Journal of Plant Research

, Volume 132, Issue 1, pp 81–91 | Cite as

Ontogenic synchronization of Bephratelloides cubensis, Annona macroprophyllata seeds and acetogenins from Annonaceae

  • Claudia Azucena Durán-Ruiz
  • Rocío Cruz-Ortega
  • Alejandro Zaldívar-Riverón
  • Hilda Araceli Zavaleta-Mancera
  • Iván De-la-Cruz-Chacón
  • Alma Rosa González-EsquincaEmail author
Regular Paper


The seeds of Annona macroprophyllata Donn. Sm. contain idioblasts with toxic acetogenins, including laherradurin and rolliniastatin-2, in relatively high proportions. Both metabolites are cataloged as potent insecticides for several species, even so, the wasp Bephratelloides cubensis Ashmead fulfills almost its entire life cycle inside the seeds of this and other annonaceous species, to such a degree, that they constitute a strong selection pressure. In order to document the chemical relationship between the two species, it is reported for the first time in this paper the presence of idioblasts and acetogenins during the ontogenic development of the seeds of A. macroprophyllata, and contrasted with the development of B. cubensis. The results indicate that idioblasts with laherradurin and rolliniastatin-2 acetogenins are formed in the middle stages of the endospermic development, also that both acetogenins are biosynthesized simultaneously, and that their proportion is dependent on the degree of development. The acetogenins are present in high amounts that suppose a sufficient toxic barrier and, in this case, laherradurin is the most abundant (> 1000 µg g dry weight−1). The wasp B. cubensis only emerges from the seeds to copulate and returns for oviposition; its larval phase coincides with the appearance of acetogenins, so it feeds on the acetogenic endosperm. The absence of acetogenins in the tissues and excreta of the insect supposes a metabolization of the molecules, which would explain the tolerance to its toxicity.


