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Kenneth M Olsen - One of the best experts on this subject based on the ideXlab platform.
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freeze induced cyanide toxicity does not maintain the Cyanogenesis polymorphism in white clover trifolium repens
American Journal of Botany, 2018Co-Authors: Mark C Ungerer, Nicholas J Kooyers, Bradley Hartman Bakken, Kenneth M OlsenAbstract:PREMISE OF THE STUDY: The maintenance of adaptive polymorphisms within species requires fitness trade-offs reflecting selection for each morph. Cyanogenesis, the ability to produce hydrogen cyanide (HCN) after tissue damage, occurs in >3000 plant species and exists as a discrete polymorphism in white clover. This polymorphism is spatially distributed in recurrent clines, with higher frequencies of cyanogenic plants in warmer climates. The HCN autotoxicity hypothesis proposes that cyanogenic plants are selected against where frosts are common, as freezing liberates HCN and could impair cellular respiration. METHODS: We tested the HCN autotoxicity hypothesis using a freezing chamber to examine survival, tissue damage, and physiological recovery as assessed via chlorophyll fluorescence following mild and severe freezing treatments. We utilized 65 genotypes from a single polymorphic population to eliminate effects of population structure. KEY RESULTS: Cyanogenic plants did not differ from acyanogenic plants in survival, tissue damage, or recovery following freezing. However, plants producing either of the two required cyanogenic precursors had lower survival and tissue damage after freezing than plants lacking both precursors. CONCLUSIONS: These results suggest that freezing-induced HCN toxicity is unlikely to be responsible for the maintenance of the Cyanogenesis polymorphism in white clover. However, energetic trade-offs associated with costs of producing the cyanogenic precursors may confer a fitness benefit to acyanogenic plants under stressful climatic conditions. The lack of evidence for HCN toxicity suggests that cyanogenic clover uses physiological mechanisms mediated by β-cyanoalanine synthase and alternative oxidase to maintain cellular function in the presence of HCN.
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adaptive Cyanogenesis clines evolve recurrently through geographical sorting of existing gene deletions
Journal of Evolutionary Biology, 2014Co-Authors: Nicholas J Kooyers, Kenneth M OlsenAbstract:Identifying the genetic basis of parallel phenotypic evolution provides insight into the process of adaptation and evolutionary constraint. White clover (Trifolium repens) has evolved climate-associated adaptive clines in Cyanogenesis (the ability to produce hydrogen cyanide upon tissue damage) in several world regions where it has been introduced. Gene-deletion polymorphisms at the CYP79D15 and Li loci underlie the presence/absence of the cyanogenic phenotype. Both loci have undergone multiple independent gene-deletion events, which are identifiable through molecular signatures in flanking regions. To investigate whether Cyanogenesis clines in introduced populations have evolved through the sorting of standing genetic variation or de novo gene deletions, we examined Cyanogenesis gene-flanking regions in three world regions. In comparison with native Eurasian populations, we find no evidence for novel gene deletion events in any introduced region, which suggests that these adaptive clines have evolved through the geographical sorting of pre-existing genetic variation.
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adaptive gains through repeated gene loss parallel evolution of Cyanogenesis polymorphisms in the genus trifolium fabaceae
Philosophical Transactions of the Royal Society B, 2014Co-Authors: Kenneth M Olsen, Nicholas J Kooyers, Linda L SmallAbstract:Variation inCyanogenesis (hydrogen cyanidereleasefollowingtissuedamage) was first noted in populations of white clover more than a century ago, and subsequent decades of research have established this system as a classic example of an adaptive chemical defence polymorphism. Here, we document polymorphisms for cyanogenic components in several relatives of white clover, and we determine the molecular basis of this trans-specific adaptive variation. One hundred and thirty-nine plants, representing 13 of the 14 species within Trifolium section Trifoliastrum, plus additional species across the genus, were assayed for cyanogenic components (cyanogenic glucosides and their hydrolysing enzyme, linamarase) and for the presence of underlying Cyanogenesis genes (CYP79D15 and Li, respectively). One or both cyanogenic components were detected in seven species, all within section Trifoliastrum; polymorphisms for the presence/absence (PA) of components were detected in six species. In a pattern that parallels our previous findings for white clover, all observed biochemical polymorphisms correspond to gene PA poly- morphisms at CYP79D15 and Li. Relationships of DNA sequence haplotypes at the Cyanogenesis loci and flanking genomic regions suggest independent evolution of gene deletions within species. This study thus provides evidence for the parallel evolution of adaptive biochemical polymorphisms through recurrent gene deletions in multiple species.
