Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123 AENSI Journals

Advances in Environmental Biology

ISSN-1995-0756 EISSN-1998-1066

Journal home page: http://www.aensiweb.com/AEB/

Causes and Prevention of Fruit Drop of Samarangense (Wax Apple): A Review

1Mohammad Moneruzzaman Khandaker, 1Nuruljannah Suhaida Idris, 1Siti Zuriani Ismail, 2Ali Majrashi, 3Abdullah Alebedi and 1Nashriyah Mat

1School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, University of Sultan Zainal Abidin, Besut Campus, 22200 Besut, Terengganu, Malaysia. 2Taif University, Department of Biological Sciences, Taif, Saudi Arabia KSA 3Department of Production, Colleges of Food and Agriculture Sciences, King Saud University, KSA

Address For Correspondence: Mohammad Moneruzzaman Khandaker, School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, University of Sultan Zainal Abidin, Tembila Campus, 22200 Besut, Terengganu, Malaysia.

This work is licensed under the Creative Commons Attribution International License (CC BY). http://creativecommons.org/licenses/by/4.0/

Received 23 August 2016; Accepted 1 November 2016; Published 20 November 2016

ABSTRACT Background: There is increasing concern about the fruit growth, development and quality of wax apple(Syzygium samarangense), a widely cultivated fruit tree in South East Asia. The growth and development of this fruit sometimes very low due low photosynthates supply and unfavourable growing conditions. Premature bud and fruit drop is a serious problem in wax apple production and quality. Growth regulators, hydrogen peroxide and phloemic stress are important tools to improve the quality and reduced the preharvest fruit dropof wax apple. Objectives:To investigate the causes and remedies of premature fruit drop of wax apple and the findings of this study will help to increase the fruit yield by reducing the bud and premature fruit abscission.Results:It was observed that plant growth regulators, hydrogen peroxide and phloemic stress improved the fruit retention and improved the quality of fruits.GA3 50 and 20 mg/L treatment during flowering reduced the bud and fruit drop of wax apple.Synthetic auxin (2,4-D and NAA) at 5 mg/L treatment during the flowering also reduced the fruit drop and enhanced the quality.C and V-shaped girdling 3 weeks before flowering increased number of flowers and reduced the premature fruit drop of wax apple fruits.Conclusion:This review also concluded that hydrogen peroxide treatment at flowering and fruit formation stage reduced bud and fruit drop and improve the fruit qaultiy of wax apple. The findings of the review have significant effect to reduce preharvest fruit drop and develop wax apple fruit industries in tropical climates.

KEYWORDS: Bud drop, fruit drop, cause, remedy, wax apple

INTRODUCTION

The wax apple is botanically identified as Syzygium samarangense [1]. It is a nonclimacteric tropical fruit from the family withthe pear-shaped fruits, usually pink, light red or red, sometimes greenish-white or cream-coloured, often crisp, with a subtle sweet taste and an aromatic flavour. Wax apple is widely cultivated throughout Malaysia, mainly as smallholdings ranging from 1 to 5 ha, with a total hectarage estimated at 1500 ha in 2005 [2]. In Malaysia, fruit production is non seasonal and almost all of the fruit is edible. The fruit pulp is a rich source of phenolics, flavonoids and several antioxidant compounds and as a result it is believed to have great potential benefits for human health[3]. It has become an increasingly popular fruit in the tropical region where it can fetch a price of up to 3USD per kilogramme and has the potential to bring great benefits to local farmers and the country’s economy. However, severe fruit drop (Figure 1) and low quality impair wax apple production, resulting in lower market prices.

