Rolliniastatin-1, a bis-tetrahydrofuran acetogenin: The major compound of Annona mucosa Jacq. (Annonaceae) has potent grain-protective properties
Introduction
The risk of selecting insecticide-resistant populations poses as a major challenge for integrated pest management (IPM) programs of stored cereals in tropical and subtropical regions. In South America, studies have described populations of maize weevil [Sitophilus zeamais Motsch. (Coleoptera: Curculionidae)] resistant to pyrethroids (Guedes et al., 1995; Corrêa et al., 2011; Cordeiro et al., 2017), organophosphates (Perez-Mendoza, 1999; Corrêa et al., 2011) and phosphine (Pimentel et al., 2009; Corrêa et al., 2014). The limited availability of active ingredients for insecticide rotation in IPM programs of stored cereals aggravates the risk of selecting insecticide-resistant populations of S. zeamais (Boyer et al., 2012). Thus, new compounds with different modes of action are needed for IPM of stored grains.
A potential source of new insecticidal compounds are the secondary metabolites of Annonaceae species, which produce and accumulate acetogenins in abundance, mainly in their seeds (Chen et al., 2012; González-Esquinca et al., 2014). Acetogenins are a class of compounds derived from long-chain fatty acids (C-32/C-34) connected to a 2-propanol unit and γ-lactone subunit (Alali et al., 1999). Acetogenins have insecticidal action and are inhibitors of mitochondrial complex I (Tormo et al., 1999). The botanical family Annonaceae encompasses a wide number of tree and shrub species, mostly native to tropical and subtropical regions, which produce edible fruits used in the food industry (Maas, 2009, 2013; Braga Sobrinho, 2014). Waste seed from Annona fruits could be used as raw material for acetogenin-based bioinsecticide production (Ribeiro et al., 2016). Bioinsecticides formulated from agro-industrial residues are a great opportunity to transform environmental problems into eco-friendly solutions for agriculture.
In addition, an advantage of acetogenin-based bioinsecticides in the global pest management market is their suitability for organic farming. Organic farming is constantly increasing worldwide and needs eco-friendly alternatives for pest management. Roughly 57.8 million hectares are cropped using organic farming, integrating a market of US$ 87.9 billion worldwide (Willer and Lernoud, 2019). Because of their chemical nature, acetogenin-based bioinsecticides could be used in the preventative management of coleopteran pests in stored organic cereals, as Ribeiro et al. (2018) demonstrated using an acetogenin-based commercial bioinsecticide registered in India.
In our previous studies, we reported the promising grain-protective properties of crude extracts from Annona mucosa Jacq. seeds against the maize weevil (Ribeiro et al., 2013), with a crude derivative from this species the most promising source of grain protectants (LC50: 288.3 mg kg−1; LT50: 86.1 h) among the tested neotropical Annonaceae (Ribeiro et al., 2016). Annona-based bioinsecticides have pronounced lethal and sublethal effects on agricultural insect pests, such as Diaphorina citri Kuwayama (Hemiptera: Liviidae) (Ribeiro et al., 2015), Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) (Ansante et al., 2015), Zaprionus indianus (Gupta) (Diptera: Drosophilidae) (Geisler et al., 2019), Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae) (Stupp et al., 2020a), and Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) (Stupp et al., 2020b). However, formulation of a botanical insecticide requires identification and establishment of minimum concentrations of active ingredients as well as identification of a chemical marker for quality control of formulations. Moreover, isolation and elucidation of chemical structures of active compounds can contribute to the synthesis of natural-derived insecticides that are more acceptable by farmers and consumers (Domingues et al., 2020).
Therefore, we conducted bioassay-guided chromatographic fractionations to isolate, purify and characterize grain-protective acetogenin(s) from A. mucosa seeds against the maize weevil, a primary pest of stored corn worldwide. The activity of isolated acetogenin was compared with a diatomaceous earth-based formulation (Insecto®) used as positive control.
Section snippets
Plant material: sources and crude extract preparation procedures
Seeds of A. mucosa were obtained from ripe fruits collected on March 17, 2011 from specimens grown at the ESALQ/USP campus, Piracicaba, São Paulo State, Brazil (22°42′28.5″S; 47°37′59.6″W; altitude: 534 m). A voucher specimen, previously identified by Dr. Heimo Rainer (Department of Systematics and Evolution of Higher Plants, University of Vienna, Vienna, Austria) is deposited under registration number 120985 at the ESA herbarium of the Department of Biological Sciences at ESALQ/USP in
Results
The hexane and hydroalcoholic phases of ethanolic extract prepared from A. mucosa seeds caused similar mortality rates (100% and 94%, respectively, Fig. 1) at the previously estimated LC50 [288.3 mg kg−1 for crude ethanolic extract (Ribeiro et al., 2016)]. The 1H NMR spectra of the hexane fraction showed triglycerides as the major compounds, whereas acetogenins prevailed in the hydroalcoholic partition (Ansante et al., 2015). Thus, the hydroalcoholic phase was selected for further fractionation.
