Fusaricidins in Paenibacillus polymyxa A21 and their antagonistic activity against Botrytis cinerea on tomato

Weicheng LIU, Xiaoli WU, Xuelian BAI, Hong ZHANG, Dan DONG, Taotao ZHANG, Huiling WU

Front. Agr. Sci. Eng. ›› 2018, Vol. 5 ›› Issue (2) : 262-270.

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Front. Agr. Sci. Eng. ›› 2018, Vol. 5 ›› Issue (2) : 262-270. DOI: 10.15302/J-FASE-2017166
RESEARCH ARTICLE
RESEARCH ARTICLE

Fusaricidins in Paenibacillus polymyxa A21 and their antagonistic activity against Botrytis cinerea on tomato

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Abstract

Four kinds of antifungal compounds from an extract of Paenibacillus polymyxa A21 with molecular masses of 883.56, 897.59, 947.55, and 961.58 Da were characterized as the members of fusaricidin-type of antibiotics according to LC-MS analysis. Fusaricidins isolated from culture filtrate displayed high antagonistic activity against several plant fungal pathogens, especially Botrytis cinerea, the causal agent of gray mold. The fusaricidins biosynthetic gene cluster (BGC) from A21 was cloned by PCR and comparative cluster analysis revealed that gene fusTE, the 3′ boundary of the fusaricidin BGC in strain PKB1, was not present in fusaricidin BGC of A21, indicating that fusTE is not necessary for fusaricidin synthesis. Fusaricidin extract from A21 significantly reduced gray mold disease incidence and severity on tomato. The mRNA levels for three patho-genesis-related proteins (PRs) revealed that treatment of tomato leaves with fusaricidin extract induced the expression of PR genes to different levels, suggesting that one reason for the reduction of gray mold infection by fusaricidin is induction of PR proteins, which lead to increased resistance to pathogens. This is the first report of the application of fusaricidins to control tomato gray mold and the comparative cluster analysis provides important molecular basis for research on fusaricidin biosynthesis.

Keywords

antifungal activity / biosynthetic gene cluster / Botrytis cinerea / fusaricidin / Paenibacillus polymyxa

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Weicheng LIU, Xiaoli WU, Xuelian BAI, Hong ZHANG, Dan DONG, Taotao ZHANG, Huiling WU. Fusaricidins in Paenibacillus polymyxa A21 and their antagonistic activity against Botrytis cinerea on tomato. Front. Agr. Sci. Eng., 2018, 5(2): 262‒270 https://doi.org/10.15302/J-FASE-2017166

1 1 Current situation of food security

1.1 1.1 Food is the precondition and foundation for human survival and development

Food security is the precondition for human survival and development, the foundation for national economic and social development, as well as the basic constraint for the existence and development of human society[1]. Under the basic self-sufficient food security policy, increased grain production has become the primary goal that the agricultural management and production departments in China have been aiming to achieve. With the increase in population, the improvement in economic conditions, and the changes in dietary patterns in China, food demand will continue to expand[2]. The constraints of resource and environment, however, restrict the further increase of grain yield. Therefore, it is of significant importance, in both theory and reality, to establish scientific and reasoned approaches so that food production and food consumption match each other by formulating an appropriate food qualitative and quantitative targets based on the human nutritional requirements.

