Skip to main content
Log in

Ontogenetic Changes in Azoxyglycoside Levels in the Leaves of Dioon edule Lindl

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Plants have multiple strategies, including phytochemicals that protect their vulnerable tissues against pathogens and herbivores. Dioon edule, like all cycads, possess unique azoxy-type compounds, azoxyglycosides (AZGs) as a chemical defense; however, the ontogenetic variability of these compounds in this long-lived cycad is unknown. Here, we investigated the effects of plant age, sex, genotype and individual heterozygosity on AZG levels in mature leaves of wild D. edule populations from eastern Mexico. Individuals were divided into three ontogenetic stages: seedlings, juveniles and adults. We established overall leaf quality by quantifying pigments associated with photosynthesis; chlorophylla, chlorophyllb and lutein. Leaf chlorophylla levels were higher in seedlings compared to adult cycads. Plants were genotyped using 11 microsatellite markers and foliar AZG levels were quantified by HPLC. AZG levels do not correlate with plant genotype or the individual’s heterozygosity. Genetic analysis identified a distinction between lowland and highland individuals; foliar AZG levels were higher in lowland adult cycads compared to highland individuals. In both populations, the highest AZG levels were found in seedlings compared to adult cycads. These young cycads are highly reliant on their few leaves since seedlings bear one or two leaves for the first years of their life and, thus, are unlikely to recover from defoliation. The results suggest that cycad leaves with a greater nutritive content and a higher value for long-term survival are better protected with higher AZG levels. Female adult cycads have higher AZG levels compared to males, suggesting that the benefits of defense could also be linked to reproductive costs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baroli I, Niyogi KK (2000) Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philos Trans R Soc 355:1385–1394

    Article  CAS  Google Scholar 

  • Bello-Bedoy R, Núñez-Farfán J (2011) The effect of inbreeding on defence against multiple enemies in Datura stramonium. J Evol Biol 24:518–530

    Article  CAS  PubMed  Google Scholar 

  • Boecklen WJ, Hoffman MT (1993) Sex-biased herbivory in Ephedra trifurca: the importance of sex-by-environment interactions. Oecologia 96:49–55

    Article  Google Scholar 

  • Boege K (2005) Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia 143:117–125

    Article  PubMed  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Bowers MD, Larin Z (1989) Acquired chemical defense in the lycaenid butterfly, Eumaeus atala. J Chem Ecol 15:1133–1146

    Article  CAS  PubMed  Google Scholar 

  • Bowers MD, Stamp NE (1993) Effects of plant age, genotype and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791

    Article  Google Scholar 

  • Castillo-Guevara C, Rico-Gray V (2003) The role of macrozamin and cycasin in cycads (Cycadales) as antiherbivore defenses. J Torrey Bot Soc 130:206–217

    Article  Google Scholar 

  • Clark DB, Clark DA (1988) Leaf production and the cost of reproduction in the Neotropical rain forest cycad, Zamia skinneri. J Ecol 76:1153–1163

    Article  Google Scholar 

  • Clark DB, Clark DA (1991) Herbivores, herbivory, and plant phenology: Patterns and consequences in a tropical rain-forest cycad. In: Price PW, Lewinsohn TM, Wilson-Fernandes G, Benson WW (eds) Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. John Wiley & Sons, New York, pp. 209–255

    Google Scholar 

  • Claydon N (1978) Insecticidal secondary metabolites from entomogenous fungi: Entomophthora virulenta. J Invertebr Pathol 32:319–324

    Article  CAS  Google Scholar 

  • Deevey E (1947) Life tables for natural populations of animals. Q Rev Biol 22:283–314

    Article  PubMed  Google Scholar 

  • Ding L, Ndejouong BLST, Maier A, Fiebig H-H, Hertweck C (2012) Elaiomycins D–F, antimicrobial and cytotoxic azoxides from Streptomyces sp. strain HKI0708. J Nat Prod 75:1729–1734

    Article  CAS  PubMed  Google Scholar 

  • Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930

    Article  Google Scholar 

  • Dominy NJ, Lucas PW, Wright SJ (2003) Mechanics and chemistry of rain forest leaves: Canopy and understory compared. J Ex Bot 54:2007–2014

    Article  CAS  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Erelli MC, Ayres MP, Eaton GK (1998) Altitudinal patterns in host suitability for forest insects. Oecologia 117:133–142

