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Pest Control: Can Chitinases Help To Reduce Pesticide Use? Ronivaldo Rodrigues da Silva*,† and Rafaela do Couto Santos‡
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Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), 15054-000 São José do Rio Preto, São Paulo, Brazil ‡ LEAF, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal pesticides in eastern China’s Zhejiang province, especially during the farming season. Furthermore, Chinese farmers are reported to have used approximately 3 times more pesticides in 2016 than the global average (http://www.sixthtone.com/ news/1000987/china-founds-pesticide-office-to-combatpollution%2C-overuse). In view of this, the Chinese government has taken steps to avoid increasing the use of pesticides.2 One example of an abusive use of pesticides relates to chlorpyrifos.4 This compound is used to combat domestic and crop insects in cereals, apples, almonds, oranges, and broccoli. It has been used intensively over the years and is reported to have compromised the development of children, and major symptoms, such as lower birth weight, reduced intelligence quotient (IQ), and loss of working memory, have been reported in the affected children.4
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HOW CAN CHITINASES CONTRIBUTE TO A REDUCTION IN PESTICIDE USE? Chitinolytic enzymes or chitinases are enzymes capable of hydrolyzing the β-1,4 bond of N-acetyl glucosamine residues in chitin. Chitin is an insoluble amino polysaccharide that is relatively resistant and constitutes an essential structural component in a number of organisms, such as nematodes, arthropods (exoskeleton), fungi (cell wall), crustaceans (shells), and shellfish (radula).5 As a result of its importance in the structure of different organisms, chitin has attracted interest as a target for pest control in agriculture and livestock management. Thus, enzymes capable of degrading chitin have gained attention as potential biopesticides to satisfy the demand for technologies capable of mitigating or replacing the use of conventional pesticides. Hydrolysis of chitin by chitinases may be exploited to reduce growth of these pests on plants or to remove ectoparasites from animals. A variety of fungi and arthropods are associated with damage to plants and postharvest plant foods. Specifically, this damage may be caused by fungal species from the following genera: Penicillium, Aspergillus, Geotrichum, Botrytis, Fusarium, Alternaria, and Colletotrichum, among others. Chitinolytic enzymes also present an attractive prospect for management of soybean crops, where they have the potential to combat nematode eggs and larvae, such as those of Meloidogyne spp., Heterodera glycines, Pratylenchus brachyurus, and Rotylenchulus reniformis.6 The annual global production of cereal has reached a high level, and development of strategies for controlling pests is therefore essential to replace pesticide use. According to data
PESTICIDE USE IN MODERN SOCIETY
Since mankind began to utilize land for crop cultivation, there has been increasing concern regarding pest control. The need to control insects in agriculture and diseases transmitted by insects, such as malaria, has boosted the development of compounds with pesticide activity. Thus, in 1939, the first pesticide, dichlorodiphenyltrichloroethane (DDT), was developed,1 with the capacity to combat crop pests. DDT paved the way for new generations of pesticides, and today, pesticides have become part of human routine. A large number of insects, mites, and plant pathogens (including bacteria, fungi, viruses, and nematodes) are known to cause damages in agriculture. Estimates suggest that insectassociated crop losses are around 14%, and those attributed to plant pathogens are approximately 13%.2 The rise in global demand for food and the need to guarantee successful harvests has led to an increase in the application of these chemicals. However, the effects are mostly detrimental, because indiscriminate use of these compounds can cause damage to human health and extended exposure can result in the development of resistance. Irresponsible use and abuse of pesticides have been reported globally. In 2016, Spain, France, Italy, and Germany accounted for the majority of pesticide sales (79%) in Europe, according to data released by the statistical body Eurostat (https://ec. europa.eu/eurostat/web/products-eurostat-news/-/DDN20181015-1). The majority of pesticides purchased in Europe are fungicidal and bactericidal agents (46%), followed by herbicides, haulm and moss killers, insecticides, and acaricides. In China, incidents of environmental contamination with pesticides have been described. Liya3 reported that between 2006 and 2015 approximately 3000 children were exposed to © XXXX American Chemical Society