1.2 1.2 Food and nutritional requirements

Food contains the nutrients that meet the needs of the human body. Proteins, fat, carbohydrates, water, vitamins and minerals are the six major nutrient groups. Among them, proteins, fat and carbohydrates are the main constituents and energy supplying materials for the activities of living cells, and their requirements are substantial, whereas vitamins and minerals are needed in only trace amounts. China is rich in resources and is completely able to meet its current and future nutritional requirements.
Fat comes mainly from vegetable oil and animal fat. In terms of nutritional requirements of fat, the people in mainland China need about 28 Mt of fat (Tab.1). Edible fat and oil consumption in China has increased from 13.5 Mt[5] in 2000 to 30.4 Mt in 2013, which shows the trend in China and a shift from an inadequate intake of oil and fat to a state of excessive consumption. In the past decade or so, the large imports of oil and oil plants have seriously inhibited domestic edible oil production using squeezing/extracting techniques[6]. In 2013, China’s vegetable oil production was about 14 Mt, while the production of edible oilseeds reached up to 58 Mt[7], which was equivalent to about 19 Mt of vegetable oil (Tab.2). In addition, the availability of animal fat was about 8.7 Mt in 2000 (supplies of pork, beef and mutton were 47 Mt, and eggs were 21 Mt[8], when the amount of soybean meal made from imported soybeans and used to feed livestock was less than 7 Mt). After taking into account a loss rate of 5%, the sum could reach 26.6 Mt, which would be 94.3% of the fat requirements of the population. Thus, from the perspective of dietary patterns and nutritional requirements, the domestic production oil plants can basically meet Chinese edible oil requirement.
Tab.1 The requirements of main nutrients (proteins, fat and carbohydrates)
Age (years old) Populationa (ten thousand) Average weight/kg Protein requirementsb Fat requirements Carbohydrate requirements
Average requirements per person each day /g Annual total requirements/kt ( × 10) Average requirements per person each day/g Annual total requirements /kt ( × 10) Average requirements per person each day/g Annual total requirements/kt ( × 10)
0 1378.64 7.85 22.32 11.23 19.84 9.99 111.62 56.17
1 2311.92 9.63 24.45 20.63 21.73 18.34 122.26 103.17
2 2412.51 12.09 31.02 27.31 27.57 24.28 155.10 136.57
3 2352.33 14.38 35.10 30.13 31.20 26.79 175.48 150.67
4 2346.62 16.36 38.52 33.00 34.24 29.33 192.61 164.98
5 2272.03 18.22 41.56 34.47 36.95 30.64 207.82 172.34
6 2283.89 20.2 44.76 37.31 39.78 33.16 223.78 186.55
7-9 4134.49 25.25 52.20 78.77 46.40 70.02 260.98 393.85
10-12 4378.96 36.20 66.33 106.01 58.96 94.23 331.63 530.04
13-15 4914.33 50.34 80.91 145.12 71.92 129.00 404.53 725.61
16-18 6032.12 61.28 85.22 187.63 75.75 166.78 426.09 938.13
19-64 91421.54 62.00 66.41 2215.90 59.03 1969.69 332.03 11079.50
Above 65 11892.72 60.84 57.03 247.56 50.69 220.06 285.16 1237.82
Total 133281.11 3175.08 2822.29 15875.39

Note: a the population data comes from the Sixth National Population Census[3], which only included Mainland China; b proteins provide 10%−15% of the total calories, and the median value of 12.5% was used; fat provides 25% of the total calories, while carbohydrates provide 60%−65%, and the median value of 62.5% was used[4].

Tab.2 Oil and fat consumption in China (2013)
Type Source Yield/kt ( × 10) Consumption/kt ( × 10)
Fat content Domestic resource Import Population Livestock and poultry
Vegetable oil Soybean oil 251 1535 1140 105
Rapeseed oil 614 153 580 /
Palm oil 1 598 428 230
Peanut oil 252 6 246 /
Sunflower Seed oil 50 75 100 25
Corn oil 72 148 72 /
Tea-seed oil 45 / 45 /
Cottonseed oil 118 / 30 30
Sesame oil 25 10 20 /
Total 1428 2525 2661 390
Animal fat Egg 8.8% 2876 / 254
Milk 3.4% 3531 20 163
Fish 2.5% 3160 417 82
Pork 28% 5493 58 1473
Beef 10.2% 673 29 61
Mutton 14.1% 408 26 57
Total 16141 550 2090

Note: Domestic production includes that made in Mainland China and import means the sum of the oil directly imported to Mainland China and the oil quantity converted from imported oil seeds.