Seed borer wasp Endosperm Idioblasts Laherradurin Rolliniastatin-2 



The authors are thankful to the Consejo Nacional de Ciencia y Tecnología (CONACYT), and to the “Posgrado en Ciencias Biológicas”, at Universidad Nacional Autónoma de México (UNAM), and to Simón Morales Rodríguez for the technical assistance at the Scanning Electron Microscopy at Colegio de Postgraduados en Ciencias Agrícolas, México. This research is part of a Ph.D. Thesis lead in the ‘‘Posgrado en Ciencias Biológicas’’, UNAM.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Acuña-Castro W, De la Cruz-Chacón I, González-Esquinca AR (2011) Actividad insecticida de Annona diversifolia frente a Atta mexicana. In: González-Esquinca AR, Luna-Cazáres LM, Gutiérrez-Jiménez J, Schlie-Guzmán A, Vidal-López DG (eds) Anonáceas plantas antiguas, estudios recientes. UNICACH, México, pp 259–273Google Scholar
  2. Ahammadsahib K, Hollingworth R, McGovren J, Hui YH, McLaughlin JL (1993) Mode of action of bullatacin: a potent antitumor and pesticidal Annonaceous acetogenin. Life Sci 53:1113–1120CrossRefGoogle Scholar
  3. Alali F, Liu X, McLaughlin J (1999) Annonaceous acetogenins: recent progress. J Nat Prod 62:504–540CrossRefGoogle Scholar
  4. Alamilla Rojas D, Reyes Trejo B, Sixtos Alonso C (2000) Evaluación de la actividad larvicida de cuatro especies del género Annona mediante el bioensayo de Culex quinquefasciatus Say. In: Memorias del Primer Congreso Nacional de Anonáceas. Universidad Autónoma de Chapingo, pp 75–80Google Scholar
  5. Álvarez Colom O, Neske A, Popich S, Bardón A (2007) Toxic Effects of Annonaceous Acetogenins from Annona cherimolia (Magnoliales: Annonaceae) on Spodoptera frugiperda. J Pest Sci 80:63–67CrossRefGoogle Scholar
  6. Álvarez Colom O, Barrachina I, Ayala I, González M, Moya P, Neske A, Bardon A (2008) Toxic effects of annonaceous acetogenins on Oncopeltus fasciatus. J Pest Sci 81:85–89CrossRefGoogle Scholar
  7. Alvarez Colom O, Salvatore A, Willink E, Ordóñez R, Isla MI, Neske A, Bardón A (2010) Insecticidal, mutagenic and genotoxic evaluation of annonaceous acetogenins. Nat Prod Commun 5:391–394Google Scholar
  8. Anaya-Lang A (2003) Ecología Química. Plaza Valdés, MéxicoGoogle Scholar
  9. Ascencio-Alvarado JI (2012) Evaluación de la actividad insecticida y repelente del extracto obtenido a partir de la semilla de Annona diversifolia (anona) sobre el Zabrotes subfasciatus (gorgojo común del frijol). Dissertation, Universidad de El SalvadorGoogle Scholar
  10. Auger B, Marnet N, Gautier V, Maia-Grondard A, Leprince F, Renard M, Guyot S, Nesi N, Routaboul JM (2010) A detailed survey of seed coat flavonoids in developing seeds of Brassica napus L. J Agric Food Chem 58:6246–6256CrossRefGoogle Scholar
  11. Brechú-Franco AE, Laguna-Hernández G, De-la-Cruz-Chacón I, González-Esquinca AR (2016) In situ histochemical localisation of alkaloids and acetogenins in the endosperm and embryonic axis of Annona macroprophyllata Donn. Sm. seeds during germination. Eur J Histochem 60:2568. CrossRefGoogle Scholar
  12. Brower L (1969) Ecological chemistry. Sci Am 220:22–29CrossRefGoogle Scholar
  13. Castañeda-Vildózola AC, Nava-Díaz J, Váldez-Carrasco C, Ruiz-Montiel L, Vidal-Hernández, Barrios-Matías S (2010) Distribution and host range of Bephratelloides cubensis Ashmead (Hymenoptera: Eurytomidae) in Mexico. Neotrop Entomol 39:1053–1055CrossRefGoogle Scholar
  14. Cavé A, Figadère B, Laurens A, Cortes D (1997) Acetogenins from Annonaceae. Fortschr Chem Org Naturst 70:81–288Google Scholar
  15. Corner E (1949) The annonaceous seed and its four integuments. New Phytol 48:332–364CrossRefGoogle Scholar
  16. Cortés D, Moreno L, Párraga J, Galán A, Cabedo N (2014) Nuevos fármacos inspirados en Annonáceas. Rev Bras de Frutic 36(spe1):22–31. CrossRefGoogle Scholar
  17. De la Cruz Chacón I (2001) Acetogeninas bioactivas de Annona diversifolia Safford. Dissertation, Instituto Tecnológico de Tuxtla GutiérrezGoogle Scholar
  18. Degli-Esposti M, Ghelli A, Ratta M, Cortes D, Estornell E (1994) Natural substances (acetogenins) from the family Annonaceae are powerful inhibitors of mitochondrial NADH dehydrogenase (Complex I). Biochem J 301:61–167CrossRefGoogle Scholar