Copyright © 2016 by authors and American-Eurasian Network for Scientific Information (AENSI Publication). 113 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

During the early growth stages, excessive fruit drop is caused by cultural and environmental factors that affect pollination, flower fertilization and fruit set. Unhealthy foliage and fruit damaged by diseases, insects and abotic factors also can result in early fruit drop. Most of the premature fruit drop is normally heavier on young trees especially if they are extremely vigorous. There is not much else a grower can do to reduce fruit drop other than trying to keep the trees in a good state of vigor and avoid moving through the orchard with equipment and sprayers that can knock off loose fruit. Plant growth regulators application and girdling have significant effect on flowering and fruit quality improvement. Girdling consists of removal of a strip of bark from the trunk or major limbs of a fruit tree, thereby blocking the downward translocation of photosynthates and metabolites through the phloem. Hydrogen peroxide can be used as a messenger molecule involved in adaptive signaling, triggering tolerance against various environmental stresses[4]. It has been shown that application of hydrogen peroxide enhanced fruit growth, development and quality of wax apple fruits [5]. Plant growth regulators such as GA3 and auxins having the ability to increase cell enlargement, thus enhancing fruit growth in wax apple[6]. The that were treated with GA3 usually can increase fruit firmness, colour, yield, and soluble solid content [7]. Recently, it has been reported that application of NAA and GA3 on wax apple showed positive effect of fruit development, reduced fruit drop as well as fruit crack and improved fruit quality of wax apple [8]. The major problems faced by production of wax apple regarding premature fruit drop will be analyse and try to find the prevention method for the problem arised. Therefore, the aim of this review is to provide a detail discussion on the causes and prevention of premature fruit drop of wax apple. Hence, the information can assist to develop wax apple as well as other tropical fruits industry in Malaysia.

Mechanism Of Fruit Drop: Fruit drop may divided into three major periods of time which are post bloom drops, june drops and pre- harvest drops. Some fruits have two additional periods of drops which are summer drop and summer-fall drop. Generally, fruit drop is the detachment or separation of a fruit from the pedicel of a branch of tree or a plant, caused by the formation of a abscission layer of cells on the fruit stalk due to a series of physiological and biochemical events. Abscission is a physiologically determined program of cell separation, provides a mechanism whereby every discrete, multicellular plant organ, such as , flowers or fruits, becomes detached from the plant body in a controlled manner. It can be initiated in response to environment events such as disease or pathogens, or programmed shedding of organs that no longer provide essential function to the plant, exemplified by the flower after aiding in pollination. Figure 1 showed the mechanism of fruit abscission.

Fig. 1: Fruit abscission mechanism [9].

114 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

Causes of Fruit Drop: The unexpected fruit drop just prior to harvest is a serious threat for some varieties of wax apple. As the fruits begin to ripen, they produce large amounts of ethylene, the ripening hormone. Ethylene stimulates softening of fruits and the formation of an abscission layer in the stem. Ethylene enhances the production of enzymes that break down the cell walls and the complex sugars that hold cell walls together in the abscission zone of the stem. As these glue-like substances break down, they leave the fruit connected only by the vascular strands, which are easily broken.Fruit drop also depends on varitey and of the plant [10]. The severity of pre-harvest drop is related to several orchard and climatic factors including pollination and fertilization, soil fertility and nutrient status, growing season temperature and water availability, heavy raining before fruit harvesting, and insect infestation or disease severity (Figure 2).

Fig. 2: Severe fruit drop in wax apple under tropical climate.

Pollination and fertilization: The understanding of wax apple flowering in the tropics and subtropics is essential to efficiently utilize crop management systems which extend both flowering and crop production season. Flowering and fruit set are the most critical events after establishing a tree crop. In nature, wax apple tree produce large number of flowers of which only a small proportion set fruit. Lack of pollination and fertilization a lot of flowers are drop after full blooming.

Soil fertility and nutrient status: Wax apple varieties that are grown in coastal area with mild alkaline and clayey soil usually get high quality fruits tht contain dark red skin and higher TSS [11]. It has been reported that soil and growing media affet the plant physiological activitity anf plant production [12]. Pre-harvest fruit drop is frequently more severe in orchards with highly saline. Due to high external osmotic pressure, the roots of wax apples growing in saline soil have difficulty in absorbing sufficient moisture and also tend to absorb large quantities of sodium, calcium and magnesium salts. It has been reported that improper nutrient balance also cause fruit cracking thus enhance fruit drop. As a result, the fruit is very small and prematurely dropped before harvest (Figure 3).

