Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter August 10, 2022

Do Colletotrichum gloeosporioides and Rhizopus stolonifer induce alkaloidal and antifungal responses in Annona muricata seedlings?

  • Christian Anabi Riley-Saldaña , Ivan de-la-Cruz-Chacón , María del Rocío Cruz-Ortega , Marisol Castro-Moreno and Alma Rosa González-Esquinca EMAIL logo

Abstract

The benzylisoquinoline alkaloids of Annona muricata have been isolated, but their physiological or ecological role is unknown. The objective was to explore whether these secondary metabolites are involved in defense against phytopathogenic fungi. To do this, the alkaloidal response of 6-leaf seedlings of A. muricata was analyzed, previously inoculated with Colletotrichum gloeosporioides and Rhizopus stolonifer. Before and after inoculation, alkaloidal extracts of roots, stems, and leaves were obtained, and the antifungal activity was evaluated in vitro. The alkaloids anonaine, reticuline, nornuciferine, assimilobine, and coreximine were identified. C. gloeosporioides caused variable increases in the production of anonaine, reticuline and nornuciferine (10–1200%), while R. stolonifer only stimulated the increase of nornuciferin and anonaine (10%) in the stems and leaves. The alkaloidal extracts of inoculated seedlings increased the antifungal activity, both against the pathogen elicitor and against the second target pathogen. These findings suggest that the alkaloids participate in the antifungal defense mechanism.


Corresponding author: Alma Rosa González-Esquinca, Laboratorio de Fisiología y Química Vegetal, Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas (UNICACH), Libramiento Norte Poniente 1150. Col. Lajas Maciel, CP. 29039, Tuxtla Gutiérrez, Chiapas, Mexico, E-mail:

Award Identifier / Grant number: CONACYT 184108-2013; INFRA2014-01-000226293

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was supported, in part, by a grant from Consejo Nacional de Ciencia y Tecnología (CONACYT 184108-2013; INFRA 2014-01-000226293) from the Mexican Research Council.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

1. Iriti, M, Faoro, F. Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution. Int J Mol Sci 2009;10:3371–99. https://doi.org/10.3390/ijms10083371.Search in Google Scholar PubMed PubMed Central

2. Cavé, A, Figadére, B, Laurens, A, Cortes, D. Acetogenins from Annonaceae. Prog Chem Org Nat Prod 1997;70:81–288.10.1007/978-3-7091-6551-5_2Search in Google Scholar PubMed

3. Guinaudeau, H, Leboeuf, M, Cavé, A. Aporphinoid alkaloids V. J Nat Prod 1998;57:103335.10.1021/np50110a001Search in Google Scholar

4. De-la-Cruz-Chacón, I, González-Esquinca, AR. Liriodenine alkaloid in Annona diversifolia during early development. Nat Prod Res 2012;26:42–9. https://doi.org/10.1080/14786419.2010.533373.Search in Google Scholar PubMed

5. Castro-Moreno, M, Tinoco-Ojangurén, CL, Cruz-Ortega, MR, González-Esquinca, AR. Influence of seasonal variation on the phenology and liriodenine content of Annona lutescens (Annonaceae). J Plant Res 2013;126:529–37. https://doi.org/10.1007/s10265-013-0550-x.Search in Google Scholar PubMed

6. Riley-Saldaña, CA, Cruz-Ortega, MR, Martínez Vázquez, M, De-la-Cruz-Chacón, I, Castro-Moreno, M, González-Esquinca, AR. Acetogenins and alkaloids during the initial development of Annona muricata L. (Annonaceae). Z Naturforsch C J Biosci 2017;26:497–506. https://doi.org/10.1515/znc-2017-0060.Search in Google Scholar PubMed

7. De-la-Cruz-Chacón, I, Riley Saldaña, CA, Arrollo Gómez, S, Sancristóbal Domínguez, TJ, Castro Moreno, M, González Esquinca, AR. Spatio temporal variation of alkaloids in Annona purpurea and the associated influence on their antifungal activity. Chem Biodivers 2019;16:e1800284.10.1002/cbdv.201800284Search in Google Scholar PubMed

8. De-la-Cruz-Chacón, I, González-Esquinca, AR. Activities of enzymes catalyzing benzylisoquinoline alkaloid biosynthesis in Annona diversifolia saff. during early development. Russ J Plant Physiol 2013;60:791–9. https://doi.org/10.1134/s1021443713060034.Search in Google Scholar

9. Puvanendran, S, Wickramasinghe, A, Karunaratne, DN, Carr, G, Wijesundara, DSA, Andersen, R, et al.. Antioxidant constituents from Xylopia championii. Pharm Biol 2008;46:352–5. https://doi.org/10.1080/13880200801887989.Search in Google Scholar

10. Conserva, LM, Araújo, CB, Barbosa-Filho, JM. Alkaloids of the Hernandiaceae: occurrence and a compilation of their biological activities. Alkaloids Chem Biol 2005;62:175–243.10.1016/S1099-4831(05)62003-2Search in Google Scholar PubMed