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aridity shapes Cyanogenesis cline evolution in white clover trifolium repens l
Molecular Ecology, 2014Co-Authors: Nicholas J Kooyers, Lily R Gage, Amal Allozi, Kenneth M OlsenAbstract:Adaptive differentiation between populations is often proposed to be the product of multiple interacting selective pressures, although empirical support for this is scarce. In white clover, populations show adaptive differentiation in frequencies of Cyanogenesis, the ability to produce hydrogen cyanide after tissue damage. This polymorphism arises through independently segregating polymorphisms for the presence/absence of two required cyanogenic components, cyanogenic glucosides and their hydrolysing enzyme. White clover populations worldwide have evolved a series of recurrent, climate-associated clines, with higher frequencies of cyanogenic plants in warmer locations. These clines have traditionally been hypothesized to reflect a fitness trade-off between chemical defence in herbivore-rich areas (warmer climates) and energetic costs of producing cyanogenic components in areas of low herbivore pressure (cooler climates). Recent observational studies suggest that cyanogenic components may also be beneficial in water-stressed environments. We investigated fitness trade-offs associated with temperature-induced water stress in the Cyanogenesis system using manipulative experiments in growth chambers and population surveys across a longitudinal precipitation gradient in the central United States. We find that plants producing cyanogenic glucosides have higher relative fitness in treatments simulating a moderate, persistent drought stress. In water-neutral treatments, there are energetic costs to producing cyanogenic components, but only in treatments with nutrient stress. These fitness tradeoffs are consistent with Cyanogenesis frequencies in natural populations, where we find clinal variation in the proportion of plants producing cyanogenic glucosides along the precipitation gradient. These results suggest that multiple selective pressures interact to maintain this adaptive polymorphism and that modelling adaptation will require knowledge of environment-specific fitness effects.
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searching for the bull s eye agents and targets of selection vary among geographically disparate Cyanogenesis clines in white clover trifolium repens l
Heredity, 2013Co-Authors: N J Kooyers, Kenneth M OlsenAbstract:The recurrent evolution of adaptive clines within a species can be used to elucidate the selective factors and genetic responses that underlie adaptation. White clover is polymorphic for Cyanogenesis (HCN release with tissue damage), and climateassociated Cyanogenesis clines have evolved throughout the native and introduced species range. This polymorphism arises through two independently segregating Mendelian polymorphisms for the presence/absence of two required components: cyanogenic glucosides and their hydrolyzing enzyme linamarase. Cyanogenesis is commonly thought to function in herbivore defense; however, the individual cyanogenic components may also serve other physiological functions. To test whether Cyanogenesis clines have evolved in response to the same selective pressures acting on the same genetic targets, we examined Cyanogenesis cline shape and its environmental correlates in three world regions: southern New Zealand, the central United States and the US Pacific Northwest. For some regional comparisons, cline shapes are remarkably similar despite large differences in the spatial scales over which clines occur (40‐1600km). However, we also find evidence for major differences in both the agents and targets of selection among the sampled clines. Variation in Cyanogenesis frequency is best predicted using a combination of minimum winter temperature and aridity variables. Together, our results provide evidence that recurrent adaptive clines do not necessarily reflect shared adaptive processes. Heredity (2013) 111, 495‐504; doi:10.1038/hdy.2013.71; published online 31 July 2013
Daniel J. Ballhorn - One of the best experts on this subject based on the ideXlab platform.