Received: May 23, 2019
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DOI: 10.1021/acs.jafc.9b03219 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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Journal of Agricultural and Food Chemistry
high inhibitory and insecticidal activities of alosamidin (isolated from Streptomyces sp.) in silkworm (Bombyx mori) were demonstrated, because it inhibited chitinases and prevented ecdysis. Besides, this inhibitor also exhibited antifungal activities against pathogenic fungi.9 Studies on argalin, isolated from Clonostachys sp., also revealed its potential as a biopesticide. Argalin inhibited chitinases from blowfly (Lucilia cuprina) and prevented the growth of the cockroach larvae (Periplaneta americana).10 Despite the existence of patents and the marketing of some chitinase inhibitors (see https://www.sigmaaldrich.com/ catalog/papers/17025016 and https://pubchem.ncbi.nlm.nih. gov/compound/Argadin#section=Patents), further studies continue to investigate new inhibitors of chitinases against different organisms; for example, inhibitors of chitinases from the insect pest Ostrinia furnacalis (Asian corn borer).11 It is crucial to acquire deeper knowledge about these potential green pesticides. The capability to synthesize chitinase inhibitors, costs in development and production, effectiveness in the field, and their environmental impact, such as biodegradation,8 are some of the issues that need to be considered for the use of chitinase inhibitors. The concept of sustainable development is based on meeting the needs of current generations without compromising the needs of future generations. In this context, alternative technologies based on reducing the use of pesticides have long been expected. It is crucial to highlight the importance of the potential role of these enzymes and inhibitors in overcoming this challenge.
from the Food and Agricultural Organization of the United Nations, global cereal production has been increasing (http:// www.fao.org/3/i8384en/I8384EN.pdf) and reached 2609 million tons in the 2016/2017 harvest (http://www.fao.org/ worldfoodsituation/csdb/en/). Control of mites and ticks in cattle breeding also presents a potential application for chitinases. Although there is a consensus that intensive bovine breeding has increased herd productivity, the extensive increase in the number of animals in a reduced space has contributed to the spread of the bovine tick Rhipicephalus (Boophilus) microplus. This parasite causes significant problems for many cattle farmers; it is estimated that tick-borne diseases have resulted in annual losses of approximately US$ 22−30 billion.7 The specific action of chitinases on the exoskeletons of ectoparasites favors their removal without being harmful to the host animals. This specific activity not only reduces the risks to human and animal health associated with conventional chemical pesticides, there is also the advantage of nondevelopment of resistance to chitinases. Microorganisms are accepted as excellent sources of enzymes and have therefore been successfully exploited for this purpose. The application of microbial chitinases in the context of pest control is a promising proposal that complies with the concept of agricultural and environmental chemistry (Figure 1). The high diversity observed in bacteria and fungi
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CONCLUDING REMARKS Chitinases offer an effective contribution to sustainable chemistry. Investigations to discover chitinases and their inhibitors to perfect their applications in combating arthropod and fungal pests may be extremely useful in efforts to reduce the negative effect associated with chemical pesticide use and abuse. Many studies have been reported regarding contamination of soil, water, animals, and plants by pesticides worldwide. It is necessary that alternatives are investigated to reduce this anthropogenic impact on nature and human health. Chitinases have emerged as a promising prospect with potential for application in the agriculture and livestock industries.
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Figure 1. Prospecting for microbial chitinases. Enzymes capable of hydrolyzing the β-1,4 bond of N-acetyl glucosamine residues in chitin from fungi, nematodes, and arthropods.
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Ronivaldo Rodrigues da Silva: 0000-0002-6504-8406
combined with their ease of cultivation present attractive characteristics that enable their use as major sources of enzyme production.