115 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

Fig. 3: Improper nutrient balance causes premature fruit drop.

Growing season, temperature and water availability: Wax apple is a tropical fruit tree speies and the optimum temperature for its proper growth is 25 – 30 oC. The cool temperature enhances total soluble solids (TSS) and skin anthocyanin accumulation in fruits and abundant water supply is required for successful wax apple cultivation[11]. The lack of water has a negative effect on cell turgor and cell protein content [13].The high temperature and water stress during the fruit development and ripening increased premature fruit [14].

Heavy raining before fruit harvesting: Earlier period of wax apple production was confined to May – July, but after the development of atechnique for adusting the production period by Wang et al. [15], it advanced to December – April. Sometimes there are favourable weather conditions as a result of which there is good fruiting which results in huge production and improved fruit quality. If the production period is adjusted to avoid December – April period, typhoon, heavy rains and chilling injury become important factors affecting production as well as premature fruit drop (Figure 4) [16]. Frequent typhoon and heavy rains in summer and autumn affected the stability of harvest and hence, the cultivated area gradually started shrinking. Heavy rain harvesting also increaed the infestation of fungus thus enhanced the fruit drop[17].

Fig. 4: Fruit drop of wax apple due to heavy rain and fungus infestation.

Infestation by insect, mites and diseases: Heavy infestations of mites, tentiform miners and fruit fly or other insects and diseases can increased the pre-harvest drop severity in wax apple fruits (Figure 5). Severe mite and lentiform leaf miner infestations have been shown to reduce photosynthatic capacity of leaves resulting in a limitation of supply to fruits late in the season [11].

116 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

Fig. 5: Insect infestation cause fruit drop in wax apple.

Preventions of Fruit Drop: The problem of fruit drop is a big issue in wax apple fruit. Chen et al. [18] stated the formation of abscission layer at the stem point lead to fruit drop from unbalanced of auxins, cytokinins and gibberellins. Currently, many researches about plant growth regulators (PGR’s), growth regulating chemicals and horticultural techniques have been successfully investigated to solve the problem about fruit drop of fruit trees. Hence, it can be said that all of these techniques had an enormous role in fruit growth, yield and quality development.

Plant Growth Regulators (PGR): The role of PGR acts as a messenger and required only in small amount at low concentration to regulate the flowering and other developmental process [19]. PGR have been proven to increase crop productivity by decreasing of bud and fruit drop and increasing the quality and fruit retention. According to Ali et al.,[20], PGR becoming vital tool among agricultural practices which have proven affected to the crop production and it also relatively low cost. Here, there are three types of PGR have been discussed: Gibberellic acid (GA3), 2,4- dichlorophenoxyacetic (2,4-D) and Naphthaleneacetic acid (NAA).

Gibberellic acid: Gibberellic acid is used widely in horticulture for improving fruit set and to control apple russeting [21] cracking in pomegranate fruits [22] and increased flowering [23]. Almeida and co-workers [24] reported that GA3 also improve the productivity of oranges by decreasing of bud drop. From the study, they found that the endogenous hormones and its balancing play a modulating role in the mobilization of nutrients to the developing organs and can influence the longevity of a bud in the fruit. Moreover, according to Khandaker et al., [25], GA3 treatments produced important effects on reduction of bud and fruit drop (Figure 6). GA3 treatments in 50 mg/L gave the lowest percentage (29%) of bud drop compared to untreated control branches with the 36% percentage of bud drop. Treated-branches of wax apple plant with 20 mg/L GA3 reduce the fruit drop with percentage 32% followed by 50 and 100 mg/L GA3 treatments. The highest percentage of wax apple fruit drop (52%) was recorded in untreated GA3 treatment branches (Figure 6).

