Impact of Secondary-lateral Branch Removal during Watermelon Production
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1 Hort. Environ. Biotechnol. 53(1): DOI /s Research Report ISSN (print) : ISSN (online) : Impact of Secondary-lateral Branch Removal during Watermelon Production Eun-Young Choi 1, Il-Hwan Cho 2, Ji-Hye Moon 2, and Young-Hoe Woo 3* 1 Department of Horticulture, KonKuk University, Chungju , Korea 2 Division of Horticultural Science, National Institute of Horticultural & Herbal Science, Suwon , Korea 3 Department of Vegetable, Korea National College of Agriculture and Fisheries, Hwaseong , Korea *Corresponding author: wooyh612@korea.kr Received December 13, 2011 / Revised January 13, 2012 / Accepted January 19, 2012 Korean Society for Horticultural Science and Springer 2012 Abstract. The cultural practice of removal of the secondary-lateral branch of watermelon during the production in greenhouse requires intensive input of human labor. Secondary-lateral branch removal practices were examined in horizontally trained two watermelon cultivars (Citrullus lanatus), Sambock-gul and Speed-honey to determine the comparative differences in labor input as well as to understand their impact on plant and fruit growth and fruit sugar accumulation. Two experiments were conducted. Experiment 1 consisted of two treatments for plants trained with one main stem and two lateral branches: removal of the entire secondary-lateral branch or removal of the secondary-lateral branch below the fruit set node (partial removal). Experiment 2 consisted of three treatments for plants trained with either two or three lateral branches after topping the main stem: removal of the entire secondary-lateral branch, removal of the secondary-lateral branch below fruit set node, or removal of the secondary-lateral branch below the 5th node above fruit set node. Results showed that removal of the secondary-lateral branch below the fruit set node lowered human labor input by 50% compared with removal of the entire secondary-lateral branch. Additionally, some physiological benefits were also found for the plant treated by partial removal of the secondary-lateral branch. While fruit growth rate and fruit sucrose accumulation were much slower than those under other treatments until 3 weeks after pollination, 4 weeks after pollination sucrose accumulation started to increase steeply, and reached the highest concentration observed, 18.2 mg ml -1. A greater increase in the length of fine roots, 0.2 mm in diameter, was observed under the partial removal treatment than for the entire removal treatment. During the fruit ripening period, the younger and developing leaves on secondary-lateral branches had a higher growth rate and higher photosynthetic activity than those of leaves on lateral branches. The integrated data indicate that active leaves on the secondary-lateral branch are likely to compete with the fruit as a sink during the fruit growing period, leading to slow fruit growth. However, during fruit ripening, the leaves on the secondary-lateral branch are likely to become a supportive source of carbon, leading to enhancement of sucrose accumulation in fruit. Additional key words: Citrullus lanatus, leaf area, root morphology, sucrose accumulation Introduction The cultural practice of removal of the secondary-lateral branch in watermelon production is used to increase marketable fruit production by reducing wilt symptoms (Chang et al., 2004), as well as to optimize assimilate translocation to fruits, which are active sinks (Kato et al., 1984). Some research has shown a close relationship between source biomass (i.e. leaves) and fruit yield. Ramirez et al. (1988) reported that a greater level of leaf removal significantly affected pickle cucumber yield, while increased leaf number had a positive effect on the fruit growth of watermelon (Kato et al., 1984). A lower source-sink ratio also stimulates development of larger tomato fruits (Heuvelink and Buiskool, 1995). In addition to yield changes, the translocation pattern of assimilate has been shown to differ depending on the source. Leaves close to the fruit bearing node are the most important source of assimilates for cucumber fruit (Murakami et al., 1982) and watermelon fruit (Lee et al., 2005). Alteration in source availability from early growth stages may result in change in the number of fruit set and biomass per fruit, with no change in the sugar content (Hubbard et al., 1990). However, Hubbard and his colleagues reported that when 50% of plant leaves were removed 28 days before harvest, a significant reduction in the soluble solid content of fruit was
