Diverse organ-specific localisation of a chemical defence, cyanogenic glycosides, in flowers of eleven species of Proteaceae
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...
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| description | 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. |
| doi_str_mv | 10.1371/journal.pone.0285007 |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0285007</identifier><identifier>PMID: 37104509</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Allocations ; Analysis ; Anthers ; Biology and Life Sciences ; Chemical defense ; Evaluation ; Fitness ; Flowers ; Flowers & plants ; Flowers - metabolism ; Fruits ; Glycosides ; Glycosides - metabolism ; Herbivores ; Hydrogen cyanide ; Laboratories ; Localization ; Mass spectrometry ; Mass spectroscopy ; Medicine and Health Sciences ; Metabolites ; Physical Sciences ; Pistils ; Plant metabolites ; Plant reproductive structures ; Plant tissues ; Plants ; Plants (botany) ; Plastics ; Pollen ; Pollination ; Pollinators ; Pollinators (Animals) ; Proteaceae ; Research and Analysis Methods ; Secondary metabolites ; Seeds ; Tyrosine ; Vascular tissue</subject><ispartof>PloS one, 2023-04, Vol.18 (4), p.e0285007-e0285007</ispartof><rights>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.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Ritmejerytė et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Ritmejerytė et al 2023 Ritmejerytė et al</rights><rights>2023 Ritmejerytė et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c642t-d60c8008fe895563935a622bfbd8fff4c89942331c3f07bbe0225ea81d6260b93</cites><orcidid>0000-0002-8605-9198</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10138830/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10138830/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37104509$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Šiler, Branislav T.</contributor><creatorcontrib>Ritmejerytė, Edita</creatorcontrib><creatorcontrib>Boughton, Berin A</creatorcontrib><creatorcontrib>Bayly, Michael J</creatorcontrib><creatorcontrib>Miller, Rebecca E</creatorcontrib><title>Diverse organ-specific localisation of a chemical defence, cyanogenic glycosides, in flowers of eleven species of Proteaceae</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>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.</description><subject>Allocations</subject><subject>Analysis</subject><subject>Anthers</subject><subject>Biology and Life Sciences</subject><subject>Chemical defense</subject><subject>Evaluation</subject><subject>Fitness</subject><subject>Flowers</subject><subject>Flowers & plants</subject><subject>Flowers - metabolism</subject><subject>Fruits</subject><subject>Glycosides</subject><subject>Glycosides - metabolism</subject><subject>Herbivores</subject><subject>Hydrogen cyanide</subject><subject>Laboratories</subject><subject>Localization</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Medicine and Health Sciences</subject><subject>Metabolites</subject><subject>Physical Sciences</subject><subject>Pistils</subject><subject>Plant 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organ-specific localisation of a chemical defence, cyanogenic glycosides, in flowers of eleven species of Proteaceae</title><author>Ritmejerytė, Edita ; Boughton, Berin A ; Bayly, Michael J ; Miller, Rebecca E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c642t-d60c8008fe895563935a622bfbd8fff4c89942331c3f07bbe0225ea81d6260b93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Allocations</topic><topic>Analysis</topic><topic>Anthers</topic><topic>Biology and Life Sciences</topic><topic>Chemical defense</topic><topic>Evaluation</topic><topic>Fitness</topic><topic>Flowers</topic><topic>Flowers & plants</topic><topic>Flowers - metabolism</topic><topic>Fruits</topic><topic>Glycosides</topic><topic>Glycosides - metabolism</topic><topic>Herbivores</topic><topic>Hydrogen cyanide</topic><topic>Laboratories</topic><topic>Localization</topic><topic>Mass 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flowers of eleven species of Proteaceae</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-04-27</date><risdate>2023</risdate><volume>18</volume><issue>4</issue><spage>e0285007</spage><epage>e0285007</epage><pages>e0285007-e0285007</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37104509</pmid><doi>10.1371/journal.pone.0285007</doi><orcidid>https://orcid.org/0000-0002-8605-9198</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Allocations Analysis Anthers Biology and Life Sciences Chemical defense Evaluation Fitness Flowers Flowers & plants Flowers - metabolism Fruits Glycosides Glycosides - metabolism Herbivores Hydrogen cyanide Laboratories Localization Mass spectrometry Mass spectroscopy Medicine and Health Sciences Metabolites Physical Sciences Pistils Plant metabolites Plant reproductive structures Plant tissues Plants Plants (botany) Plastics Pollen Pollination Pollinators Pollinators (Animals) Proteaceae Research and Analysis Methods Secondary metabolites Seeds Tyrosine Vascular tissue |
| title | Diverse organ-specific localisation of a chemical defence, cyanogenic glycosides, in flowers of eleven species of Proteaceae |
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