Fig. 6: GA3 treatment effects on bud and fruit drop of wax apple [25]

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From the studies of Tuan and Chung-Ruey[8], they reported that the reducing number of flower and fruit drop of wax apple can be resolved when spraying with 10 ppm GA3. Davies and Zalman[26] also reported that GA3 treatment increased the total number of fruits, fruit weight per plant significantly by reducing pre-harvest fruit drop. From the research that have been done, Jiet al.,[27]stated that by spraying GA3 at 50 mg/L for 5 weeks after flower blooming reduced the fruit drop in “Huaizhi”. Spraying of GA3 at 50–100 mg/l at full bloom also enhanced fruit retention and fruit size in “Early seedless” and “Calcuttia” litchi in India [28]. It has been reported that growth regulators application enhanced flower bud development and other physiological activities of plant [29].

2,4-dichlorophenoxyacetic, (2,4-D): The compound 2, 4-D is regarded as one of the most effective ones in preventing fruit drop in citrus [30]. 2, 4-D is a synthetic auxin type growth regulator that brings about a growth response in plants at a low concentration but at higher concentration it becomes a herbicide [31]. 2, 4-D enhanced the inflorescence development; fruit set and increased the number of fruit per plant in strawberry and raspberry [32]. Auxin (2, 4-D) is general growth factors involved in many developmental processes throughout the plant, nevertheless, they can play a major role in the fruit set and development [33]. The use of auxins prevents dropping of fruit by maintaining the cells at zone of abscission, preventing the synthesis of hydrolytic enzymes such as cellulase, which decompose the cell wall. Davies and Zalman [26] was observed that synthetic auxin (2, 4-D) significantly reduced the fruit drop in citrus fruits. Agusti et al.[34] also described similar observations that, 2, 4-D at 15 mg/L treatment reduced abscission by 50-75% and that had no effect on the external and internal characteristics of the fruit.

Fig. 7: 2, 4-D treatment effects on bud and fruit drop of wax apple [23]

Khandakeret al., [35] reported that the application of 2, 4-D treatments had a significant effect on fruit dropping of wax apple (Figure 7). The study shown 2, 4-D treatments significantly reduced the fruit drop but at a higher doses of 2, 4-D is less effected. They stated that the least fruit drop (18%) were recorded in the 5 mg/L 2,4-D treatment followed by 10 mg/L 2, 4-D and 20 mg/L 2, 4-D with a value of 26 and 25%, respectively, whilst, the highest (40%) fruit drop observed in control branch (Figure 7). Lima and Davies [36] successfully reduced summer drop in with 20 ppm 2, 4-D or in combination with 20 ppm GA applied to nine weeks after mid bloom.El-Otmani, [37] also reported that the combined application of GA3 and 2, 4-D reduces the precocious drop of fruit through the action of auxin and retards the softening and senescence of the peel, by the longer harvest time, and more economical storing in areas where stocking capacity is limited and the cost is high. So, to control the highest fruit drop was exhibited by 2, 4-D resulting in high yield and quality of fruit.

Naphthalene acetic acid (NAA): To prevent fruit drop, naphthalene acetic acid (NAA) have been used [38]. Besides reducing fruit drop, NAA also may enhance background colour development and fruit softening, under circumstantial environmental conditions [39]. NAA has been reported to stimulate cell enlargement in orange, enhancing fruit growth in citrus [40]. More recently, it was observed that NAA significantly increased fruit set, fruit length, diameter and weight as well as yield in guava [41]. It was found that application of NAA reduced the fruit drop, increased yield, TSS, total sugar and -C contents in guava fruits [42] .