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Jasmonic Acid Enhances Plant Cyanogenesis and Resistance to Herbivory in Lima Bean
Journal of Chemical Ecology, 2014Co-Authors: Stefanie Kautz, Julie A. Trisel, Daniel J. BallhornAbstract:Jasmonic acid (JA) is a natural plant hormone ubiquitously distributed in plants and centrally involved in the induction of direct and indirect plant defenses. Defenses up-regulated by this hormone include trichomes—a direct, mechanical defense—and alkaloids—a direct chemical defense—as well as two indirect chemical defenses: volatile organic compounds (VOCs) and extrafloral nectar (EFN). Plant Cyanogenesis—the release of toxic hydrogen cyanide (HCN) from preformed cyanogenic precursors in fruits, leaves, and seeds of many plants—is recognized as a direct, constitutive plant defensive trait, and is among the most widely distributed of all direct chemical plant defenses. The cyanogenic system in plants is composed of three parameters: The cyanogenic potential (HCNp; concentration of cyanogenic precursors), β-glucosidase activity, and cyanogenic capacity (HCNc; release of gaseous hydrogen cyanide). Here, we demonstrated that experimental application of aqueous solutions of JA ranging from 0.001 to 1.0 mmol L^−1, as well as insect herbivory significantly enhanced HCNc via the induction of β-glucosidase activity in wild lima bean ( Phaseolus lunatus L.). In choice feeding trials with JA induced and damaged leaves, adult Mexican bean beetles—natural herbivores of lima bean—rejected leaves with enhanced β-glucosidase activity and HCNc. Our findings suggest that jasmonic acid plays a critical role in regulating activity of β-glucosidases, which determines the rate of Cyanogenesis, and thus mediates direct plant defense against herbivores.
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salinity mediated Cyanogenesis in white clover trifolium repens affects trophic interactions
Annals of Botany, 2014Co-Authors: Daniel J. Ballhorn, Jacob D EliasAbstract:†Background and Aims Increasing soil salinity poses a major plant stress in agro-ecosystems worldwide. Surprisingly little is known about the quantitative effect of elevated salinity on secondary metabolism in many agricultural crops. Such salt-mediated changes in defence-associated compounds may significantly alter the quality of food and forage plants as well as their resistance against pests. In the present study, the effects of soil salinity on Cyanogenesis in white clover (Trifolium repens), a forage crop of international importance, are analysed. †Methods Experimental clonal plants were exposed to five levels of soil salinity, and cyanogenic potential (HCNp, total amount of accumulated cyanide in a given plant tissue), b-glucosidase activity, soluble protein concentration and biomass production were quantified. The attractiveness of plant material grown under the different salt treatments was tested using cafeteria-style feeding trials with a generalist (grey garden slug,Deroceras reticulatum) and a specialist (clover leaf weevil, Hypera punctata) herbivore. †Key Results Salt treatment resulted in an upregulation of HCNp, whereas b-glucosidase activity and soluble protein concentration showed no significant variation among treatments. Leaf area consumption of both herbivore species was negatively correlated with HCNp, indicating bottom-up effects of salinity-mediated changes in HCNp on plant consumers. †Conclusions The results suggest that soil salinity leads to an upregulation of Cyanogenesis in white clover, which results in enhanced resistance against two different natural herbivores. The potential implications for such salinitymediated changes in plant defence for livestock grazing remain to be tested.
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direct trade off between Cyanogenesis and resistance to a fungal pathogen in lima bean phaseolus lunatus l
Journal of Ecology, 2010Co-Authors: Daniel J. Ballhorn, Andrea Pietrowski, Reinhard LiebereiAbstract:Summary 1. Plants are simultaneously attacked by multiple herbivores and pathogens. While some plant defences act synergistically, others trade-off against each other. Such trade-offs among resistances to herbivores and pathogens are usually explained by the costs of resistance, i.e. resource limitations compromising a plant’s overall defence. 2. Here, we demonstrate that trade-offs can also result from direct negative interactions among defensive traits. We studied Cyanogenesis (release of HCN) of lima bean (Fabaceae: Phaseolus lunatus) and effects of this efficient anti-herbivore defence on resistance to a fungal pathogen (Melanconiaceae: Colletotrichum gloeosporioides). 3. Leaf tissue destruction by fungal growth was significantly higher on high cyanogenic (HC) lima bean accessions than on low cyanogenic (LC) plants. The susceptibility of HC accessions to the fungal pathogen was strongly correlated to reduced activity of resistance-associated polyphenol oxidases (PPOs) in leaves of these plants. LC accessions, in contrast, showed high PPO activity, which was correlated with distinct resistance to C. gloeosporioides. 4. Experimentally applied, gaseous HCN reduced PPO activity and significantly increased the size of lesions caused by C. gloeosporioides in LC leaves. 5. Field observations of a wild lima bean population in Mexico revealed a higher infection rate of HC compared to LC plant individuals. The types of lesions observed on the different cyanogenic plants in nature were similar to those observed on HC and LC plants in the laboratory. 6. Synthesis. We suggest that Cyanogenesis of lima bean directly trades off with plant defence against fungal pathogens and that the causal mechanism is the inhibition of PPOs by HCN. Our findings provide a functional explanation for the observed phenomenon of the low resistance of HC lima beans in nature.
