Steryl glucoside concentration declines with Cycas micronesica seed age
Thomas E. Marler A C , Vivian Lee B , J. Chung B and Christopher A. Shaw BA CNAS-AES, University of Guam, UOG Station, Mangilao, GU 96923, USA.
B Department of Ophthalmology, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4.
C Corresponding author. Email: tmarler@uog.edu
Functional Plant Biology 33(9) 857-862 https://doi.org/10.1071/FP05321
Submitted: 23 December 2005 Accepted: 22 May 2006 Published: 1 September 2006
Abstract
Neurotoxins contained in the seeds of Cycas micronesica K.D. Hill have been implicated in the Guam neurological disease cluster, amyotrophic lateral sclerosis–parkinsonism dementia complex (ALS–PDC). Some of these neurotoxins remain in the washed cycad seed flour that was historically an important part of the Chamorro diet. Of these, variant steryl glucosides have been identified by us as a possible etiological factor in the disease. In vitro and in vivo animal studies have strongly supported a role for these molecules in some forms of neurodegeneration. As part of a series of studies, we have now determined the concentrations of several steryl glucosides and their sterol precursors as affected by the age of C. micronesica seeds. The concentration of these molecules declined with seed age from 2.0 to 30.5 months. Following log-transformation of both axes, the decline was linear. Similarly, concentration of all but one of the molecules declined with age when samples were restricted to gametophyte tissue. Factors suspected of influencing phenotypic plasticity must be addressed when interpreting plant physiology data. Our results confirm for the first time that tissue age must be documented and reported in cycad seed biochemistry studies to remove ambiguities from results. Past studies in this important area of research have failed to account for the potential impact of seed age, rendering previous outcomes and interpretations of cycad neurotoxins in their impact on ALS–PDC ambiguous.
Keywords: ALS–PDC, cycad, Cycas micronesica, neurotoxin, seed age, sterol, steryl glucoside.
Acknowledgments
We thank N Dongol for field assistance. Support provided by USDA CSREES Tropical and Subtropical Agricultural Research Grants Program (Project 2003-05495) to TEM and USA Army Medical and Materiel Command (DAMD17-02-1-0678), NSERC Canada, and Scottish Rite Charitable Foundation of Canada to CAS.
Banack SA, Cox PA
(2003) Distribution of the neurotoxic nonprotein amino acid BMAA in Cycas micronesica. Botanical Journal of the Linnean Society 143, 165–168.
| Crossref | GoogleScholarGoogle Scholar |
Cantatore JL,
Murphy SM, Lynch DV
(2000) Compartmentation and topology of glucosylceramide synthesis. Biochemical Society Transactions 28, 748–750.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dastur DK
(1964) Cycad toxicity in monkeys: clinical, pathological, and biochemical aspects. Federation Proceedings 23, 1368–1369.
| PubMed |
He J-X,
Fujiko S,
Li T-C,
Kang SG,
Seto H,
Takatsuto S,
Yoshida S, Jang J-C
(2003) Sterols regulate development and gene expression in Arabidopsis. Plant Physiology 131, 1258–1269.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Khabazian I,
Bains JS,
Williams DE,
Cheung J, Wilson JMB , et al.
(2002) Isolation of various forms of sterol β-d-glucoside from the seed of Cycas circinalis: neurotoxicity and implications for ALS–PDC. Journal of Neurochemistry 82, 516–528.
| Crossref | d-glucoside from the seed of Cycas circinalis: neurotoxicity and implications for ALS–PDC.&journal=Journal of Neurochemistry&volume=82&pages=516-528&publication_year=2002&author=JMB%20Wilson&hl=en&doi=10.1046/j.1471-4159.2002.00976.x" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |
Kim Y-K,
Wang Y,
Liu Z-M, Kolattukudy PE
(2002) Identification of a hard surface contact-induced gene in Colletotrichum gloeosporioides conidia as a sterol glycosyl transferase, a novel fungal virulence factor. The Plant Journal 30, 177–187.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kunimoto S,
Murofushi W,
Kai H,
Ishida Y,
Uchiyama A,
Kobayashi T,
Kobayashi S,
Murofushi H, Murakami-Murofushi K
(2002) Steryl glucoside is a lipid mediator in stress-responsive signal transduction. Cell Structure and Function 27, 157–162.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kurland LT
(1988) Amyotrophic lateral sclerosis and Parkinson’s disease complex on Guam linked to an environmental toxin. Trends in Neurosciences 11, 51–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ly PTT,
Liang XB,
Wang Q,
Andreasson K, Shaw CA
(2006) The neurotoxic effects of β-sitosterol glucosides in NSC 34 cells, a mouse motor neuron-derived cell line. Society for Neuroscience Abstracts in press ,
Marler TE,
Lee V, Shaw CA
(2005a) Cycad toxins and neurological diseases in Guam: defining theoretical and experimental standards for correlating human disease with environmental toxins. HortScience 40, 1598–1606.
Marler TE,
Lee V, Shaw CA
(2005b) Spatial variation of steryl glucosides in Cycas micronesica plants: within- and among-plant sampling procedures. HortScience 40, 1607–1611.
Peng L,
Kawagoe Y,
Hogan P, Delmer D
(2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295, 147–150.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sakaki T,
Zähringer U,
Warnecke DC,
Fahl A,
Knogge W, Heinz E
(2001) Sterol glycosides and cerebrosides accumulate in Pichia pastoris, Rhynchosporium secalis and other fungi under normal conditions or under heat shock and ethanol stress. Yeast 18, 679–695.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shaw CA,
Wilson JMB,
Cruz-Aguado R,
Singh S,
Hawkes EL,
Lee V, Marler T
(2006) Cycad-induced neurodegeneration in a mouse model of ALS–PDC: is the culprit really BMAA or is a novel toxin to blame? Botanical Review in press ,
Whiting MG
(1963) Toxicity of cycads. Economic Botany 17, 270–302.
Wilson JMB,
Tabata RC, Shaw CA
(2006) In vivo sterol glucoside neurotoxicity: implications for ALS–PDC and ALS. Society of Neuroscience Abstracts in press ,
Wright SD, McConnaughay KDM
(2002) Interpreting phenotypic plasticity: the importance of ontogeny. Plant Species Biology 17, 119–131.
| Crossref | GoogleScholarGoogle Scholar |
Yagi F
(2004) Azoxyglycoside content and β-glycosidase activities in leaves of various cycads. Phytochemistry 65, 3243–3247.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang ZX,
Andersen DW,
Mantel N, Roman GC
(1996) Motor neuron disease on Guam: geographic and familial occurrence, 1956–85. Acta Neurologica Scandinavica 94, 51–59.
| PubMed |
Zotz G
(2000) Size-related intraspecific variability in physiological traits of vascular epiphytes and its importance for plant physiological ecology. Perspectives in Plant Ecology, Evolution and Systematics 3, 19–28.
| Crossref | GoogleScholarGoogle Scholar |