  19. Genest K (1966) Changes in ergoline alkaloids in seeds during ontogeny of Ipomoea violacea. J Pharm Sci 55:1284–1288CrossRefGoogle Scholar
  20. González M, Tormo J, Bermejo A, Zafra-Polo M, Estorell E, Cortés D (1997) Rollimembrina, a novel acetogenin inhibitor of mammalian mitochondrial complex I. Bioorg Med Chem Lett 7:11131118Google Scholar
  21. González-Coloma A, Guadano A, Inés C, Martínez-Díaz R, Cortes D (2002) Selective action of acetogenin mitochondrial complex I inhibitors. Z Naturforsch 57C:1028–1034CrossRefGoogle Scholar
  22. González-Esquinca AR, Luna-Cazáres LM, Schlie-Guzmán MA, Chacón I, Laguna Hernández G, Flores Breceda S, Montoya Gerardo P (2012) In vitro larvicidal evaluation of Annona muricata L., A. diversifolia Saff. and A. lutescens Saff. extracts against Anastrepha ludens Larvae (Diptera, Tephritidae). Interciencia 4:284–289Google Scholar
  23. González-Esquinca AR, De-La-Cruz-Chacón I, Domínguez-Gutú LM (2015) Dormancy and germination of Annona macroprophyllata (Annonaceae): the importance of the micropylar plug and seed position in the fruits. Bot Sci 93:509–515CrossRefGoogle Scholar
  24. González-Esquinca AR, De-La-Cruz-Chacón I, Castro-Moreno M, Riley-Saldaña CA (2016) Phenological strategies of Annona species from the tropical deciduous forest of Chiapas, Mexico. Bot Sci 94:531–541CrossRefGoogle Scholar
  25. Grissell EE, Schauff ME (1990) A synopsis of the seed-feeding genus Bephratelloides (Chalcidoidea: Eurytomidae). Proc Entomol Soc Wash 92:177–187Google Scholar
  26. Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics software package for education and data analysis. Paleontol Electrón 4:1–9Google Scholar
  27. Hartmann T, Theuring C, Witte L, Pasteels J (2001) Sequestration, metabolism and partial synthesis of tertiary pyrrolizidine alkaloids by the neotropical leaf-beetle Platyphora boucardi. Insect Biochem Mol Biol 31:1041–1056CrossRefGoogle Scholar
  28. Hernández-Fuentes LM, Urias-López MA, Bautista-Martínez N (2010) Biología y hábitos del barrenador de la semilla Bephratelloides cubensis Ashmead (Hymenoptera: Eurytomidae). Neotrop Entomol 39:527–534CrossRefGoogle Scholar
  29. Konno K, Ono H, Nakamura M, Tateishi K, Hirayama C, Tamura Y, Hattori M, Koyama A, Kohno K (2006) Mulberry latex rich in antidiabetic sugar-mimic alkaloids forces dieting on caterpillars. Proc Natl Acad Sci USA 103:1337–1341CrossRefGoogle Scholar
  30. Labeyrie E, Dobler S (2004) Molecular adaptation of Chrysochus leaf beetles to toxic compounds in their food plants. Mol Biol Evol 21:218–221CrossRefGoogle Scholar
  31. Laguna G, Brechú AE, De-la-Cruz-Chacón I, González-Esquinca AR (2015) Histochemical detection of acetogenins and storage molecules in the endosperm of Annona macroprophyllata Donn Sm. seeds. Eur J Histochem 59:2502. Google Scholar
  32. Li XH, Hui YH, Rupprecht JK, Liu YM, Wood KV, Smith DL, Chang CJ, McLaughlin JL (1990) Bullatacin, bullatacinone, and squamone, a new bioactive acetogenin, from the bark of Annona squamosa. J Nat Prod 53:81–86CrossRefGoogle Scholar
  33. Liaw C-C, Liao W-Y, Chen C-S J, S-C Wu, Y-C S, C-N, Wu S-H (2011) The Calcium-Chelating Capability of Tetrahydrofuranic Moieties Modulates the Cytotoxicity of Annonaceous Acetogenins. Angew Chem Int 50:7885–7891CrossRefGoogle Scholar
  34. Liaw C-C, Liou J-R, Wu T-Y, Chang F-R, Wu Y-C (2016) Acetogenins from Annonaceae. Prog Chem Org Nat Prod 101:113–230. CrossRefGoogle Scholar
  35. Luna-Cazáres LM, González-Esquinca AR (2010) Susceptibility of bacteria and complete spheroplasts of Escherichia coli, Pseudomonas aeruginosa and Salmonella typhi to rolliniastatin-2. Nat Prod Res 24:1139–1145CrossRefGoogle Scholar
  36. Marroquín-Andrade L, Cuevas-Sánchez JA, Guerra Ramírez D, Reyes L, Reyes-Chumacero A, Reyes-Trejo B (2011) Proximate composition, mineral nutrient and fatty acids of the seed of ilama, Annona diversifolia Saff. Sci Res Essays 6:3089–3093Google Scholar
  37. Martin J, Madigosky S, Gu Z-M, Zhou D, Wu J, McLaughlin J (1999) Chemical defense in the zebra swallowtail butterfly, Eurytides marcellus, involving annonaceous acetogenins. J Nat Prod 62:2–4CrossRefGoogle Scholar
