Advertisement

Journal of Chemical Ecology

, Volume 42, Issue 11, pp 1142–1150 | Cite as

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

  • Alberto Prado
  • Gabriel Rubio-Mendez
  • Laura Yañez-Espinosa
  • Jacqueline C. BedeEmail author
Article

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.

Keywords

Azoxyglycosides Dioon edule Heterozygosity Ontogeny Specialized metabolism 

Notes

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).

Supplementary material

10886_2016_774_MOESM1_ESM.docx (2 mb)
Supplemental Figure 1 (DOCX 2080 kb)
10886_2016_774_MOESM2_ESM.docx (342 kb)
Supplemental Figure 2 (DOCX 341 kb)
10886_2016_774_MOESM3_ESM.docx (36 kb)
Supplemental Table 1 (DOCX 36 kb)
10886_2016_774_MOESM4_ESM.docx (61 kb)
Supplemental Table 2 (DOCX 61 kb)
10886_2016_774_MOESM5_ESM.docx (40 kb)
Supplemental Table 3 (DOCX 39 kb)

References

  1. Baroli I, Niyogi KK (2000) Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philos Trans R Soc 355:1385–1394CrossRefGoogle Scholar
  2. Bello-Bedoy R, Núñez-Farfán J (2011) The effect of inbreeding on defence against multiple enemies in Datura stramonium. J Evol Biol 24:518–530CrossRefPubMedGoogle Scholar
  3. Boecklen WJ, Hoffman MT (1993) Sex-biased herbivory in Ephedra trifurca: the importance of sex-by-environment interactions. Oecologia 96:49–55CrossRefGoogle Scholar
  4. Boege K (2005) Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia 143:117–125CrossRefPubMedGoogle Scholar
  5. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448CrossRefPubMedGoogle Scholar
  6. Bowers MD, Larin Z (1989) Acquired chemical defense in the lycaenid butterfly, Eumaeus atala. J Chem Ecol 15:1133–1146CrossRefPubMedGoogle Scholar
  7. Bowers MD, Stamp NE (1993) Effects of plant age, genotype and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791CrossRefGoogle Scholar
  8. Castillo-Guevara C, Rico-Gray V (2003) The role of macrozamin and cycasin in cycads (Cycadales) as antiherbivore defenses. J Torrey Bot Soc 130:206–217CrossRefGoogle Scholar
  9. Clark DB, Clark DA (1988) Leaf production and the cost of reproduction in the Neotropical rain forest cycad, Zamia skinneri. J Ecol 76:1153–1163CrossRefGoogle Scholar
  10. 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. 209–255Google Scholar
  11. Claydon N (1978) Insecticidal secondary metabolites from entomogenous fungi: Entomophthora virulenta. J Invertebr Pathol 32:319–324CrossRefGoogle Scholar
  12. Deevey E (1947) Life tables for natural populations of animals. Q Rev Biol 22:283–314CrossRefPubMedGoogle Scholar
  13. 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 75:1729–1734CrossRefPubMedGoogle Scholar
  14. Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930CrossRefGoogle Scholar
  15. Dominy NJ, Lucas PW, Wright SJ (2003) Mechanics and chemistry of rain forest leaves: Canopy and understory compared. J Ex Bot 54:2007–2014CrossRefGoogle Scholar
  16. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  17. Erelli MC, Ayres MP, Eaton GK (1998) Altitudinal patterns in host suitability for forest insects. Oecologia 117:133–142CrossRefGoogle Scholar
  18. 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 80:457–467CrossRefGoogle Scholar
  19. Goodger JQ, Ades PK, Woodrow IE (2004) Cyanogenesis in Eucalyptus polyanthemos seedlings: heritability, ontogeny and effect of soil nitrogen. Tree Physiol 24:681–688CrossRefPubMedGoogle Scholar
  20. Jing SW, Coley PD (1990) Dioecy and herbivory: the effect of growth rate on plant defense in Acer negundo. Oikos 58:369–377CrossRefGoogle Scholar
  21. 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 28:1128–1136CrossRefGoogle Scholar
  22. Johnson M, Smith S, Rausher M (2009) Plant sex and the evolution of plant defenses against herbivores. Proc Natl Acad Sci U S A 106Google Scholar
  23. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefPubMedGoogle Scholar
  24. 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 100:1014–1021CrossRefPubMedGoogle Scholar
  25. Kaufman L, Rousseeuw PJ (2009) Finding groups in data: An introduction to cluster analysis. John Wiley & Sons, New YorkGoogle Scholar
  26. Laqueur GL, Spatz M (1968) Toxicology of cycasin. Cancer Res 28:2262–2267PubMedGoogle Scholar