    Article  Google Scholar 

  • González-Astorga J, Vovides A, Ferrer M, Iglesias C (2003) Population genetics of Dioon edule Lindl. (Zamiaceae, Cycadales): Biogeographical and evolutionary implications. Biol J Linn Soc 80:457–467

    Article  Google Scholar 

  • Goodger JQ, Ades PK, Woodrow IE (2004) Cyanogenesis in Eucalyptus polyanthemos seedlings: heritability, ontogeny and effect of soil nitrogen. Tree Physiol 24:681–688

    Article  PubMed  Google Scholar 

  • Jing SW, Coley PD (1990) Dioecy and herbivory: the effect of growth rate on plant defense in Acer negundo. Oikos 58:369–377

    Article  Google Scholar 

  • Jing J, Hong J, Shuquan Y, Guomo Z (2008) Sex-linked photosynthetic physiologic research and the evolutionary ecological analysis in living fossil plant, Ginkgo biloba L. Acta Ecol Sin 28:1128–1136

    Article  Google Scholar 

  • Johnson M, Smith S, Rausher M (2009) Plant sex and the evolution of plant defenses against herbivores. Proc Natl Acad Sci U S A 106

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Kariyat RR, Balogh CM, Moraski RP, De Moraes CM, Mescher MC, Stephenson AG (2013) Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae. Am J Bot 100:1014–1021

    Article  PubMed  Google Scholar 

  • Kaufman L, Rousseeuw PJ (2009) Finding groups in data: An introduction to cluster analysis. John Wiley & Sons, New York

    Google Scholar 

  • Laqueur GL, Spatz M (1968) Toxicology of cycasin. Cancer Res 28:2262–2267

    CAS  PubMed  Google Scholar 

  • Liu Y-J, Tong Y-P, Zhu Y-G, Ding H, Smith FA (2006) Leaf chlorophyll readings as an indicator for spinach yield and nutritional quality with different nitrogen fertilizer applications. J Plant Nutr 29:1207–1217

    Article  CAS  Google Scholar 

  • Lloyd DG, Webb C (1977) Secondary sex characters in plants. Bot Rev 43:177–216

    Article  Google Scholar 

  • Matsushima T, Matsumoto H, Shirai A, Sawamura M, Sugimura T (1979) Mutagenicity of the naturally occurring carcinogen cycasin and synthetic methylazoxymethanol conjugates in Salmonella typhimurium. Cancer Res 39:3780–3782

    CAS  PubMed  Google Scholar 

  • Mora R, Yáñez-Espinosa L, Flores J, Nava-Zárate N (2013) Strobilus and seed production of Dioon edule (Zamiaceae) in a population with low seedling density in San Luis Potosí, Mexico. Trop Conserv Sci 6:268–282

    Article  Google Scholar 

  • Moynihan J, Meerow AW, Francisco-Ortega J (2007) Isolation, characterization and cross-species amplification of microsatellite loci in the cycad genus Dioon (Zamiaceae). Potential utilization in population genetic studies of Dioon edule. Mol Ecol 7:72–74

    Article  CAS  Google Scholar 

  • Norstog KJ, Nicholls TJ (1997) The biology of the Cycads. Cornell University Press, New York

    Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348

    Article  Google Scholar 

  • Ornduff R (1987) Sex ratios and coning frequency of the cycad Zamia pumila L.(Zamiaceae) in the Dominican Republic. Biotropica 19:361–364

    Article  Google Scholar 

  • Prado A, Ledezma J, Cubilla-Rios L, Bede JC, Windsor D (2011) Two genera of Aulacoscelinae beetles reflexively bleed azoxyglycosides found in their host cycads. J Chem Ecol 37:736–740

    Article  CAS  PubMed  Google Scholar 

  • Prado A, Sierra A, Windsor D, Bede JC (2014) Leaf traits and herbivory levels in a tropical gymnosperm, Zamia stevensonii (Zamiaceae). Am J Bot 101:437–447

    Article  PubMed  Google Scholar 

  • Prado A, Cervantes-Díaz F, Perez-Zavala FG, González-Astorga J, Bede JC, Cibrián-Jaramillo A (2016) Transcriptome-derived microsatellite markers for Dioon (Zamiaceae) cycad species. Appl Plant Sci 4