Carbohydrates are the main nutrients that supply energy. They occur extensively in rice, wheat, corn, tuberous crops and bean crops. In 2013, the food production in China included grain production of 601 Mt[9], which contains 400 Mt of carbohydrates, and about 201 Mt[10] of carbohydrates used for human consumption. In terms of the total nutritional requirements, the people in Mainland China needed about 159 Mt of carbohydrates per year, and the domestic grain production can meet this need now and for the next 20 years (Tab.1). The proportion of China’s food consumption to total grain consumption decreased gradually by 51% between 1995 and 2008, reaching 268 Mt in 2008. The growth of grain used for animal feed is the main reason for the increase of grain consumption in China, with the proportion reaching 34% in 2009, and grain for industrial uses accounting for 15%[11]. While the proportion of grain imports in gross production was less than 3%[12]. These data illustrate that China’s supply of carbohydrates can perfectly ensure the nutritional requirements of its population.
Proteins are indispensable for sustaining life, and mainly come from meat, eggs, milk, fish, beans, wheat and corn (Tab.3). Based on the required protein intake, which also provides 12.5%−15% of the total calories, the preliminarily estimate of the protein requirement of the Chinese population is 31.8 to 38.1 Mt in 2013 (Tab.1). In 2013, protein consumption in China was 46.3 Mt (equivalent to the recommended dietary protein, Tab.4) and the current supply of protein was lower than the protein requirement based on a healthy target. Secondly, lysine, methionine, threonine and tryptophan in plant-derived proteins occur in relatively low proportions, which means the supply of these amino acids from plant sources is restricted and must be supplemented by animal-based foods[13]. Currently vegetable protein (2.5 Mt) and animal protein (9.0 Mt) available in China come from imported meat products or are indirectly produced from imported agricultural products, including imported soybeans (63 Mt). The country’s self-sufficiency rate of edible proteins is 73.1% (Tab.5), and the self-sufficiency rate for protein feeds is about 52.6%. Imported agricultural products can have a competitive price advantage over domestic agricultural products. Therefore, from the perspective of nutritional requirements and food quality, the grain security issue is, in essence, dependent on protein production and supply.
Tab.3 Protein source for China (2013)
Source Protein content Total/kt ( × 10) Population consumption/kt ( × 10) Livestock consumption/kt ( × 10)
Domestic Imported Food Protein Feed Protein
Vegetable protein Rice 8.5% 20308 227 16190 1376 1690 144
Wheat 14.0% 10490 553 8275 1159 1525 214
Corn 11.0% 20020 327 1360 150 15400 1694
Potato 2.3% 8893 4 5783 133 1512 35
Soybean 35.0% 1256 6338 938 328 / /
Bean pulp 42.0% 992 5153 / / 5220 2193
Rapeseed meal 36.0% 1105 20 / / 638 230
Cotton seed meal 44.0% 437 127 / / 375 165
Total / 63601 12749 32546 3146 26360 4675
Animal protein Egg 13.3% 2020 863 2883 383 / /
Milk 3.3% 3531 20 3538 117 / /
Fish 18.5% 3160 417 3277 606 / /
Pork 13.2% 2498 3053 5262 695 / /
Beef 20.0% 673 29 659 132 / /
Mutton 19.0% 408 26 406 77 / /
/ 13603 3545 16025 2010 / /

Note: Protein contents are mean values for all kinds of food.

Tab.4 Edible dietary protein for Chinese (2013)
Type Consumable Protein/kt ( × 10) Loss rate Dietary protein for population/kt ( × 10) Type Consumable Protein/kt ( × 10) Loss rate Dietary protein for population/kt ( × 10)
Vegetable protein Rice 1376 20% 1101 Animal protein Egg 383 12.5% 335
Wheat 1159 20% 927 Milk 117 5% 111
Corn 150 20% 120 Fish 606 15% 515
Potato 133 20% 106 Pork 695 12% 612
Soybean 328 20% 262 Beef 132 12% 116
Mutton 77 12% 68
Total 2516 Total 2010 1757
Recommended dietary protein /kt ( × 10) 4273

Note: The value of loss rate were adopted according to mean estimated value.

Tab.5 Supply and requirement of protein in Chinaa
Type Amount/kt ( × 10) Requirementb/kt ( × 10) Supply rate/%
2013* 2013# 2030* 2030# 2013* 2030#
Consumption 4273 3175 3810 3617 4340 134.6 98.5
Domestic resource 3122 98.3 71.9
Imported resource 1151 36.3 26.5
Potential by techniques 927 29.2 21.4
Predictionc 4049 127.5 93.3
Max domestic potentiald 4850 152.8 111.8

Note: a the population data comes from the Sixth National Population Census, which included only Mainland China[3]; b the population is estimated to be 1.515 billion in 2030; c the predicted supply was calculated based on the sum of domestic and potential yield in 2013 from processing and preserving techniques; d the value is estimated based on land and sea resources of Mainland China in 2025 assuming that food and agricultural products from oversea cannot be imported. * assuming that proteins provide 12.5% of the total calories; # assuming that proteins provide 15% of the total calories.