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Cyanogenesis of wild lima bean phaseolus lunatus l is an efficient direct defence in nature
PLOS ONE, 2009Co-Authors: Daniel J. Ballhorn, Martin Heil, Stefanie Kautz, Adrian D HegemanAbstract:In natural systems plants face a plethora of antagonists and thus have evolved multiple defence strategies. Lima bean (Phaseolus lunatus L.) is a model plant for studies of inducible indirect anti-herbivore defences including the production of volatile organic compounds (VOCs) and extrafloral nectar (EFN). In contrast, studies on direct chemical defence mechanisms as crucial components of lima beans' defence syndrome under natural conditions are nonexistent. In this study, we focus on the cyanogenic potential (HCNp; concentration of cyanogenic glycosides) as a crucial parameter determining lima beans' Cyanogenesis, i.e. the release of toxic hydrogen cyanide from preformed precursors. Quantitative variability of Cyanogenesis in a natural population of wild lima bean in Mexico was significantly correlated with missing leaf area. Since existing correlations do not by necessity mean causal associations, the function of Cyanogenesis as efficient plant defence was subsequently analysed in feeding trials. We used natural chrysomelid herbivores and clonal lima beans with known cyanogenic features produced from field-grown mother plants. We show that in addition to extensively investigated indirect defences, Cyanogenesis has to be considered as an important direct defensive trait affecting lima beans' overall defence in nature. Our results indicate the general importance of analysing ‘multiple defence syndromes’ rather than single defence mechanisms in future functional analyses of plant defences.
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research article quantitative variability of Cyanogenesis in cathariostachys madagascariensis the main food plant of bamboo lemurs in southeastern madagascar
2009Co-Authors: Daniel J. Ballhorn, Stefanie Kautz, Fanny RakotoariveloAbstract:Giant bamboo (Cathariostachys madagascariensis) is a major food plant for three sympatric species of bamboo-eating lemurs (Hapalemur aureus, H. griseus, and Prolemur simus) in the rain forests of southeastern Madagascar. This plant species is strongly cyanogenic. However, quantitative data on cyanide concentration in C. madagascariensis are scarce. Previous studies reported 15mg cyanide per 100g fresh shoot material (corresponding to approx. 57mmol cyanide per gram dry weight). However, we found mean concentrations (7SE) ranging from 139.3719.32 in ground shoots to 217.7716.80mmol cyanide per gram dry weight in branch shoots. Thus, Cyanogenesis of C. madagascariensis was up to four times higher than reported before. In contrast to the strongly cyanogenic shoots no cyanide could be detected in differently aged leaves of C. madagascariensis confirming earlier studies. Within individual shoots fine-scaled analysis revealed a characteristic ontogenetic pattern of cyanide accumulation. Highest concentrations were found in youngest parts near the apical meristem, whereas concentrations decreased in older shoot parts. Beyond the general intra-individual variability of cyanogenic features analyses indicated site-specific variability of both, the ontogenetic pattern of cyanide concentration as well as the total amount of cyanide accumulated in shoots. Additionally, analyses of soluble proteins—one important nutritive measure affecting food plant quality— demonstrated a converse quantitative relation of protein concentrations in leaves to cyanide concentration in shoots at the site-specific level. We, thus, suggest integrative analyses on quantitative variation of Cyanogenesis together with nutritive plant parameters in future studies. This approach would allow obtaining more detailed insights into spatial variability of giant bamboo’s overall browse quality and its impact on lemur herbivores. Am. J. Primatol. 71:305‐315, 2009. r 2009 Wiley-Liss, Inc.
Joel S Shore - One of the best experts on this subject based on the ideXlab platform.
