific Purple’ was limited to those plants that were harvested until 15 May 2015. Subsequently, the diameter of the stem of each harvested stock plant was measured using digital calipers after the spring and summer–autumn harvest in each year, and the spear weight and yield were estimated using a yield estimation program (Motoki et al. 2007).

Table 1.

The harvest period of the long-term harvest production system.

Table 1.

Statistical analysis.

To evaluate the sex differences in the growth and yield, statistical software [IBM SPSS Statistics version 28.0.1.0 (142); IBM Corp., Armonk, NY, USA] was used to perform the two-way analysis of variance (ANOVA) or three-way ANOVA and the independent samples t test.

Results and Discussion

Growth and yield differences between female and male plants in RPFC (1-year-old plants).

Data of ‘Early California’ were obtained for 2 years, 2014 and 2016. However, the description was focused on the results of 2016 to evaluate the sex differences between the two cultivars (Early California and UC157). Female plants had a significantly higher rootstock weight than male plants (P = 0.009; two-way ANOVA) (Table 2), and the t test analysis showed that the stem diameter of ‘Early California’ in 2014 (P = 0.029) and the rootstock weight (P = 0.004) and storage root Brix (P = 0.015) of ‘UC157’ in 2016 were significantly higher for female plants than for male plants. Koizumi et al. (2003) and Uragami et al. (2016) also examined the growth differences between the sexes in RPFC and found that the rootstock weight of female plants was significantly higher than that of male plants by 20% and 10%, respectively. In the present study, the rootstock weight of female plants was significantly higher than that of male plants (i.e., 30% higher for ‘UC157’ and 11% higher for ‘Early California’); this finding was consistent with that of Koizumi et al. (2003) and Uragami et al. (2016). Regarding the storage root Brix, Uragami et al. (2016) found no significant difference between the sexes, whereas Koizumi et al. (2003) found that female plants had significantly (6%) higher storage root Brix than that of male plants. The storage root Brix was significantly (P = 0.015) higher in UC157 female plants than in UC157 male plants, but there was no significant difference between the sexes of ‘Early California’ (P = 0.913). This result of ‘Early California’ was consistent with the findings of Uragami et al. (2016). There was a significant difference between the cultivars in terms of rootstock weight (P = 0.012) and storage root Brix (P < 0.001), with the relative measurements of UC157 being significantly higher than those of Early California. Therefore, ‘Early California’ plants may have less underground growth compared with that of ‘UC157’ plants, even though they show equivalent aboveground growth.

Table 2.

Results of the two-way ANOVA of growth and yield using rootstock planting forcing culture.

Table 2.

There was no significant difference between the sexes in terms of any of the yield measurements (two-way ANOVA and t test) (Table 2). In contrast, Koizumi et al. (2003) found that the yield and thick spear ratio (>15 g) of ‘UC157’ were significantly higher for female plants than for male plants. They also reported that the spear of female plants had superior quality in terms of head tightness and anthocyanin production in scaly leaves, although they found no significant difference between the sexes in terms of spear number; therefore, they suggested that female plants would be more profitable than male plants. Uragami et al. (2016) reported that the rootstock weight and spear weight of female ‘UC157’ plants were significantly higher than those of male plants, whereas the number of spears was significantly higher for male plants than for female plants. In the present study, female plants had 14% and 6% higher spear weights than male ‘UC157’ and ‘Early California’ plants, respectively. The yield of male ‘UC157’ plants was 12% higher than that of female plants, whereas the yield of male ‘Early California’ plants was 2% lower than that of female plants. In 2016, male plants had more spears than female plants (26% more for ‘UC157’ and 2% more for ‘Early California’). Regarding ‘UC157’, our results were similar to those reported by Uragami et al. (2016) in terms of sex differences in rootstock weight and storage root Brix. Uragami et al. (2016) stated that the female plants used by Koizumi et al. (2003) may have had markedly higher rootstock weight and storage root Brix compared with those of male plants, indicating that the yield and spear number reported by Koizumi et al. (2003) may not be generalizable.