2 Hort. Environ. Biotechnol. 53(1): observed. While a large amount of reference material is available on source-sink relationships and sugar accumulation, there is little information on the human labor expenditure for the practice of secondary-lateral branch removal. In addition, there is a lack of studies exploring interactions between secondary-lateral branch removal and fruit sugar accumulation for watermelon production. The aim of the current study, therefore, was to examine secondary-lateral branch removal practices in horizontally trained watermelon, to determine differences in human labor input and to understand their impacts on plant and fruit growth and fruit sugar accumulation. Materials and Methods Experiment 1 Watermelon seeds (Citrullus lanatus), Speed-honey (Nong Woo Bio Co., Seoul Korea) were sown on the 25 th of January, and seedlings were grafted onto the rootstock of FR Chambak (Lagenaria siceraria S., Seminis Korea Co., Seoul Korea) 10 days later. On 4 th March, 2011, seedlings were transplanted in two furrows mulched with polyethylenefilm. The plants were spaced at 500-mm intervals in a naturally ventilated greenhouse (480 m 2, W 6 m L 80 m) with a height of 2.2 m located in Uiryeong, Gyeongnam (lat N, long E). Plants were transplanted into field soil inside PVC containers, 70 cm in diameter and 30 cm in depth that were placed into the soil to separate roots from the soil. Roots obtained from the container grown plants were washed by hand and were kept in a refrigerator in a 50% of diluted ethanol solution until the measurement of surface area, volume, diameter, or length of roots by a flat-bed root scanner. Two tunnels of approximately 2.4 m in width were built inside the greenhouse. The tunnels were covered at night with a single-layer polyethylene film and multifold thermal covers consisting of 1 layer of cashmere, 4 layers of polyfoam (1 mm deep), 2 layers of nonwoven fabrics, and 1 layer of polypropylene. Maximum air temperature and root zone temperature were maintained at 38 and 25, respectively, during daytime from 10 a.m. to 16 p.m. with the average daily temperature at 30 and 23, respectively. Water was applied by an irrigation hose, depending on soil moisture and weather conditions. Plants at a six-true leaf stage were pinched to produce two lateral branches on each plant, and all secondary-lateral branches were removed until fruit was set on the third female flower. The third female flower was produced on the 18th node were bee pollinated on 3 rd of April. Only one pollinated flower was left on each branch. Composts (about 2,500 kg) and nutrients (N:P:K, 6:5:5 kg) were applied to 1,000 m 2 of the field and container soils as a basal fertilizer. Additional nutrients (N:K, 8:5 kg) were also applied to 1,000 m 2 as a supplemental fertilizer. The two fertilizers were divided into two applications each. Experiment 2 Seeds of watermelon cultivar (Citrullus lanatus) Sambok-gul (Seminis Korea, Co., Seoul Korea) were sown on the 21 th of March, and the seedlings were grafted onto rootstock of Daeryeok No. 3 (Lagenaria siceraria S., Dongbu Hannong, Co., Seoul, Korea). On the 29th of April 2011, 249 grafted seedlings were transplanted in each of two furrowsmulched with polyethylene film. The plants were spaced at 350 mm intervals in a greenhouse (585 m 2, W 6.5 m L 95 m) with a height of 2.5 m located in Jincheon, Chungbuk (lat N, long E). An overhead sprinkle irrigation system was used for irrigation. Plant training and pollination methods used in experiment 2 were the same as that in experiment 1, except for the following. Plants at a six true leaf stage were pinched to produce either two or three secondary-lateral branches on each plant. Soil fertilization was exactly the same as the experiment 1 with clay soil containing the following nutritional composition: NO 3 -N (353 mg kg -1 ), NH 4 -N (16.45 mg kg -1 ), P 2 O 5 (1152 mg kg -1 ), K (3.27 cmol kg -1 ), Ca (12.6 cmol kg -1 ), Mg (6.59 cmol kg -1 ), organic matter (5.8%), ph (6.8) and EC (7.0 ds m -1 ). Greenhouse environmental conditions were recorded every 30 mins using ALMEMO datalogger. During daytime to nighttime, temperature ranged from 19 to 42 with the average daily temperature at 27, relative humidity from 45 to 100%, CO 2 concentration from 350 to 720 µmol mol -1 and photosynthetically active radiation (PAR) from 0 to 700 µm m -2 s -1 (data not shown). Human labor input was calculated in Uiryeong region, Gyeongnam province (lat N, long E). Data were collected in experiment 1 from January to May of 2011 as well as survey results from other farms collected by Uiryeong Agricultural Development & Technology Center. Experiment 1 consisted of two treatments for the plants trained with one main stem and two lateral branches; removal of entire secondary-lateral branch and removal of secondary-lateral branch below fruit set node (Table 1 and Fig. 1). Experiment 2 consisted of three treatments for the plants trained with either two or three lateral branches; removal of entire secondary-lateral branch, removal of secondary-lateral branch below fruit set node, removal of secondary-lateral branch below the 5th node above fruit set node.