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Cyanogenesis in turnera ulmifolia l turneraceae ii developmental expression heritability and cost of Cyanogenesis
Evolutionary Ecology Research, 2000Co-Authors: P J Schappert, Joel S ShoreAbstract:We examine the Cyanogenesis polymorphism in Turnera ulmifolia on Jamaica with respect to our hypothesis that seedlings in some populations have significantly higher levels of Cyanogenesis than mature plants because of the developmental loss of Cyanogenesis. Furthermore, we provide estimates of among-family variance, as estimates of broad sense heritability, for a number of fitness-related traits, and also examine the potential cost of Cyanogenesis in this species. Our data reveal that there is a marked developmental loss of Cyanogenesis in some populations of T. ulmifolia. Seedlings have significantly greater levels of Cyanogenesis than mature plants in ‘acyanogenic’ populations, but this developmental loss is absent in predominantly cyanogenic populations. This is the first study to document extensive developmental loss of chemical defence in a cyanogenic species. We suggest that, in these populations, there might be selection favouring Cyanogenesis in seedlings. There is substantial among-family variance in a number of traits in five T. ulmifolia populations examined, including plant height, time to first flowering, total flower production and Cyanogenesis. Phenotypic and, more importantly, negative genetic correlations between total flower production and Cyanogenesis provide evidence for a cost of Cyanogenesis in three of five populations.
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effects of Cyanogenesis polymorphism in turnera ulmifolia on euptoieta hegesia and potential anolis predators
Journal of Chemical Ecology, 1999Co-Authors: P J Schappert, Joel S ShoreAbstract:We examine the effects of the Cyanogenesis polymorphism in Turnera ulmifolia on larvae, pupae, and adults of Euptoieta hegesia, the most damaging herbivore of T. ulmifolia in terms of tissue loss per unit time. We provide evidence that female E. hegesia do not show preference for host plants on the basis of their Cyanogenesis level but do prefer T. ulmifolia over equally cyanogenic, closely related secondary host-plant species (Passiflora sp.). Similarly, Cyanogenesis in T. ulmifolia has little effect on the food preference, growth, or development of the larvae. The potential host range of E. hegesia is limited, even within the genus Turnera, but this does not appear to be due to host-plant Cyanogenesis. Pupae suffer very high mortality levels in the wild that are not associated with host-plant Cyanogenesis, although our studies indicate that larvae are capable of sequestering cyanogenic glycosides from their host plants and possibly of synthesizing these or similar compounds. We provide evidence that the presence of sequestered cyanogenic compounds in the larvae protects them from terrestrial-based predators such as Anolis lizards
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Cyanogenesis herbivory and plant defense in turnera ulmifolia on jamaica
Ecoscience, 1999Co-Authors: P J Schappert, Joel S ShoreAbstract:Field surveys of eight populations of Turnera ulmifolia L., a Jamaican weed exhibiting quantitative genetic variation for Cyanogenesis, were undertaken to assess the effectiveness of Cyanogenesis as a plant defense. Populations known to be characteristically acyanogenic, cyanogenic or to exhibit within-population variation were surveyed for Cyanogenesis, plant size, and the presence and identity of invertebrate plant visitors. A developmental series of 10 leaves from a shoot of each surveyed plant was analyzed, using image analysis techniques, for the type and extent of damage present. We also surveyed two additional plant populations for the presence of plants with eggs or larvae of Euptoieta hegesia Cramer, a Nymphalid butterfly that is potentially the most damaging herbivore of T. ulmifolia, and a paired comparison analysis of Cyanogenesis in plants with the herbivore versus plants without the herbivore was conducted. We found that T. ulmifolia are attacked by a reasonably diverse insect fauna, but a relatively small suite of specialist herbivores that are seemingly undeterred by Cyanogenesis inflicts most of the leaf damage. Cyanogenesis does appear to play a role in determining the types, numbers, and presence of generalist herbivores found within and between populations. Tissue loss sustained by plants varies both within and between populations; however, the proportion of leaf tissue lost due to herbivory is low, ranging from only 1-9% on average, and does not appear to be correlated with Cyanogenesis in a consistent way. An analysis of covariance did, however, reveal that Cyanogenesis has a significant effect on both plant height and number of shoots per plant. These results suggest that Cyanogenesis might afford protection against herbivory from generalizing herbivores. Keywords: natural selection, variation, cost, herbivore damage, chemical defense, colonization, specialization, Euptoieta hegesia. Resume :N ous avons etudie huit populations de Turnera ulmifolia, une mauvaise herbe de la Jamaique demontrant une variation quantitative genetique de la production de cyanure, afin d'evaluer