11. Patiño, OJ, Cuca, LE. Monophyllidin, a new alkaloid L-proline derivative from Zanthoxylum monophyllum. Phytochem Lett 2011;4:22–5. https://doi.org/10.1016/j.phytol.2010.10.002.Search in Google Scholar

12. Tsai, IL, Liou, YF, Lu, ST. Screening of isoquinoline alkaloids and their derivatives for antibacterial and antifungal activies. Gaoxiong Yi Xue Ke Xue Za Zhi 1989;5:132–45.Search in Google Scholar

13. Hufford, CD, Sharma, S, Oguntimein, BO. Antibacterial and antifungal activity of liriodenine and related oxoaporphine. J Pharm Sci 1980;69:1180–3. https://doi.org/10.1002/jps.2600691016.Search in Google Scholar PubMed

14. Khan, MR, Kihara, M, Omoloso, AD. Antimicrobial activity of Michelia champaca. Fitoterapia 2002;69:744–8. https://doi.org/10.1016/s0367-326x(02)00248-4.Search in Google Scholar PubMed

15. Rahman, MM, Lopa, SS, Sadik, G, Islam, R, Khondkar, P, Alam, AK, et al.. Antibacterial and cytotoxic compounds from the bark of Cananga odorata. Fitoterapia 2005;76:758–61. https://doi.org/10.1016/j.fitote.2005.08.011.Search in Google Scholar PubMed

16. Wu, CC, Wu, CL, Huang, SL, Chang, HT. Antifungal activity of liriodenine from Michelia formosana heartwood against wood-rotting fungi. Wood Sci Technol 2012;46:737–47. https://doi.org/10.1007/s00226-011-0428-9.Search in Google Scholar

17. Monteiro, MCM, Leptokarydis, IH, Silva, GH, da Silva, VC, Bolzani, VS, Young, MCM, et al.. Constituintes químicos isolados dos caules de Michelia champaca L. (Magnoliaceae). Eclet Quím 2007;32:13–8. https://doi.org/10.1590/s0100-46702007000300002.Search in Google Scholar

18. Cruz-Chacón, IDL, López-Fernández, NY, Riley-Saldaña, CA, Castro-Moreno, M, González-Esquinca, AR. Antifungal activity in vitro of Sapranthus microcarpus (Annonaceae) against phytopathogens. Acta Bot Mex 2019;126:e1420.10.21829/abm126.2019.1420Search in Google Scholar

19. Hasrat, JA, De Bruyne, T, De Backer, JP, Vauquelin, G, Vlietinck, AJ. Isoquinoline derivatives isolated from the fruit of Annona muricata as 5-HTergic 5-HT1A receptor agonists in rats: unexploited antidepressive (lead) products. J Pharm Pharmacol 1997;11:1145–9. https://doi.org/10.1111/j.2042-7158.1997.tb06058.x.Search in Google Scholar PubMed

20. Lannuzel, A, Patrick, PM, Caparros-Lefebvre, D, Abaul, J, Hocquemiller, R, Ruberg, M. Toxicity of Annonaceae for dopaminergic neurons: potential role in atypical parkinsonism in Guadeloupe. Mov Disord 2002;17:84–90. https://doi.org/10.1002/mds.1246.Search in Google Scholar PubMed

21. Leboeuf, M, Cavé, A, Bhaumik, PK, Mukherjee, B, Mukherjee, R. The phytochemistry of the Annonaceae. Phytochemistry 1982;21:2783–813. https://doi.org/10.1016/0031-9422(80)85046-1.Search in Google Scholar

22. Fofana, S, Keita, A, Balde, S, Ziyaev, R, Aripova, SF. Alkaloids from leaves of Annona muricata. Chem Nat Compd 2012;48:714. https://doi.org/10.1007/s10600-012-0363-5.Search in Google Scholar

23. Matsushige, A, Kotake, Y, Matsunami, K, Otsuka, H, Ohta, S, Takeda, Y. Annonamine, a new aporphine alkaloid from the leaves of Annona muricata. Chem Pharm Bull 2012;60:257–9. https://doi.org/10.1248/cpb.60.257.Search in Google Scholar PubMed

24. Riley-Saldaña, CA. Metabolitos constitutivos e inducidos de Annona muricata L. [Ph.D. thesis]. Ciudad de México, México: Universidad Nacional Autónoma de México; 2019.Search in Google Scholar

25. Feeny, P. Plant apparency and chemical defense. In: Wallace, JW, Mansell, RL, editors. Biochemical interaction between plants and insects. Recent advances in phytochemistry. Boston, MA: Springer; 1976, vol 10.10.1007/978-1-4684-2646-5_1Search in Google Scholar

26. Rhoades, DF, Cates, RG. Toward a general theory of plant antiherbivore chemistry. In: Wallace, JW, Mansell, RL, editors. Biochemical interaction between plants and insects. Recent advances in phytochemistry. Boston, MA: Springer; 1976, vol 10.10.1007/978-1-4684-2646-5_4Search in Google Scholar

27. Ministry of Agriculture. Reglas Internacionales para Ensayos de Semillas. México: Instituto. Nacional de Semillas y plantas de vivero. Dirección General de la Producción Agraria, reimpreso por la SARH; 1976.Search in Google Scholar