3 26 Eun-Young Choi, Il-Hwan Cho, Ji-Hye Moon, and Young-Hoe Woo Table 1. Summary of treatments for secondary-lateral branch removal applied in horizontally trained watermelon. Fig. 1. Watermelon plants showing the secondary-lateral branch removal applied in horizontally trained watermelon grown at greenhouses in Uiryeong (C and C-I) and in Jincheon (2C, 2C-I, 2C-II, and 3C-II). Fruits, 5 to 10 g were sampled from the center flesh of the fruit into test tubes and kept on dry ice during the sampling in the field. The samples were then stored at -20 for water soluble carbohydrates. Squeezed fruit juice (8 ml) was centrifuged (15000 rpm) for 15 mins at 2. The supernatants were transferred to a new tube and kept on ice prior to filtration through a 0.45 m nylon filter (Watman, USA). Sugars were separated in an analytical HPLC system (Ultimate 3000, Dionex, Sunnyvale, CA, USA).
4 Hort. Environ. Biotechnol. 53(1): Four fruits from each treatment were randomly chosen to determine the fruit weight and soluble solid content. The selected fruits were sliced, and rinds and seeds were removed. Juice was extracted from each fruit, and soluble solids concentration was determined at 20 using Atago ACT-1 refractometer (Atago Co. Ltd, Tokyo, Japan). Leaf photosynthesis was measured with an open infrared gas analyzer (model 6400, LI-COR Biosciences, Lincoln, Nebraska, USA) equipped with a 250 mm 3 leaf chamber. A red-blue LED (light emitting diode) light source ( B Red/Blue LED) was used to provide 1500 µmol m -2 s -1 of photosynthetically active radiation (PAR). Measurements were conducted at 20 with natural CO 2 condition. Thus, the CO 2 efflux rate could be determined in the light (Rl) and in the dark (i.e., dark respiration rate, Rd). The CO 2 efflux was measured 5 to 10 times at 30 s intervals. Measurement was repeated 3 times on four leaves randomly selected from 3 individual plants of each treatment. RGR is calculated using the following equation: RGR = (ln W2 - ln W1)/(t2-t1). Where, ln is natural logarithm, t1 and t2 are time one (in days) and two (in days), and W1 and W2 are dry weight of plant at time one (in grams) and at time two (in grams), respectively. Root morphological traits, including root length and diameter, were measured using the WinRHIZO Image Analysis system (Reagent Instruments Inc., Canada) (Choi et al., 2006). The entire root system was placed into the WinRHIZO root positioning system ( mm tray) filled with distilled water. Roots were carefully cut out along the main axis and spread out evenly to minimize overlapping prior to the analysis. Data were represented with mean values of 3 replications, and were subjected to analysis of variance using the SAS 9.1 statistical package. Significant mean separation was done by Duncan s multiple range test. Results Input of Human Labor Removal of the entire secondary-lateral branch (C) was more labor intensive than the removal of the secondarylateral branch below the fruit set node (C-I). The labor input for the C-I treatment was half that required for the C treatment (Table 2): the C treatment required a total of 48 h input of human labor per 1000 m 2, in comparison with a total of 24 h input required for the C-I treatment. Plant Growth Considerable compensatory leaf growth was induced by the C treatment, in which the areas of leaves on the two lateral branches and main stem were higher by 33% (P < 0.05), compared to those in the C-I treatment (Table 3). In Table 2. Amount of human labor input (days and hours per 1000 m 2 ). Table 3. Total leaf fresh weight, total leaf number, total areas of leaves on main stem and lateral branches (LALB), total areas of leaves on secondary-lateral branches (LASLB), fresh fruit weight and soluble solid content (SSC) measured at 5 weeks after pollination as affected by different branch-training methods.