Discussion
Bioassay-guided fractionations of the crude extract from A. mucosa seeds led to the isolation of bis-tetrahydrofuran acetogenin rolliniastatin-1 as a major component from A. mucosa seeds, and our toxicological trials confirmed its potent grain-protective properties. Although phytochemical studies have isolated rolliniastatin-1 from seeds of A. mucosa (Pettit et al., 1987) and from other species of Annonaceae [Rollinia membranacea Triana & Planch (Saez et al., 1993), Ophrypetalum odoratum Diels.
Declaration of competing interest
The authors declare that they have no competing interests or conflict of interest.
Acknowledgments
The authors thank the National Institute of Science and Technology in Biorational Insect Pest Control (INCT-CBIP), the Research Support Foundation of the State of São Paulo (FAPESP, grant 2010/52638-0) and the National Council for Scientific and Technological Development (CNPq, grants 445518/2014-6 and 305377/2019-1) for financial support.
References (50)
- et al.
Secondary metabolites from Neotropical Annonaceae: screening, bioguided fractionation, and toxicity to Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae)
Ind. Crop. Prod.
(2015) - et al.
Six cytotoxic annonaceous acetogenins from Annona squamosa seeds
Food Chem.
(2012) - et al.
Insecticide resistance, mixture potentiation and fitness in populations of the maize weevil (Sitophilus zeamais)
Crop Prot.
(2011) - et al.
Squamocin induce histological and ultrastructural changes in the midgut cells of Anticarsia gemmatalis (Lepidoptera: Noctuidae)
Ecotoxicol. Environ. Saf.
(2018) - et al.
Allyl isothiocyanate actions on populations of Sitophilus zeamais resistant to phosphine: toxicity, emergence inhibition and repellency
J. Stored Prod. Res.
(2016) - et al.
Resistance to DDT and pyrethroids in Brazilian populations of Sitophilus zeamais Motsch. (Coleoptera: Curculionidae)
J. Stored Prod. Res.
(1995) - et al.
Overdispersion: models and estimation
Comput. Stat. Data Anal.
(1998) Total synthesis of (+)-rolliniastatin 1
Tetrahedron Lett.
(1994)Complex I inhibitors as insecticides and acaricides
Biochim. Biophys. Acta
(1998)Survey of insecticide resistance in Mexican populations of maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae)
J. Stored Prod. Res.
(1999)
Phosphine resistance in Brazilian populations of Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae)
J. Stored Prod. Res.
Annona mucosa Jacq. (Annonaceae): a promising source of bioactive compounds against Sitophilus zeamais Mots. (Coleoptera: Curculionidae)
J. Stored Prod. Res.
Kinetic characterization of mitochondrial complex I inhibitors using annonaceous acetogenins
Arch. Biochem. Biophys.
Losses caused by insects, mites and microorganisms
Sistema de Agrotóxicos Fitossanitários - Ministério da Agricultura, Pecuária e Abastecimento, Brazil
Annonaceous acetogenins: recent progress
J. Nat. Prod.
Chemical constituents and insecticidal activity of Rollinia leptopetala (Annonaceae)
Nat. Prod. Comm.
Bioactive compounds of Annona
Annona mucosa (Annonaceae) para o controle de pragas: estudo fitoquímico biomonitorado, síntese de mímicos e desenvolvimento de processos de nanoencapsulação
A review of control methods and resistance mechanisms in stored-product insects
Bull. Entomol. Res.
Produção integrada de anonáceas no Brasil
Rev. Bras. Frutic.
Insecticide resistance and size assortative mating in females of the maize weevil (Sitophilus zeamais)
Pest Manag. Sci.
Are mitochondrial lineages, mitochondrial lysis and respiration rate associated with phosphine susceptibility in the maize weevil Sitophilus zeamais?
Ann. Appl. Biol.
Toxicity of squamocin on Aedes aegypti larvae, its predators and human cells
Pest Manag. Sci.
Half-normal plots and overdispersion
Glim Newsletter
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2022, Crop ProtectionCitation Excerpt :Despite the differences in bioassay procedures, conditions and exposure times, based on the comparison of the LC50 values estimated in the aforementioned studies (variable between 200 and 8,000 ppm) with the one obtained in this study (11.91 ppm), it is possible to verify that P. forficifera is the most sensitive species, among all those tested so far, to the active components of the seed extract of this Annona. Aqueous emulsions prepared from the ethanol extract of A. mucosa seeds are constituted by structurally diversified acetogenins, with the bis-tetrahydrofuran acetogenin rolliniastatin-1 being the major constituent and the potential chemical marker for quality control of the formulations produced (Ribeiro et al., 2020). However, the presence of other compounds considered secondary (i.e., alkaloids) could interact synergistically, increasing the bioactivity levels of this botanical derivative (Ribeiro et al., 2013, 2020).
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