Diverse organ-specific localisation of a chemical defence, cyanogenic glycosides, in flowers of eleven species of Proteaceae

Edita Ritmejerytė; Berin A Boughton; Michael J Bayly; Rebecca E Miller

doi:10.1371/journal.pone.0285007

Diverse organ-specific localisation of a chemical defence, cyanogenic glycosides, in flowers of eleven species of Proteaceae

PLoS One. 2023 Apr 27;18(4):e0285007. doi: 10.1371/journal.pone.0285007. eCollection 2023.

Authors

Edita Ritmejerytė^{1

2

3}, Berin A Boughton^{2

4}, Michael J Bayly², Rebecca E Miller^{1

5}

Affiliations

¹ School of Ecosystem and Forest Sciences, The University of Melbourne, Richmond, Victoria, Australia.
² School of BioSciences, The University of Melbourne, Parkville, Victoria, Australia.
³ Australian Institute of Tropical Health and Medicine, James Cook University, Smithfield, Queensland, Australia.
⁴ Australian National Phenome Centre, Murdoch University, Murdoch, Western Australia, Australia.
⁵ Royal Botanic Gardens Victoria, South Yarra, Victoria, Australia.

Abstract

Floral chemical defence strategies remain under-investigated, despite the significance of flowers to plant fitness. We used cyanogenic glycosides (CNglycs)-constitutive secondary metabolites that deter herbivores by releasing hydrogen cyanide, but also play other metabolic roles-to ask whether more apparent floral tissues and those most important for fitness are more defended as predicted by optimal defence theories, and what fine-scale CNglyc localisation reveals about function(s)? Florets of eleven species from the Proteaceae family were dissected to quantitatively compare the distribution of CNglycs within flowers and investigate whether distributions vary with other floral/plant traits. CNglycs were identified and their localisation in florets was revealed by matrix-assisted laser desorption ionisation mass spectrometry imaging (MALDI-MSI). We identified extremely high CNglyc content in floral tissues of several species (>1% CN), highly tissue-specific CNglyc distributions within florets, and substantial interspecific differences in content distributions, not all consistent with optimal defence hypotheses. Four patterns of within-flower CNglyc allocation were identified: greater tissue-specific allocations to (1) anthers, (2) pedicel (and gynophore), (3) pollen presenter, and (4) a more even distribution among tissues with higher content in pistils. Allocation patterns were not correlated with other floral traits (e.g. colour) or taxonomic relatedness. MALDI-MSI identified differential localisation of two tyrosine-derived CNglycs, demonstrating the importance of visualising metabolite localisation, with the diglycoside proteacin in vascular tissues, and monoglycoside dhurrin across floral tissues. High CNglyc content, and diverse, specific within-flower localisations indicate allocations are adaptive, highlighting the importance of further research into the ecological and metabolic roles of floral CNglycs.

Copyright: © 2023 Ritmejerytė et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Flowers / metabolism
Glycosides / metabolism
Plants
Pollen
Pollination
Proteaceae*

Substances

cyanogenic glycosides
Glycosides

Grants and funding

“This work was supported by an Early Career Researcher grant to Rebecca Miller, and the Holsworth Wildlife Research Endowment & the Ecological Society of Australia, the Albert Shimmins Fund Scholarship and Norma Hilda Schuster Scholarship to Edita Ritmejerytė. Edita Ritmejerytė was a recipient of an Australian Postgraduate Award Scholarship. Rebecca Miller’s lectureship received support from the Cybec Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.”