Unique and highly specific cyanogenic glycoside localization in stigmatic cells and pollen in the genus Lomatia (Proteaceae)

Ritmejeryte, Edita, Boughton, Berin A., Bayly, Michael J., and Miller, Rebecca E. (2020) Unique and highly specific cyanogenic glycoside localization in stigmatic cells and pollen in the genus Lomatia (Proteaceae). Annals of Botany, 126. mcaa038. pp. 387-400.

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Background and Aims: Floral chemical defence strategies remain understudied despite the significance of flowers to plant fitness, and the fact that many flowers contain secondary metabolites that confer resistance to herbivores. Optimal defence and apparency theories predict that the most apparent plant parts and/or those most important to fitness should be most defended. To test whether within-flower distributions of chemical defence are consistent with these theories we used cyanogenic glycosides (CNglycs), which are constitutive defence metabolites that deter herbivores by releasing hydrogen cyanide upon hydrolysis.

Methods: We used cyanogenic florets of the genus Lomatia to investigate at what scale there may be strategic allocation of CNglycs in flowers, what their localization reveals about function, and whether levels of floral CNglycs differ between eight congeneric species across a climatic gradient. Within-flower distributions of CNglycs during development were quantified, CNglycs were identified and their localization was visualized in cryosectioned florets using matrix-assisted laser desorption ionization mass spectrometry imaging (MALDI-MSI).

Key Results: Florets of all congeneric species studied were cyanogenic, and concentrations differed between species. Within florets there was substantial variation in CNglyc concentrations, with extremely high concentrations (up to 14.6 mg CN g−1 d. wt) in pollen and loose, specialized surface cells on the pollen presenter, among the highest concentrations reported in plant tissues. Two tyrosine-derived CNglycs, the monoglycoside dhurrin and diglycoside proteacin, were identified. MALDI-MSI revealed their varying ratios in different floral tissues; proteacin was primarily localized to anthers and ovules, and dhurrin to specialized cells on the pollen presenter. The mix of transient specialized cells and pollen of L. fraxinifolia was ~11 % dhurrin and ~1.1 % proteacin by mass.

Conclusions: Tissue-specific distributions of two CNglycs and substantial variation in their concentrations within florets suggests their allocation is under strong selection. Localized, high CNglyc concentrations in transient cells challenge the predictions of defence theories, and highlight the importance of fine-scale metabolite visualization, and the need for further investigation into the ecological and metabolic roles of CNglycs in floral tissues.

Item ID: 63647
Item Type: Article (Research - C1)
ISSN: 1095-8290
Keywords: Apparency theory, chemical defence, cyanogenesis, florivory, MALDI, mass spectrometry imaging, optimal allocation, pollinator, spatial metabolomics
Copyright Information: © The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
Funders: Holsworth Wildlife Research Endowment & the Ecological Society of Australia, Albert Shimmins Fund
Projects and Grants: Faculty of Science Early Career Researcher grant, Albert Shimmins Fund Scholarship, Norma Hilda Schuster Scholarship, Australian Postgraduate Award Scholarship
Date Deposited: 21 Jul 2020 03:19
FoR Codes: 31 BIOLOGICAL SCIENCES > 3101 Biochemistry and cell biology > 310101 Analytical biochemistry @ 50%
31 BIOLOGICAL SCIENCES > 3108 Plant biology > 310802 Plant biochemistry @ 50%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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