  27. 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 29:1207–1217CrossRefGoogle Scholar
  28. Lloyd DG, Webb C (1977) Secondary sex characters in plants. Bot Rev 43:177–216CrossRefGoogle Scholar
  29. 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 39:3780–3782PubMedGoogle Scholar
  30. 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 6:268–282CrossRefGoogle Scholar
  31. 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 7:72–74CrossRefGoogle Scholar
  32. Norstog KJ, Nicholls TJ (1997) The biology of the Cycads. Cornell University Press, New YorkGoogle Scholar
  33. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  34. Ornduff R (1987) Sex ratios and coning frequency of the cycad Zamia pumila L.(Zamiaceae) in the Dominican Republic. Biotropica 19:361–364CrossRefGoogle Scholar
  35. 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 37:736–740CrossRefPubMedGoogle Scholar
  36. Prado A, Sierra A, Windsor D, Bede JC (2014) Leaf traits and herbivory levels in a tropical gymnosperm, Zamia stevensonii (Zamiaceae). Am J Bot 101:437–447CrossRefPubMedGoogle Scholar
  37. 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 4Google Scholar
  38. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  39. Puig H (1976) Végétation de la Huasteca, Mexique. Mission Archeologique et Ethnologique Français au Mexique, MéxicoGoogle Scholar
  40. Rasmann S, Pellissier L, Defossez E, Jactel H, Kunstler G (2014) Climate-driven change in plant–insect interactions along elevation gradients. Funct Ecol 28:46–54CrossRefGoogle Scholar
  41. Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. Recent Adv Phytochem 10:168–213Google Scholar
  42. 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.Google Scholar
  43. Schappert PJ, Shore JS (2000) Cyanogenesis in Turnera ulmifolia L.(Turneraceae): II. Developmental expression, heritability and cost of cyanogenesis. Evol Ecol Res 2:337–352Google Scholar
  44. Schoonhoven LM, Van Loon JJ, Dicke M (2005) Insect-plant biology:. Oxford University Press, OxfordGoogle Scholar
  45. Seguin P, Tremblay G, Pageau D, Liu W, Turcotte P (2011) Soybean lutein concentration: impact of crop management and genotypes. Crop Sci 51:1151–1160CrossRefGoogle Scholar
  46. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573CrossRefPubMedGoogle Scholar
  47. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55CrossRefPubMedGoogle Scholar
  48. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285CrossRefGoogle Scholar
  49. Teas HJ, Dyson JG (1967) Mutation in Drosophila by methylazoxymethanol, the aglycone of cycasin. Proc Soc Exp Biol Med 125:998–990CrossRefGoogle Scholar
  50. Teas HJ, Dyson JG, Whisenant BR (1966) Cycasin metabolism in Seirarctia echo Abbot and Smith (Lepidoptera: Arctiidae). J GA. Entomol Soc 1:21–22Google Scholar
  51. van Dam NM, Horn M, Mareš M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568CrossRefPubMedGoogle Scholar
  52. 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 77:1532–1543Google Scholar
  53. Wardlaw IF (1990) Tansley review no. 27. The control of carbon partitioning in plants. New Phytol 116:341–381CrossRefGoogle Scholar
  54. Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215CrossRefGoogle Scholar
  55. 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 144:307–313CrossRefGoogle Scholar
  56. Whitelock L (2004) Variation in the Mexican cycad Dioon edule (Zamiaceae). Bot Rev 70:240–249CrossRefGoogle Scholar
  57. 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 16:5057–5069CrossRefPubMedGoogle Scholar
  58. Yagi F (2004) Azoxyglycoside content and [beta]-glycosidase activities in leaves of various cycads. Phytochemistry 65:3243–3247CrossRefPubMedGoogle Scholar
  59. 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 127:413–422CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Alberto Prado
    • 1
  • Gabriel Rubio-Mendez
    • 2
  • Laura Yañez-Espinosa
    • 2
  • Jacqueline C. Bede
    • 1
    Email author
  1. 1.Department of Plant ScienceMcGill UniversityAnne de BellevueCanada
  2. 2.Instituto de Investigación en Zonas DesérticasUniversidad Autónoma de San Luis PotosíSan Luis PotosíMexico

Personalised recommendations