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puig H (1976) Végétation de la Huasteca, Mexique. Mission Archeologique et Ethnologique Français au Mexique, México

    Google Scholar 

  • Rasmann S, Pellissier L, Defossez E, Jactel H, Kunstler G (2014) Climate-driven change in plant–insect interactions along elevation gradients. Funct Ecol 28:46–54

    Article  Google Scholar 

  • Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. Recent Adv Phytochem 10:168–213

    CAS  Google Scholar 

  • Rubio-Méndez G (2010) Estructura poblacional de Dioon edule Lindl. (Zamiaceae) en la Sierra Madre Oriental del Estado de San Luís Potosí. Thesis. Universidad Autónoma de San Luís Potosí.

  • Schappert PJ, Shore JS (2000) Cyanogenesis in Turnera ulmifolia L.(Turneraceae): II. Developmental expression, heritability and cost of cyanogenesis. Evol Ecol Res 2:337–352

    Google Scholar 

  • Schoonhoven LM, Van Loon JJ, Dicke M (2005) Insect-plant biology:. Oxford University Press, Oxford

    Google Scholar 

  • Seguin P, Tremblay G, Pageau D, Liu W, Turcotte P (2011) Soybean lutein concentration: impact of crop management and genotypes. Crop Sci 51:1151–1160

    Article  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  Google Scholar 

  • Teas HJ, Dyson JG (1967) Mutation in Drosophila by methylazoxymethanol, the aglycone of cycasin. Proc Soc Exp Biol Med 125:998–990

    Article  Google Scholar 

  • Teas HJ, Dyson JG, Whisenant BR (1966) Cycasin metabolism in Seirarctia echo Abbot and Smith (Lepidoptera: Arctiidae). J GA. Entomol Soc 1:21–22

    Google Scholar 

  • van Dam NM, Horn M, Mareš M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568

    Article  PubMed  Google Scholar 

  • Vovides AP (1990) Spatial distribution, survival, and fecundity of Dioon edule (Zamiaceae) in a tropical deciduous forest in Veracruz, Mexico, with notes on its habitat. Am J Bot 77:1532–1543

  • Wardlaw IF (1990) Tansley review no. 27. The control of carbon partitioning in plants. New Phytol 116:341–381

    Article  CAS  Google Scholar 

  • Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215

    Article  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophyll a and b, as well as total carotenoids, using various solvents with spectrophotometer of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Whitelock L (2004) Variation in the Mexican cycad Dioon edule (Zamiaceae). Bot Rev 70:240–249

    Article  Google Scholar 

  • Wimp G, Wooley S, Bangert R, Young W, Martinsen G, Keim P, Rehill B, Lindroth R, Whitham T (2007) Plant genetics predicts intra-annual variation in phytochemistry and arthropod community structure. Mol Ecol 16:5057–5069

    Article  CAS  PubMed  Google Scholar 

  • Yagi F (2004) Azoxyglycoside content and [beta]-glycosidase activities in leaves of various cycads. Phytochemistry 65:3243–3247

    Article  CAS  PubMed  Google Scholar 

  • Yáñez-Espinosa L, Flores J, Rodríguez-Millan PS, Rubio-Méndez G (2014) Influence of germination date on Dioon edule (Zamiaceae) seedling tolerance to water stress. J Plant Res 127:413–422

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Marc Hersh, Gabriel Gálvez, Andrés Everaert and Hugo Lagarto Castillo for assistance in the field and the laboratory. We thank Don Windsor for mentorship and two anonymous reviewers for beneficial comments. This research was funded through the Consejo Nacional de Ciencia y Tecnología (Mexico) (AP, GR-M and LY-E) and the Natural Sciences and Engineering Research Council of Canada (JCB).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jacqueline C. Bede.

Electronic supplementary material

Supplemental Figure 1

(DOCX 2080 kb)

Supplemental Figure 2

(DOCX 341 kb)

Supplemental Table 1

(DOCX 36 kb)

Supplemental Table 2

(DOCX 61 kb)

Supplemental Table 3

(DOCX 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prado, A., Rubio-Mendez, G., Yañez-Espinosa, L. et al. Ontogenetic Changes in Azoxyglycoside Levels in the Leaves of Dioon edule Lindl. J Chem Ecol 42, 1142–1150 (2016). https://doi.org/10.1007/s10886-016-0774-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-016-0774-z

Keywords

Navigation