l'efficacite du cyanure comme mecanisme de defense chez les plantes. Nous avons examine la taille des plantes dans des populations connues, ne produisant aucun cyanure, etant cyanurique ou demontrant une variation dans cette production dans une meme population aussi bien que la presence et l'identification des invertebres visitant ces plantes. Une serie developpementale de dix feuilles de pousse de chaque plante ont ete examinees a l'aide des techniques d'analyse d'images pour evaluer le type et le niveau des dommages. Deux autres populations de plantes ont ete etudiees afin de deceler la presence d'oeufs et de larves de Euptoieta hegesia Cramer (Nymphalidae), un papillon qui est un des herbivores eventuellement les plus destructifs de T. ulmifolia. Une analyse du cyanure des plantes avec ou sans herbivores a aussi ete effectuee. Nous avons trouve que T. ulmifolia est attaque par un assez grand nombre d'insectes, mais que seulement un petit nombre d'herbivores specialises, causant le plus de dommages, semblent n'etre d'aucune facon affectes par le cyanure. Le cyanure semble jouer un role dans la quantite, le type et la presence des herbivores generalises dans une meme population et parmi les populations de plantes. La perte de tissu vegetal dans une meme population et entre les populations de plantes varie, mais la proportion de cette perte demeure faible, variant en moyenne de 1 % a 9 %; cette derniere ne semble pas etre correlee de facon constante avec le cyanure. Une analyse de covariance a par contre demontre que la production de cyanure a un effet significatif sur la hauteur et le nombre de pousses que chaque plante produit. Ces resultats suggerent que la production de cyanure peut fournir une certaine protection contre l'herbivorie par les herbivores generalistes. Mots-cles : selection naturelle, variation, cout, dommages causes par les herbivores, defense chimique, colonisation, specialisation, Euptoieta hegesia.
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Cyanogenesis in turnera ulmifolia l turneraceae i phenotypic distribution and genetic variation for Cyanogenesis on jamaica
Heredity, 1995Co-Authors: P J Schappert, Joel S ShoreAbstract:Cyanogenesis in Turnera ulmifolia L. (Turneraceae). I. Phenotypic distribution and genetic variation for Cyanogenesis on Jamaica
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Variation in Cyanogenesis within and among populations and species of Turnera series Canaligerae (Turneraceae)
Biochemical Systematics and Ecology, 1992Co-Authors: Joel S Shore, Christa M. ObristAbstract:Nine species of Turnera series Canaligerae, at three ploida levels, were tested for Cyanogenesis. Four of nine species (including both diploids and hexaploids) possessed cyanogenic plants. Tetraploids were never found to be cyanogenic. Variation for Cyanogenesis occurred within three species. All acyanogenic plants investigated possess β-glucosidases capable of hydrolysing exogenously supplied cyanogenic glycosides. Floral parts and seedling tissues are cyanogenic. Within-plant variation occurs and the intensity of Cyanogenesis varies with leaf age.
Nicholas J Kooyers - One of the best experts on this subject based on the ideXlab platform.
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freeze induced cyanide toxicity does not maintain the Cyanogenesis polymorphism in white clover trifolium repens
American Journal of Botany, 2018Co-Authors: Mark C Ungerer, Nicholas J Kooyers, Bradley Hartman Bakken, Kenneth M OlsenAbstract:PREMISE OF THE STUDY: The maintenance of adaptive polymorphisms within species requires fitness trade-offs reflecting selection for each morph. Cyanogenesis, the ability to produce hydrogen cyanide (HCN) after tissue damage, occurs in >3000 plant species and exists as a discrete polymorphism in white clover. This polymorphism is spatially distributed in recurrent clines, with higher frequencies of cyanogenic plants in warmer climates. The HCN autotoxicity hypothesis proposes that cyanogenic plants are selected against where frosts are common, as freezing liberates HCN and could impair cellular respiration. METHODS: We tested the HCN autotoxicity hypothesis using a freezing chamber to examine survival, tissue damage, and physiological recovery as assessed via chlorophyll fluorescence following mild and severe freezing treatments. We utilized 65 genotypes from a single polymorphic population to eliminate effects of population structure. KEY RESULTS: Cyanogenic plants did not differ from acyanogenic plants in survival, tissue damage, or recovery following freezing. However, plants producing either of the two required cyanogenic precursors had lower survival and tissue damage after freezing than plants lacking both precursors. CONCLUSIONS: These results suggest that freezing-induced HCN toxicity is unlikely to be responsible for the maintenance of the Cyanogenesis polymorphism in white clover. However, energetic trade-offs associated with costs of producing the cyanogenic precursors may confer a fitness benefit to acyanogenic plants under stressful climatic conditions. The lack of evidence for HCN toxicity suggests that cyanogenic clover uses physiological mechanisms mediated by β-cyanoalanine synthase and alternative oxidase to maintain cellular function in the presence of HCN.