The rootstock weight was significantly higher for ‘UC157’ than for ‘Early California’, and it was significantly higher for female plants than for male plants; however, there was no significant difference in yield between the sexes. These results may be attributed to the differences in appropriate chilling hours between the sexes. Therefore, no apparent difference in yield emerged. Having compared the yield of female and male 2-year-old plants in terms of chilling hours, Koizumi et al. (2002) reported that the yield of female plants was higher at 600 h than at 300 h, whereas male plants showed no significant difference in yield according to chilling hours. Therefore, they concluded that female plants had higher low-temperature requirements for dormancy breaking than male plants. In the present study, both cultivars were dug up simultaneously to examine female and male plants. Therefore, the female plants with higher low-temperature requirements may have been dug up earlier than appropriate. These findings indicate that the yield of female plants is likely to be significantly higher than that of male plants in RPFC, and no apparent difference was observed because of the lack of appropriate chilling hours for female plants. Future studies should determine appropriate chilling hours for male and female plants and each cultivar.

Growth and yield differences between female and male plants using a LHPS in open field and semi-forcing culture (2- to 4-year-old plants).

The spear weight of ‘UC157’ (P < 0.001, both harvest periods) and its yield (P = 0.002, spring; P = 0.007, summer–autumn) were significantly higher for female plants than for male plants (three-way ANOVA) (Table 3). There was also a significant difference between the cropping types in terms of the spear weight of the summer–autumn harvest (P = 0.004) and the yield of the spring harvest (P < 0.001). Previous studies reported that spear weight was higher for female plants compared with male plants, regardless of cropping type and cultivar (Hamasaki and Jinno 2019; Ikeuchi and Kobayakawa 1999; Robbins and Jones 1925), which is consistent with our findings. The difference between the sexes in terms of yield is inconsistent among previous studies. For example, the yield of 1- to 2-year-old (Ikeuchi and Kobayakawa 1999) and 2- to 7-year-old (Hamasaki and Jinno 2019) ‘UC157’ cultivated in a semi-forcing culture was higher for female plants than for male plants, whereas the yield of 2-year-old ‘Mary Washington’, ‘Washington’, and ‘Palometto’ cultivated in an open field culture (Robbins and Jones 1925) was shown to be higher for male plants than for female plants. Such inconsistencies might be attributable to differences in mother fern methods, stock grade, and the individual plants tested. In the present study, each stock grade of ‘UC157’ was analyzed using a two-way ANOVA. The results showed significant differences between the sexes in terms of the yield of the 2-year-old plants (P = 0.023, spring; P = 0.004, summer–autumn) and the spring harvest of 3-year-old plants (P = 0.042); in other words, female plants had significantly higher yields than male plants (S. Motoki, unpublished data). These finding were consistent with those of Ikeuchi and Kobayakawa (1999), who tested 1- to 2-year-old plants in a semi-forcing culture. Notably, there was no significant difference between the sexes in terms of the yield after the summer–autumn harvest of 3-year-old plants (P = 0.096 0.752). Collectively, these findings indicate that the yield is higher for younger female plants, although sex differences apparently become negligible as the stock grade and other factors, such as mother fern methods and environmental effects from previous years become more prominent.

Table 3.

Results of the three-way ANOVA of spear weight and yield of ‘UC157’.

Table 3.

For ‘Pacific Purple’, there were significant differences among stock grades in terms of spear weight (P < 0.001, both harvest periods) and yield (P < 0.001, both harvest periods), as well as between cropping types in terms of spear weight (P < 0.001) and yield (P < 0.001, spring; P = 0.019, summer–autumn), except for spear weight of the spring harvest (P = 0.358) (three-way ANOVA) (Table 4). There were also significant differences between the sexes in terms of spear weight (P < 0.001, spring; P = 0.004, summer–autumn), and there were significant interactions between stock grade and sex for spear weight (P < 0.001, spring; P = 0.001, summer–autumn) and between cropping type and sex for yield (P = 0.046, spring; P = 0.023; summer–autumn). To determine sex differences, the stock grade data for spear weight and cropping type data for yield were analyzed separately. For 2-year-old plants, there was no significant difference between the sexes in terms of spear weight, except in the summer–autumn harvest in the semi-forcing culture. However, for 3- and 4-year-old plants, the sexes showed significant differences in spear weight, with female plants possessing heavier spears than male plants, except in the summer–autumn harvest in the semi-forcing culture (S. Motoki, unpublished data). In the semi-forcing culture, there was no significant difference between the sexes in terms of yield. In the open field culture, the yield of male plants was equivalent to or higher than that of female plants (S. Motoki, unpublished data). Unlike ‘UC157’, there was a significant interaction in the ANOVA for ‘Pacific Purple’, indicating that sex differences in spear weight increase with stock grade. Furthermore, our data show that sex differences in yield vary depending on the combination of cropping types. The yield of male plants is likely to be higher than that of female plants in open field cultures, but there was no significant difference in this case, except for in the summer–autumn harvest of 4-year-old plants. Therefore, the investigation of the yield of ‘Pacific Purple’ should be continued after 5 years. Our findings indicate that when using LHPS in open field culture and semi-forcing culture in Japan, the selective production of female plants may be advantageous in terms of growing heavier spears with a higher unit price (Motoki 2003, 2016; Motoki et al. 2011), which would, in turn, increase profits. Notably, purple asparagus is known to have fewer spears than green asparagus, and the yield of young purple plants is known to be substantially lower than that of green plants, even when they have the same planting density (Motoki et al. 2011). In this study, it was also observed that the yield of purple asparagus was lower than that of green asparagus; however, selective production of female purple asparagus plants may increase spear weight, thereby increasing the profitability of young plants.