28. González, EAR. Contribución al estudio del género Annona (Annonaceae). Análisis fitoquímico de tres especies del estado de Chiapas [Ph.D. thesis]. Distrito Federal, México: Universidad Nacional Autónoma de México; 2001.Search in Google Scholar

29. Agostini, JP, Timmer, LW, Mitchell, DJ. Morphological and pathological characteristics of strains of Colletotrichum gloeosporioides from citrus. Phytopathology 1992;82:1377–82. https://doi.org/10.1094/phyto-82-1377.Search in Google Scholar

30. Álvarez, E, Ospina, CA, Mejía, JF, Llano, GA. Caracterización morfológica, patogénica del agente causal de la antracnosis (Colletotrichum gloeosporioides) en guanábana (Annona muricata L.) en el Valle de Cauca. Fitopatol Colomb 2000;28:1–8.Search in Google Scholar

31. Mafacioli, R, Tessmann, DJ, Santos, ÁFD, Vida, JB. Caracterização morfo-fisiológica e patogenicidade de Colletotrichum gloeosporioides da pupunheira. Summa Phytopathol 2006;32:113–7. https://doi.org/10.1590/s0100-54052006000200003.Search in Google Scholar

32. Villanueva-Arce, R, Yáñez-Morales, MDJ, Hernández-Anguiano, AM. Especies de Colletotrichum en chirimoya (Annona cherimola Mill). Agrociencia 2008;42:689–701.Search in Google Scholar

33. Amini, J, Sidovich, D. The effects of fungicides on Fusarium oxysporum f. sp. lycopersici associated with Fusarium wilt of tomato. J Plant Protect Res 2010;50:172–8. https://doi.org/10.2478/v10045-010-0029-x.Search in Google Scholar

34. Stamp, N. Out of the quagmire of plant defense hypotheses. Q Rev Biol 2003;78:23–55. https://doi.org/10.1086/367580.Search in Google Scholar PubMed

35. Cline, SD, Coscia, CJ. Stimulation of sanguinarine production by combined fungal elicitation and hormonal deprivation in cell suspension cultures of Papaver bracteatum. Plant Physiol 1988;86:161–5. https://doi.org/10.1104/pp.86.1.161.Search in Google Scholar PubMed PubMed Central

36. Saunders, J, O’Neill, N. The characterization of defense responses to fungal infection in alfalfa. BioControl 2004;49:715–28. https://doi.org/10.1007/s10526-004-5281-4.Search in Google Scholar

37. Jasiński, M, Kachlicki, P, Rodziewicz, P, Figlerowicz, M, Stobiecki, M. Changes in the profile of flavonoid accumulation in Medicago truncatula leaves during infection with fungal pathogen Phoma medicaginis. Plant Physiol Biochem 2009;47:847–53. https://doi.org/10.1016/j.plaphy.2009.05.004.Search in Google Scholar PubMed

38. Muth, D, Kachlicki, P, Krajewski, P, Przystalski, M, Stobiecki, M. Differential metabolic response of narrow leafed lupine (Lupinus angustifolius) leaves to infection with Colletotrichum lupini. Metabolomics 2009;5:354–62. https://doi.org/10.1007/s11306-009-0162-6.Search in Google Scholar

39. Pedras, MSC, Zheng, QA, Gadagi, RS, Rimmer, SR. Phytoalexins and polar metabolites from the oil seeds canola and rapeseed: differential metabolic responses to the biotroph Albugo candida and to abiotic stress. Phytochemistry 2008;69:894–910. https://doi.org/10.1016/j.phytochem.2007.10.019.Search in Google Scholar PubMed

40. El Oirdi, M, Trapani, A, Bouarab, K. The nature of tobacco resistance against Botrytis cinerea depends on the infection structures of the pathogen. Environ Microbiol 2010;12:239–53. https://doi.org/10.1111/j.1462-2920.2009.02063.x.Search in Google Scholar PubMed

41. Perrone, ST, McDonald, KL, Sutherland, MW, Guest, DI. Superoxide release is necessary for phytoalexin accumulation in Nicotiana tabacum cells during the expression of cultivar-race and non-host resistance towards Phytophthora spp. Physiol Mol Plant Pathol 2003;62:127–35. https://doi.org/10.1016/s0885-5765(03)00026-2.Search in Google Scholar

42. Egydio-Brandão, APM, Novaes, P, Santos, DYAC. Alkaloids from Annona: review from 2005 to 2016. Biochem Mol Biol 2017;4:1031.Search in Google Scholar

43. Afek, U, Sztejnberg, A, Carmely, S. 6, 7–Dimethoxycoumarin, a citrus phytoalexin conferring resistance against Phytophthora gummosis. Phytochemistry 1986;25:1855–6. https://doi.org/10.1016/s0031-9422(00)81162-0.Search in Google Scholar

Received: 2021-11-11
Accepted: 2022-07-15
Published Online: 2022-08-10
Published in Print: 2023-01-27

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 15.5.2024 from https://www.degruyter.com/document/doi/10.1515/znc-2021-0297/html
Scroll to top button