Notes
The authors declare no competing financial interest.
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CHITINASE INHIBITORS In fungi and arthropods, chitinases perform many functions; they help in the growth of hyphae or the cellular separation of fungi and degrade chitin during the ecdysis process in arthropods. Because the functions of chitinases are important for the life of these organisms, chitinase inhibitors have been considered to be another strategy for crop protection.8 Over the past few decades, several studies have been conducted on chitinase inhibitors. Alosamidin and argalin are two of the many chitinase inhibitors discovered.8−10 In 1987,
REFERENCES
(1) Jarman, W. M.; Ballschmiter, K. From coal to DDT: The history of the development of the pesticide DDT from synthetic dyes till Silent Spring. Endeavour 2012, 36, 131−142. (2) Zhang, W. Global pesticide use: Profile, trend, cost/benefit and more. Proc. Int. Acad. Ecol. Environ. Sci. 2018, 8, 1−27. (3) Liya, F. China Founds Pesticide Office to Combat Pollution, Overuse. Sixth Tone; Shanghai United Media Group: Shanghai, China, 2017; http://www.sixthtone.com/news/1000987/chinafounds-pesticide-office-to-combat-pollution%2C-overuse (accessed March 24, 2019).
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DOI: 10.1021/acs.jafc.9b03219 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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Journal of Agricultural and Food Chemistry (4) Lipton, E. Court Orders E.P.A. to Ban Chlorpyrifos, Pesticide Tied to Children’s Health Problems. The New York Times; The New York Times Company: New York; 2018; https://www.nytimes.com/ 2018/08/09/us/politics/chlorpyrifos-pesticide-ban-epa-court. html?rref=collection%2Ftimestopic%2FPesticides&action= click&contentCollection=timestopics®ion=stream&module= stream_unit&version=latest&contentPlacement=4&pgtype= collection (accessed March 24, 2019). (5) Beygmoradi, A.; Homaei, A.; Hemmati, R.; Santos-Moriano, P.; Hormigo, D.; Fernández-Lucas, J. Marine chitinolytic enzymes, a biotechnological treasure hidden in the ocean? Appl. Microbiol. Biotechnol. 2018, 102, 9937−9948. (6) Stetina, S. R.; Smith, J. R.; Ray, J. D. Identification of Rotylenchulus reniformis Resistant Glycine Lines. J. Nematol. 2014, 46, 1−7. (7) Tabor, A. E.; Ali, A.; Rehman, G.; Rocha Garcia, G.; Zangirolamo, A. F.; Malardo, T.; Jonsson, N. N. Cattle Tick Rhipicephalus microplus−Host Interface: A Review of Resistant and Susceptible Host Responses. Front. Cell. Infect. Microbiol. 2017, 7, 506. (8) Saguez, J.; Vincent, C.; Giordanengo, P. Chitinase Inhibitors and Chitin Mimetics for Crop Protection. Pest Technol. 2008, 2, 81−86. (9) Sakuda, S.; Isogai, A.; Matsumoto, S.; Suzuki, A. Search for microbial insect growth regulators. II. Allosamidin, a novel insect chitinase inhibitor. J. Antibiot. 1987, 40, 296−300. (10) Arai, N.; Shiomi, K.; Yamaguchi, Y.; Masuma, R.; Iwai, Y.; Turberg, A.; Kolbl, H.; O̅ mura, S. Argadin, a new chitinase inhibitor, produced by Clonostachys sp. FO-7314. Chem. Pharm. Bull. 2000, 48, 1442−1446. (11) Dong, Y.; Hu, S.; Jiang, X.; Liu, T.; Ling, Y.; He, X.; Yang, Q.; Zhang, L. Pocket-based Lead Optimization Strategy for the Design and Synthesis of Chitinase Inhibitors. J. Agric. Food Chem. 2019, 67, 3575−3582.
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DOI: 10.1021/acs.jafc.9b03219 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