118 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

Fig. 8: NAA treatment effects on bud and fruit drop of wax apple [43]

Regarding to the previous study, Khandaker and co-workers [43] reported that NAA treatments reduced the fruit premature fruit drop and their concentration of treatments were significantliy differences among each other (Figure 8). They also observed that heavy rain before harvesting that enhanced fruit drop significantly. They stated that the lowest concentration of NAA treatment (5 mg/L) gave the best result compare to others for percentage of fruit drop (30 %) followed by 10 mg/L (41 %) and 20 mg/L (42 %) (Figure 8). The untreated NAA branch shows the highest of fruit drop (52 %). It proved that NAA treatment can reduced the fruit drop.Davies and Zalman [26] also reported that NAA gave the big impact in reducing of fruit drop in citrus fruits. NAA at 50 mg/L and 50 mg/L GA3 at full bloom and three months after the first spray gave the positive results in reducing pre harvest fruit drop and fruit seed contents in guava was studied by El-Shewy [44].Dutta and Banik [41] reported applying GA3 and NAA before flowering, followed by three weeks after fruit setting and observed that foliar application of NAA significantly improve the fruit length, diameter and fruit weight and crop yield of guava. Improved fruit yield and quality can thus be obtained by reducing heavy fruit drop. It had been shown that NAA increased final fruit size through its thinning effect, so reducing competition among developing fruits [45]. It is believed that during part of the period of abscission, both this process and hence fruit set and fruitlet growth rate are related to carbohydrate and other metabolites availability.

Horticulture technique (Girdling): Girdling is an old practice that has been used to improve crop productivity. The removal of a small strip of bark around a branch or trunk obstruct basipetal phloem transport and make available more photosynthetic metabolites to the growing regions above the strip [46]. Although removing the strip of bark wounds the tree, it heals within several weeks. A technique of girdling branches which enhanced carbohydrate availability to fruit lets as it is believed to remove competition with the roots, reduces fruitlet abscission but had no effect on flower abscission in apple [47]. The increasing in carbohydrate supply caused by girdling correlated with a transient reduction in fruitlet abscission in ‘Ponkon’ mandarin was studied by Mataa et al.,[48]. Besides, the different types of girdling exhibited the lowest bud abscission and increase the fruit set [48].

Fig. 9: The different types of girdling affected to reduce of fruit drop [49].

119 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

Fig. 10: Girdling treatment effects on bud and fruit drop of wax apple [49].

Khandaker et al.[49] reported that the V-shape girdling exhibited the lowest bud abscission number, averaging about 10 % followed by C-shape girdling, 50% stress, 100% stress and I-shape girdling with percentage of bud drop 16, 30, 30 and 36 %, respectively (Figure 9 & 10). They also found that non-treated control branches recorded around 48 % bud dropped and almost five times more buds dropped in untreated branches compared with the V-shape girdled branch, which was statistically significant. From the graph, untreated control treatment of branches produced the highest percentage of fruit drop (55 %) followed by the 100 % phloemic stress and I- shaped (both same result, 40% fruit drop), C-shaped and V-shaped (both same result, 36% fruit drop), and the lowest fruit drop was 50% phloemic stress with 35 % of fruit drop (Figure 10). Girdling few weeks before flowering were decrease the fruitlet abscission but increased leaf chlorophyll content and chlorophyll fluorescence[50]. Furthermore, among the other different factors, poor tree nutrition is a crucial factor which can cause bud and fruit drop [51]. From the previous studies, the girdling technique is well known can improve photosynthesized availability and increase fruit-set and yield in citrus fruit [52].