2 2 Problems concerning China’s food security and protein security

People are the foundation of a nationality, food is the basic requirement of the people. China’s total grain production has been increasing for ten consecutive years, which lays a solid foundation for ensuring the national grain security and stabilizing the economic development. However, considering the large population and relatively scarce agricultural land in China, the total agricultural resources are insufficient and the per capita resources are far below the world average. Grain security remains a critically important global strategic issue for the future, which has a bearing on national economic development, social stability and national security in China.

2.1 2.1 China faces great pressure in guaranteeing the continuously adequate grain supply

Over the last decade, China’s grain production has been increasing annually, with the total grain production reaching 602 Mt in 2013[9], which was the highest level of production recorded. Concurrently, the yield of grain crop per unit showed logarithmic growth; the yield of the grain per unit continues to increase and variation in yields decreased gradually. This indicates that to achieve an increase in grain yield per unit area will become increasingly difficult[14]. It can thus be seen that China faces great pressure to enhance grain production. The three main factors that restrict the increase of grain production are as follows.

2.1.1 2.1.1 High rate of loss of cultivated land resources

Cultivated land is the basis of food production as it produces grain directly and provides various meat and milk products indirectly via the feed use pathway. First, the quality of cultivated land is being seriously degraded and this degradation poses a clear threat to the stability of grain production. Overuse of land and man-made emissions of waste gas, waste water and other wastes destroy the nutritive materials in the soil, resulting in the degradation of farmland. Currently, degraded farmland accounts for over 40% of the total cultivated area in the country[15]. Secondly, the quantity of farmland is reduced. As the economy is developing and the ratio of urbanization is increasing, a large amount of agricultural land is transformed into urban land and farmland per capita declines. Mu et al. pointed out that the farmland per capita in China declined from 0.10605 hm2 in 1996 to 0.10138 hm2 in 2009[16]. In the investigation conducted by Liu Jinghui, it was found that medium and high-production farmland contributed more than 80% of grains[17]. Therefore, the present low population-carrying capacity of farmland in China is a serious problem, which limits the development of China's agriculture as well as the increase of protein production.

2.1.2 2.1.2 Water resources are in short supply and unevenly distributed

China is a country with relatively scarce water resources which, on a per capita basis, are only equivalent to 28% of the world average. Also, national water resources are unevenly distributed, with water and soil resources being severely misaligned. Northern farmland area takes up 60% of the national farmland area while water resources only account for 20% of the national total[18]. Finally, with the increase in domestic and industrial sewage, available water resources for irrigation further decline. Wang et al. found serious problems contributing to agricultural water shortage and pollution which would restrict the development of agriculture[19]. Thus, water resources have a serious influence on the stability of grain production, further influencing protein security in China.

2.1.3 2.1.3 High dependence on imported protein

Over recent years, feed resource shortage has become a limiting factor for China’s feed and breeding industries, and the dependence on imported protein feed resources country increases annually. Soybean and fish meal are the main proteins in good supply for quality feed, but these are lacing in China and must be imported in large amount. In 2013, domestic production of soybeans was 12.6 Mt and imports were 63.4 Mt, meaning the dependence on imported soybean was 83.9%[20]. During the period from 2004 to 2010, the external dependence of China on fish meal remained above 70%[21]. Thus, protein supply in China showed obvious characteristics of limited domestic production growth, sharp increase of imports, and high foreign dependence.

2.2 2.2 Demand for protein in China increases annually

With growth of population, rising incomes, and promotion of urbanization, total demand for food proteins in China increases annually.
Firstly, the population is growing and the economy is developing. China’s population increases on average by 12 million per year and the demand for proteins increases about 0.3 Mt, equivalent to 1.3 Mt of pork. At the same time as growth in population, urbanization directly promotes a change in nutritional and dietary patterns, thus increasing the demand for proteins per capita[22]. Hence, population growth and urbanization are becoming increasingly important factors influencing the demand for proteins in China.
Secondly, the consumption of proteins of high biological value is increasing. With increased food consumption and improved consumption structure, China’s consumption of animal proteins has grown rapidly[23]. In 1990, China consumed meat products, aquatic animal, and milk of 25.3, 12.5, and 4.2 Mt, respectively, and 71.0, 64.9, and 47.9 Mt respectively in 2013. From 2010 to 2012, the average growth rate of feed production reached 8%[24], while the growth rates of grain were only 2.9, 4.5, and 3.2%[25]. The growth rate of feed grain greatly exceeded that of grain production in the same period, which has exerted great pressure on grain production, feed grain supply and food security in China.