  38. Nadel H, Peña J (1991) Hosts of Bephratelloides cubensis (Hymenoptera: Eurytomidae) in Florida. Florida Entomol 74:476–479CrossRefGoogle Scholar
  39. Ornosa C, Ortíz-Sánchez FJ (2004) Hymenoptera, Apoidea I. In: Ramos MA et al (eds) Fauna Ibérica. Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, p 556Google Scholar
  40. Peña JE, Glenn H, Baranowski RM (1984) Important insect pests of Annona spp. in Florida. Proc Fla State Hort Soc 97:337–340Google Scholar
  41. Pérez-Amador MC, González Esquinca A, García Argáez A, Bratoeff E, Labastida C (1997) Oil composition and flavonoid profiles of the seeds of three Annona species. Phyton 61:77–80Google Scholar
  42. Reyes-Trejo B, Marroquin L, Peralta M, Navarrete A, Joseph-Nathan P (1997) Laherradurina: Acetogenina activa de Annona diversifolia Safford. In: Memorias del I Congreso Internacional de Anonáceas. Universidad Autónoma Chapingo. Estado de México, Chapingo, p 24Google Scholar
  43. Reyes-Trejo B, Vázquez V, Guerra D, Zuleta H, Reyes L, Sánchez H (2014) Estudio fitoquímico biodirigido de la actividad insecticida de semillas de Annona diversifolia Saff. en larvas de Aedes aegypti L. In: Memorias del VII Congreso Nacional de Anonáceas 2014. Universidad Veracruzana, Xalapa, pp 56–57Google Scholar
  44. Riley-Saldaña CA, Cruz-Ortega MDR, Martínez Vázquez M, De-la-Cruz-Chacón I, Castro-Moreno M, González-Esquinca AR (2017) Acetogenins and alkaloids during the initian development of Annona muricata L. (Annonaceae). Z Naturforsch C.
  45. Rosenthal G (1983) Biochemical adaptations of the bruchid beetle, Caryedes brasiliensis to L-canavanine, a higher plant allelochemical. J Chem Ecol 9:803–815CrossRefGoogle Scholar
  46. Ruiz Hidalgo J, Parellada EA, Bardón A, Vera N, Neske A (2018) Insecticidal activity of Annonaceous acetogenins and their derivates on Spodoptera frugiperda Smith (Lepidoptera:Noctuidae). J Agric Chem Environ 7:105–116Google Scholar
  47. Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, OxfordGoogle Scholar
  48. Schlie-Guzmán MA, García-Carrancá A, González-Esquinca AR (2009) In Vitro and In Vivo antiproliferative activity of laherradurin and cherimolin-2 of Annona diversifolia Saff. Phytother Res 23:1128–1133CrossRefGoogle Scholar
  49. Sharkey MJ, Fernández F (2006) Biología y diversidad de Hymenoptera. In: Fernández F, Sharkey MJ (eds) Introducción a los Hymenoptera de la Región Neotropical, 1st edn. Sociedad Colombiana de Entomología y Universidad Nacional de Colombia, Bogotá, pp 93–108Google Scholar
  50. Stamp N (2003) Out of the quagmire of plant defende hypotheses. Q Rev Biol 78:23–55CrossRefGoogle Scholar
  51. Tolosa D, Álvarez O, Bardón A, Neske A (2012) Insecticidal Effects of Acetogenins from Rollinia occidentalis Seed Extract. Nat Prod Commun 7:1645–1646Google Scholar
  52. Tormo JR, González MC, Cortés D, Stornell E (1999) Kinetic Characterization of mitochondrial complex I inhibitors using annonaceous acetogenins. Arch Biochem Biophys 369:119–126CrossRefGoogle Scholar
  53. Tormo JR, Estornell E, Gallardo T, González MC, Cavé A, Granell S, Cortes D, Zafra-Polo MC (2001) Gamma-lactone-Functionalized antitumoral acetogenins are the most potent inhibitors of mitochondrial complex I. Bioorg Med Chem Lett 11:681–684CrossRefGoogle Scholar
  54. Zhang Y, Ma H, Feng D, Lai X, Chen Z, Xu M, Zhang Z (2012) Induction of detoxification enzymes by quercetin in the silkworm. J Econ Entomol 105:1034–1042CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Claudia Azucena Durán-Ruiz
    • 1
  • Rocío Cruz-Ortega
    • 2
  • Alejandro Zaldívar-Riverón
    • 3
  • Hilda Araceli Zavaleta-Mancera
    • 4
  • Iván De-la-Cruz-Chacón
    • 1
  • Alma Rosa González-Esquinca
    • 1
    Email author
  1. 1.Laboratorio de Fisiología y Química Vegetal, Instituto de Ciencias BiológicasUniversidad de Ciencias y Artes de ChiapasTuxtla GutiérrezMexico
  2. 2.Laboratorio de Alelopatía, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  3. 3.Colección Nacional de Insectos, Departamento de Zoología, Instituto de BiologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  4. 4.Laboratorio de Anatomía e Histoquímica VegetalColegio de Postgraduados en Ciencias AgrícolasTexcocoMexico

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