Growth regulating chemical (Hydrogen peroxide): Hydrogen peroxide (H2O2) plays an important role as a signaling molecule in physiological process and regulator of the expression of some genes in cells [53].Woods et al.[54] reported the reactive oxygen spesies including H2O2 were influencing the development, ripening and senescence in many fruits. Webber and co- workers [55] also stated that the used of the hydrogen peroxide to nasturtium flowers improve the bud and increase the number of the flower. Besides, Souza et al. [56] stated that hydrogen peroxide also increased floral receptivity in passion fruits. Some other researcher stated that disease also caused a significant loss of crop by enhancing preharvest loss [57] Based on the Figure 11, Khandaker and co-workers [58] reported that hydrogen peroxide-treated branches have positive effect on bud and fruit development in wax apple plant . The branches with 20 mM H2O2 treatments reduced bud abscission numbers with 29 % of bud drop followed by the 50 mM (33 % bud drop) and 5 mM (39% bud drop). Untreated H2O2 branches shows the highest bud drop with percentage 48%. Furthermore, they also found that the positive result in decreasing of wax apple fruit drop. With 5 mM H2O2 treatments, the percentage of fruit drop were decreased which is 28% followed by 20 mM (35%) and 50 mM (38%) H2O2 treatments. These results were found to be in an agreement with Ozaki et al., [59] who reported that hydrogen peroxide play a major role in melon fruit set and premature fruit drop as well as enhanced the fruit quality. It has been reported that growth regulators and growth promoting chemicals produced a significant effect on physiochemical properties of wax apple [60].

120 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

Fig. 11: H2O2 effects on fruit drop [58]

Conclusions: Wax apple is one of the popular fruit in Malaysia and other South East Asian countries. which have a lot of commercial values due to its properties. The major problems faced by wax apple production regarding to premature fruit drop. One of the cause of fruit drop is pollination and fertilization failure. Lack of pollination and fertilizer will increase the amount of flower drop. Wax apple that planted at highly saline soil also have difficulty in absorbing enough moisture from the soil as well as unbalanced nutrient in premature fruit also were causes of premature fruit drop. In ddition, the lack of water supply and high temperature also gave the negative effect to wwax apple fruit development. Another causes of fruit drop were heavy rains and chilling injury berofe harvesting and infestation by insect, mites and diseases. Some precautions to overcome the bud and fruit drop in wax apple fruits have been done reviewed in this study. Significant enhancement of fruit growth and development were recorded in S. samarangense in response to some plant growth regulators application. With GA3, these improvements included increased fruit set and reduced fruit drop. Wax apple treated –branches with GA3 treatments in 20 mg/L gave the lowest percentage (32%) of fruit drop compared to untreated control branches with the 52% percentage of fruit drop. The used of low concentration of 2,4-D treatment will be maintain the cells at zone of abscission which is reduced the wax apple fruit drop. 2,4-D with 5 mg/L gave positive result to premature fruit drop with percentage dropped, 18% whilst, 40% fruit drop observed in untreated control branch. Similarly with NAA treatment also significantly reduced fruit drop with 5 mg/L NAA treatment (30 %) compare to untreated NAA branch with 52 % of fruit drop. Girdling technique also was observed gave a significant effect on fruit retention, bud number and fruit number. Fruit set of girdled branches increased significantly, possibly due to accumulation of carbohydrate in the upper part of girdling. Girdling treatments (C-shaped and I-50 %) reduced the bud and fruit drop with percentage 10 % and 35 %, respectively. In addition, hydrogen peroxide treatments have been proved can improved fruit set and reduced bud drop of wax apple with concentration 5 mM and 20 mM H2O2, respectively.

Future Works: The findings of this study will help to identify the cause and remedy of fruit drop at tropical climates. Integrated plant nutrient management, major insects responsible for premature fruit drop and pathological fruit drop, merit to further study.

Contribution of The Study: There is a great scope to increase the development of wax apple industry in Malaysia and other tropical countries. The Malaysian climate is suitable for the wax apple production and fruits can be harvested all the year round. It has been well documented that the application of some plant growth regulators, horticultural technique and promoting chemical were believe can improved the postharvest behavior of the wax apple fruits which is reduced the premature fruit drop. This study was bring great benefits to local farmers and also stakeholders who are interested to invest in agriculture business. So, it directly contributing in country’s economy. Lastly, for education point view, this knowledge also will gave the advantages to the students, researchers and local farmers. Acknowledgements:

121 Mohammad Moneruzzaman Khandaker, 2016 Advances in Environmental Biology, 10(11) November 2016, Pages: 112-123

We acknowledge the Research Management & Innovation Complex (RMIC), Universiti Sultan Zainal Abidin for publication support.

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