2.3 2.3 Improvements in storage, transportation, and processing technology for protein production

Currently, there are mainly three aspects affecting China’s protein resource development and utilization. Firstly, losses occur during grain preservation, transportation. Secondly, the contribution of protein processing technologies to both resource and the overall utilization rate are both relatively low. Finally, there is considerable wastage of food resources during utilization.

2.3.1 2.3.1 Serious post-harvest loss of grain

Post-harvest loss of grain is an issue that cannot be ignored and requires an urgent solution. Looking at the domestic and international conditions of food utilization, a large amount of food is not stored or transported appropriately after production. Loss and waste inevitably occur during harvesting, purchase, transport, storage, processing and consumption of food. China’s loss rate at all stages is shown in Fig.1, with the overall loss rate reaching 16%−22%[26]. Considering just the storage, transport and processing, the total amount of grain loss and table waste after production reached 122 Mt (in 2012, China’s total grain production weighed 590 Mt), taking up 21% of the country’s total production in 2012[27].
Fig.1 Loss rates at each stage of food production and consumption

Full size|PPT slide

2.3.2 2.3.2 Low overall utilization rate

At present, the utilization rate of protein resource in mainland China is relatively low. Plenty of by-products that are rich in protein are not fully utilized, either being thrown away or used as fertilizers, which causes a huge wastage of protein resources. For instance, around 10 Mt of rapeseed cake (the byproduct of oil extraction) is produced annually in China, only 42% of which is used as fodder. The annual production of cottonseed meal is around 5 Mt, only 30% of which is used for feed and most of which is used as fertilizer. On the whole, the efficiency of transforming feed into protein is low, thus causing huge wastage of feed protein resource. Taking broiler and pig feed, as examples the efficiency of transforming feed into protein in the United States is respectively 18.8% and 25.0% higher than China[28]. Thus, an effective way to solve the issue of China’s protein security is to achieve high-value, resourcing and ecological utilization of low-valued biological protein by using high-tech means, to eliminate toxins and anti-nutritional factors and to provide a balance of dietary amino acids.

2.3.3 2.3.3 Food contamination wastes precious protein

Ever since China’s economic reform and liberalization, the overuse and improper use of pesticides, veterinary drugs and additives has resulted in excessive residues of toxic and harmful substances in agricultural products. Also there has been a series of food safety incidents, such as poisonous milk powder, illegal cooking oil, tainted steamed buns, water-injected meat and the like. These not only affect the intake of the nutritional components in food, but more importantly, cause severe damage to human health[29]. In 2008, the melamine incident caused over 100 kt of inedible tainted milk powder, which is a good example of protein waste, indicating how food safety events can cause protein loss or weaken its nutritional impact. Such food safety events in China affect protein supply or edible value.

2.4 2.4 Out-of-balance dietary structure lowers food’s nutritional value and damages human health

Chinese dietary structure is out-of-balance in the country. The distribution situation of consumed protein is also dramatically different for people in economically developed or developing areas. According to an investigation conducted by He Yuna and the others, in 2002, the ratio of calories originating from fat already reached 35% of the total calories consumed by China’s urban residents, exceeding the 30% upper limit recommended by the World Health Organization (WHO). The proportion of calories from protein was around 11.8% of the total calories. Among urban dwellers, energy provided by cereals was 48.5% of the total calories, obviously lower than the recommended range of 55%−65% and the 61.5% for rural residents[30]. These data illustrate that urban residents take in excessive fat, insufficient protein and too little carbohydrate. When taking into consideration the regional differences and income gaps, food protein intake is woefully inadequate in some regions. For dwellers in big cities, 49.4% of the protein comes from the high-quality protein contained in beans and animal food, while in the countryside, the percentage ranges between 17.1% and 28.0%, which seriously influences the health of rural people.

3 3 Suggestions for ensuring food and protein security

3.1 3.1 A small increase in total grain production and progressive adjustment to the proportion of animal and plant protein

Guaranteeing grain security is a strategic problem for a country’s social stability and national self-sufficiency. Total grain production can be increased slowly and steadily through policy guidance, meticulous management, technological contributions, and capital-driven means. According to our forecast, even though the population will increase by 13.7% (up to 1.515 billion), China can supply 100% of the carbohydrate and 95% of the fat. Tang predicts that, by 2030, 1.515 billion people may need 586 Mt[31] of grain, and the estimate is calculated at 650 Mt using the econometric methods.
Multiple methods are needed to increase the quantity of protein supply, such as increasing the yield of feed grain, increasing the proportion of non-grain fodder through science and technology, and improving the efficiency of transforming feed into animal protein. The food security policy in China can be refined as the need for protein security. This viewpoint is more intensive and scientific than Pan's presentation that China’s grain problem is mainly the feed grain problem[32]. Therefore, China should ensure the quantity of animal protein transformed from grain or non-grain fodder is sufficient and improve the conversion efficiency.