5 28 Eun-Young Choi, Il-Hwan Cho, Ji-Hye Moon, and Young-Hoe Woo Fig. 2. Changes in total root length and average root diameter (A) and propotional root length in diameter between 0 and 0.2 mm of total root length (B) in watermelon plant as affected by different branch-training methods. Values represent mean values of four samples for treatment. Bars represent standard errors of four replications. Fig. 3. Change in fruit weight after pollination as affected by different branch-training methods. Values represent mean values of four samples for treatment. Bars represent standard errors of four replications. Fig. 4. Relationship between the LASLB: LALB ratio and fruit fresh weight. Observations were made at 2, 3, 4, and 5 weeks after pollination. Data presented in each week were collected from four treatments (2C, 2C-I, 2C-II, and 3C-II). contrast, the application of the C-I treatment significantly (P < 0.05) resulted in significantly higher total leaf number, compared to those in the C treatment. Removal of the secondary-lateral branch below the fruit node (C-I) had no significant effect on fruit weight, whereas soluble sugar content in the fruit increased by 6.3% (P < 0.05) compared to the C treatment. Removal of the entire secondary-lateral branch (C) was associated with a 123% decrease in total root length (P < 0.05) compared to that of secondary-lateral branch removal below the fruit set node (C-I) (Fig. 2). Thinner root diameter at 5 weeks after fruit set in the C-I treatment was associated with increase in root length less than 0.2 mm in diameter by 37.3%. Plant Growth Removal of entire secondary-lateral branches (2C) (Fig. 3 and Table 5) resulted in a rapid rate of fruit growth from 2 to 3 weeks after pollination, whereas partial removal of the secondary-lateral branch (2C-I) caused a steadier fruit growth rate from 2 to 3 weeks after pollination. By 5 weeks after pollination, however, there was no significant difference between fruit weight for all the treatments (Fig. 3). In the 2C-I treatment, the total areas of leaves on the secondarylateral branch (LASLB) per fruit weight was about 4-fold higher (P < 0.05) at 2 weeks after pollination than for other treatments (Table 4). In contrast, the total areas of leaves on the lateral branch (LALB) per fruit weight in the 2C-I treatment was significantly lower (P < 0.05) 2 weeks after pollination than for other treatments. There was a negative relationship between LASLB: LALB ratio and fruit fresh weight 2 to 4 weeks after pollination (Fig. 4). The correlation coefficients (r 2 ) were 0.45, 0.60, and 0.33 at 2, 3, and 4 weeks after pollination, respectively. The relative growth rate of single leaves borne on the lateral branch or secondarylateral branch was not affected by the treatments when measured between 2 and 3 weeks after treatment. However, the relative growth rate of leaves borne on the secondarylateral branch was 2-fold higher, at about cm 2 day -1 (P < 0.05), than that of leaves borne on the lateral branch, regardless of the treatments (Table 5).
6 Hort. Environ. Biotechnol. 53(1): Table 4. Areas of leaves on lateral branch (LALB) and secondary-lateral branch (LASLB) per weight fresh fruit (fruit fresh wt.). Table 5. Relative growth rate of area of single leaf on lateral- and secondary-lateral branch single leaf area (MBLA RGR and SBLA RGR) and fresh fruit weight (fruit RGR) as affected by different branch-training methods. Table 6. Photosynthesis and gas exchange activity in the leaves born on the 5th node above fruit set in lateral branch and leaves born on secondary-lateral branches above fruit set grown under the 2C-1 treatment at 5 weeks after pollination. Photosynthesis Photosynthetic activity, stomatal conductivity and transpiration rate of leaves borne on the secondary-lateral branch in the 2C-1 treatment were significantly higher, at around 24, 32, and 27% (P < 0.05), respectively, than that of the leaves borne on the lateral branch, when measured at 5 weeks after pollination (Table 6). Sugar Accumulation in Fruit Removal of the secondary-lateral branch was found to significantly influence fruit sugar accumulation. Sucrose accumulation in fruit started from 3 weeks after pollination and accumulation of glucose and fructose was evident from 2 weeks after pollination, regardless of treatments (Table 7). The sucrose concentration reached about mg ml -1,