Table 4.

Results of the three-way ANOVA of spear weight and yield of ‘Pacific Purple’.

Table 4.

In conclusion, our data showed that female asparagus plants had spear weights and yields that were equivalent to or significantly more than those of male ‘UC157’ and ‘Pacific Purple’ plants cultivated in LHPS in the open field and semi-forcing cultures. Notably, this trend did not apply to the spear weight of 3-year-old ‘Pacific Purple’ plants in the summer autumn harvest in a semi-forcing culture or the yield of 4-year-old plants in an open field culture. Therefore, selective production of female plants may improve the profitability when using the LHPS in the open field and semi-forcing culture, regardless of the cultivar. However, there was no significant difference in spear weight and yield between male and female plants in the RPFC, irrespective of the cultivar. These sex differences in spear weight and yield may be hindered by external factors, such as chilling hours in RPFC, plant age, mother fern methods, and environmental effects from previous years on LHPS. Future studies should evaluate whether such external factors affect the genetic factors that regulate the sex differences in terms of growth and yield of asparagus plants. It should also be noted that the sex identification process for plants is time-consuming and can be costly because it involves DNA extraction and polymerase chain reaction analysis. Although the development of simpler sex identification methods is ongoing (Ii et al. 2012), the cost of such methods must be considered when determining the cost-effectiveness of female plant production for each cropping type, cultivar, and region. The development of a simple and low-cost method for sex identification would be beneficial.

References

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    Fig. 1.

    Test area and sprouting status of white asparagus in the rootstock planting forcing culture.

  • Hamasaki, K. & Jinno, N. 2019 Differences between male and female plant in semi-forcing green asparagus cultivation Nagasaki Agric For Tech Dev Ctr. 9 21 27

    • Search Google Scholar
    • Export Citation
  • Honda, H. & Hirai, A. 1990 A simple and efficient method for identification of hybrids using nonradioactive rDNA as probe Jpn J Breed. 40 3 339 348 https://doi.org/10.1270/jsbbs1951. 40.339

    • Search Google Scholar
    • Export Citation
  • Ii, Y., Uno, Y., Kanechi, M. & Inagaki, N. 2012 Screening of sex in asparagus at early growth stages HortTechnology 22 1 77 82 https://doi.org/10.21273/HORTTECH.22.1.77

    • Search Google Scholar
    • Export Citation
  • Ikeuchi, T. & Kobayakawa, H. 1999 Study on half-forcing long-term crop cultivation of asparagus characteristics of female and male plants Bull Kagawa Agric Expt Sta. 51 27 32

    • Search Google Scholar
    • Export Citation
  • Kanno, A., Kubota, S. & Ishino, K. 2014 Conversion of a male-specific RAPD marker into an STS marker in Asparagus officinalis L Euphytica 197 39 46 https://doi.org/10.1007/s10681-013-1048-2

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Satoru MotokiFaculty of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Kazuki OkadaGraduate School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Shumpei ImaiGraduate School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Takumi TaguchiGraduate School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

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Akira KannoGraduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-Ku, Sendai, Miyagi 980-8577, Japan

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Contributor Notes

S.M. is the corresponding author. E-mail: motoki@meiji.ac.jp.

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