3.2 3.2 Promoting the application of technologies for protein extraction and processing

Intensifying the development and utilization of existing protein resources is the most effective way to guarantee protein security in China. Efficient use of existing technology and the development of new technology could vastly improve the nutritional characteristics of protein resources and enhance the digestibility and use efficiency of protein, effectively removing the toxic and harmful substances, and realizing the goal of saving resources and improving nutrition, food safety and environmental protection. The application of new and high technology such as shell removal, extrusion and expansion, fermentation, ultrafiltration, and superfine grinding can increase the amount of protein extracted from bean pulp, rapeseed meal, cottonseed meal, and other protein resources with high protein content by over 10.5 Mt. Chen et al. found that the functional indices of corn gluten meal after extrusion can be improved significantly, in addition the color, smell and water solubility of the products can also be improved, protease inhibitor activity inhibited, and digestibility and use efficiency raised[33]. Science and technology has a considerable prospect for maximizing the potential of protein resources, and is one of the most effective ways to relieve China’s protein safety problems.

3.3 3.3 Adjustments to dietary patterns and promotion of nutrition security

Grain, nutrition and food security is a great challenge for all parts of the world. In October 2012, the Committee on World Food Security suggested to replace “grain security” with “food and nutrition security,” which reflected the rising awareness of this issue at the international level. Chinese people can adopt more balanced dietary patterns to improve the biological value and nutritive value of protein. Eating two or more kinds of protein sources can provide a balance of essential amino-acids for the human body and thus improve the biological value of protein. For example, when eating either bean curd or wheat gluten separately, the biological values of the two are 65 and 67 respectively. But when eating them with a proportion of 42 to 58, the biological value is increased to 76[34]. Advocating a mixed diet of meat and vegetables in our daily life can adequately supplement the value of protein (or limiting amino acids) and make the amino acids or polypeptides in the food more easily absorbed, thus achieving better nutritional and health outcomes.

3.4 3.4 Raising awareness of nutrition and improving consumption habits

China should effectively improve people’s cognitive level of nutritional knowledge, gradually popularize the use of nutrition labeling, and adequately promote understanding of the properties of food through the popularization of science and the power of mass media. Furthermore, China should raise people’s awareness of nutrition, correct bad eating habits, improve the dietary patterns, and enhance the health literacy by intensifying education concerning a scientifically-based diet[35]. In addition, China needs to guide the consumers to consume scientifically and rationally, oppose wasteful behavior and change bad consumption habits[36].

4 4 Conclusions

From the perspective of nutritional requirements and food quality, the supply of fat and carbohydrates from China’s domestic agricultural production can meet the nutritional requirements of a population up to 1.515 billion. The grain security issue is, in essence, dependent on protein production and supply, especially proteins of high biological value or animal protein. Therefore, the food security policy in China can be refined as an issue of protein security. The potential increase in the amount of protein (9.27 Mt) produced by processing and preserving techniques can replace 80.5% of imported protein. A number of measures should be adopted to raise people's awareness of nutrition and improve their consumption behavior to achieve best practice in use of precious protein resources.

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Supplementary materials

The online version of this article at https://doi.org/10.15302/J-FASE-2017166 contains supplementary material (Tables S1).

Acknowledgements

This work was supported by the Scientific and Technological Innovation Capacity Construction Special Funds, Beijing Academy of Agriculture and Forestry (KJCX20170410), the Science and Technology Innovation Fund from the Beijing Academy of Agriculture and Forestry Sciences (QNJJ201519), and Beijing Key Laboratory of Environment Friendly Management on Fruit Diseases and Pests in North China (BZ0432).

Compliance with ethics guidelines

Weicheng Liu, Xiaoli Wu, Xuelian Bai, Hong Zhang, Dan Dong, Taotao Zhang, and Huiling Wu declare that they have no conflicts of interest or financial conflicts to disclose.
This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2017. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
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