7 30 Eun-Young Choi, Il-Hwan Cho, Ji-Hye Moon, and Young-Hoe Woo Table 7. Sugar accumulation in fresh fruit as affected by different branch-training methods in Experiment 2. Fruits were collected at 2, 3, 4, and 5 weeks after pollination. while the final concentrations of glucose and fructose were 30 and 60 mg ml -1, respectively. Sucrose constituted 15-19% of fruit sugar, while glucose and fructose were in the ranges of 25-48% and 50-60%, respectively (data not shown). These proportions were not affected by the treatments. With partial removal of the secondary-lateral branch (2C-I), sucrose accumulation in the fruit started to increase more steeply from 3 to 4 weeks after pollination than for other treatments. At 5 weeks after pollination, the concentration of sucrose in fruit grown under the 2C-1 treatment was highest, at 18.2 mg ml -1 (P < 0.005), compared to all the treatments. Unlike sucrose, the levels of glucose and fructose in the fruit grown under the 2C-1 treatment remained steady. At 5 weeks after pollination, the fruit grown under the 2C treatment had lower concentrations of glucose and fructose than those of other treatments. Discussion Results from the present study have shown that removal of the entire secondary-lateral branch was more labor intensive than that of removal of the secondary-lateral branch below the fruit set node. In Experiment 1, the labor input for the C-1 treatment was 50% of that required for entire removal of the secondary-lateral branch (C treatment) (Table 2). According to the 2008 Agricultural earning data (RDA, 2009), individual cultivation of 1000 m 2 of watermelon per year in South Korea requires a total of 165 h of human labor input, of which part-time labor is used for about 36.6 hours (12.5%) and operator labor is used for about hours (41.5%). In addition to labor saving benefits, several physiological advantages were associated with partial branch removal treatment. Secondary-lateral branch removal below the fruit node (C-I) had higher total leaf numbers, total leaf areas, growth of roots finer than 0.2 mm in diameter (P < 0.05), and soluble sugar content in the fruit (Fig. 2), compared with the C treatment. However, there were no significant differences in the total leaf weight and fruit weight between the two treatments (C and C-I). The increase in fine root growth and soluble sugar content for the C-I treatment may indicate enhancement of assimilate partitioning toward the fruit and roots that appears to be related to higher leaf number and area. A previous study reported that pinching lateral vines below the fruit bearing node induced higher sugar content in fruit than either pinching lateral vines above the bearing node, or pinching all lateral vines (Kato et al., 1984). In general, the growth of a root system depends on metabolic utilization of sucrose, the main carbon and energy source in root metabolism (Gasparikova, 1992). Leaves provide the source substrate (e.g. sucrose) for storage root enlargement (Loomis and Torrey, 1964). Overall, applying the cultural practice of partial branch removal can contribute to a farmer s income by reducing labor costs and improving fruit quality without compromising fruit yield. In Experiment 2, some implications of secondary-lateral
8 Hort. Environ. Biotechnol. 53(1): branch removal were explored further. Partial removal of the secondary-lateral branch (2C-1) caused much steadier fruit growth rate; that is, the greater the area of leaves on the secondary-lateral branch, the slower the observed fruit growth (Table 4). However, at 5 weeks after pollination, there was no significant difference in fruit weight for any of the treatments. As shown in Experiment 1, none of the treatments affected final fruit yield. Applying the 2C-1 treatment sharply increased fruit sucrose accumulation starting 3 to 4 weeks after pollination compared with other treatments (Table 7). This may correspond to an enhancement in photosynthetic activity due to the leaves on the secondary-lateral branch, although carbohydrate accumulation in the leaves was not measured in the present study. It is known that the photosynthetic efficiency of leaves is greater in the middle or upper leaves than for lower leaves on the watermelon vine (Okano et al., 1998). In addition, the leaves borne on the secondary-lateral branch leaves had a much higher growth rate than those on the lateral branch (Table 5). Sucrose accumulation in fruit started from 3 weeks after pollination, while the accumulation of glucose and fructose was evident from 2 weeks after pollination. These results are the same as previously reported by others (Brown and Summers, 1985; Elmstrom and Davis, 1981). While sucrose accumulation in fruit grown under the 2C-1 treatment started to increase steeply from 3 to 4 weeks after pollination, levels of glucose and fructose remained steady. This result suggests that the accumulated sucrose was not synthesized from glucose and fructose available in the fruit, since they remained constant (Chrost and Schmitz, 1996; Hubbard et al., 1989; McCollum et al., 1988). Interestingly, the concentrations of glucose and fructose in the fruit grown under the 2C treatment were lower than for other treatments. Taken together, the data indicate that, during fruit development, the active leaves on the secondarylateral branch are likely to be a competing sink with fruit and lead to slower fruit growth. However, over the fruit ripening period, the leaves on the secondary-lateral branch are likely to be a supportive source, leading to enhancement of sucrose accumulation in fruit. The functional transition, either from sink to source of carbon, or from source to sink, between older and younger leaves may impact on the availability of carbohydrates for fruit development and quality, as demonstrated by studies involving radioactive labeling and removal of secondary shoots (Candolfi-Vasconcelos and Koblet, 1990). More detailed investigations are being conducted on the contribution of leaves on the secondary-lateral branches to total sucrose production, and their role as a source of assimilates for sink tissues (i.e. root and fruit). Literature Cited Brown, A.C. and W.L. Summers Carbohydrate accumulation and color development in watermelon. J. Amer. Soc. Hort. Sci. 110: Candolfi-Vasconcelos, M.C. and W. Koblet Yield, fruit quality, bud fertility and starch reserves of the wood as function of leaf removal in Vitis vinifera Evidence of compensation and stress recovering. Vitis 29: Chrost, B. and K. Schmitz Changes in soluble sugar and activity of -galatosidases and acid invertase during muskmelon (Cucumis melo L.) fruit development. J. Plant Physiol. 151: Chang, Y.H., J.S. Shim, C.W. Ro, J.M. Lim, and J.L. Cho Effects of eliminating method of lateral branch on fruit characteristics and wilting symptom of watermelon in protected cultivation. Kor. J. Hort. Sci. Technol. 22:35. Choi, E.Y., A.M. McNeill, D. Coventry, and J.C.R. Stangoulis Whole plant response of crop and weed species to high subsoil boron. Aust. J. Agri. Res. 57: Elmstrom, G.W. and P.L. Davis Sugars in developing and mature fruits of several watermelon cultivars. J. Amer. Soc. Hort. Sci. 106: Gasparikova, O Root metabolism, p In: J. Kolek and V. Kozinka (eds.). Physiology of the plant root system. Kluwer Academic Publishers, Dordrecht, Boston, and London. Heuvelink, E. and R.P.M. Buiskool Influence of sink-source interaction on dry matter production in tomato. Ann. Bot. 75: Hubbard, N.L., S.C. Huber, and D.M. Pharr Sucrose phosphate synthase and acid invertase as determinations of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits. Plant Physiol. 91: Hubbard, N.L., D.M. Pharr, and S.C. Huber Sucrose metabolism in ripening muskmelon fruit as affected by leaf area. J. Amer. Soc. Hort. Sci. 115: Kato, T., Y. Fukumoto, and S. Kinoshita Effect of training, pinching and defoliation on the development and quality of fruit in watermelon [Citrullus lanatus]. Res. Rpt. Kochi Univ. Agr. Sic. 33: Rural Development Administration (RDA) Korean Agricultural Earning Data. RDA, Suwon, Korea. Lee, S.G., K.D. Ko, and C.W. Lee Interaction of source-sink relationship for translocation and distribution of C14 carbohydrates in watermelon (Citrullus vulgaris). J. Kor. Soc. Hort. Sci. 46: Loomis R.S. and J.G. Torrey Chemical control of vascular cambium initiation in isolated radish roots. Proc. Natl. Acad. Sci. U.S.A. 52:3-11. McCollum, T.G., D.J. Huber, and D.J. Cantliffe Soluble sugar accumulation and activity of related enzymes during muskmelon fruit development. J. Amer. Soc. Hort. Sci. 113: Murakami, T., M. Inayama, and K.S. Kobayashi Translocation and distribution of photoassimilates and relation of set fruit in cucumber. Natl. Inst. Agr. Sci. Rpt. D33: Okano, K., S. Watanabe, and Y. Sakamoto Field measurement of leaf photosynthesis in watermelon by a portable photosynthesis system. J. Japan. Soc. Hort. Sci. 67(Suppl.):156. Ramirez, D.R., T.C. Wehner, and C.H. Miller Source limitation by defoliation and its effect on dry matter production and yield of cucumber. HortScience 23:
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