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adaptive Cyanogenesis clines evolve recurrently through geographical sorting of existing gene deletions
Journal of Evolutionary Biology, 2014Co-Authors: Nicholas J Kooyers, Kenneth M OlsenAbstract:Identifying the genetic basis of parallel phenotypic evolution provides insight into the process of adaptation and evolutionary constraint. White clover (Trifolium repens) has evolved climate-associated adaptive clines in Cyanogenesis (the ability to produce hydrogen cyanide upon tissue damage) in several world regions where it has been introduced. Gene-deletion polymorphisms at the CYP79D15 and Li loci underlie the presence/absence of the cyanogenic phenotype. Both loci have undergone multiple independent gene-deletion events, which are identifiable through molecular signatures in flanking regions. To investigate whether Cyanogenesis clines in introduced populations have evolved through the sorting of standing genetic variation or de novo gene deletions, we examined Cyanogenesis gene-flanking regions in three world regions. In comparison with native Eurasian populations, we find no evidence for novel gene deletion events in any introduced region, which suggests that these adaptive clines have evolved through the geographical sorting of pre-existing genetic variation.
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adaptive gains through repeated gene loss parallel evolution of Cyanogenesis polymorphisms in the genus trifolium fabaceae
Philosophical Transactions of the Royal Society B, 2014Co-Authors: Kenneth M Olsen, Nicholas J Kooyers, Linda L SmallAbstract:Variation inCyanogenesis (hydrogen cyanidereleasefollowingtissuedamage) was first noted in populations of white clover more than a century ago, and subsequent decades of research have established this system as a classic example of an adaptive chemical defence polymorphism. Here, we document polymorphisms for cyanogenic components in several relatives of white clover, and we determine the molecular basis of this trans-specific adaptive variation. One hundred and thirty-nine plants, representing 13 of the 14 species within Trifolium section Trifoliastrum, plus additional species across the genus, were assayed for cyanogenic components (cyanogenic glucosides and their hydrolysing enzyme, linamarase) and for the presence of underlying Cyanogenesis genes (CYP79D15 and Li, respectively). One or both cyanogenic components were detected in seven species, all within section Trifoliastrum; polymorphisms for the presence/absence (PA) of components were detected in six species. In a pattern that parallels our previous findings for white clover, all observed biochemical polymorphisms correspond to gene PA poly- morphisms at CYP79D15 and Li. Relationships of DNA sequence haplotypes at the Cyanogenesis loci and flanking genomic regions suggest independent evolution of gene deletions within species. This study thus provides evidence for the parallel evolution of adaptive biochemical polymorphisms through recurrent gene deletions in multiple species.
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aridity shapes Cyanogenesis cline evolution in white clover trifolium repens l
Molecular Ecology, 2014Co-Authors: Nicholas J Kooyers, Lily R Gage, Amal Allozi, Kenneth M OlsenAbstract:Adaptive differentiation between populations is often proposed to be the product of multiple interacting selective pressures, although empirical support for this is scarce. In white clover, populations show adaptive differentiation in frequencies of Cyanogenesis, the ability to produce hydrogen cyanide after tissue damage. This polymorphism arises through independently segregating polymorphisms for the presence/absence of two required cyanogenic components, cyanogenic glucosides and their hydrolysing enzyme. White clover populations worldwide have evolved a series of recurrent, climate-associated clines, with higher frequencies of cyanogenic plants in warmer locations. These clines have traditionally been hypothesized to reflect a fitness trade-off between chemical defence in herbivore-rich areas (warmer climates) and energetic costs of producing cyanogenic components in areas of low herbivore pressure (cooler climates). Recent observational studies suggest that cyanogenic components may also be beneficial in water-stressed environments. We investigated fitness trade-offs associated with temperature-induced water stress in the Cyanogenesis system using manipulative experiments in growth chambers and population surveys across a longitudinal precipitation gradient in the central United States. We find that plants producing cyanogenic glucosides have higher relative fitness in treatments simulating a moderate, persistent drought stress. In water-neutral treatments, there are energetic costs to producing cyanogenic components, but only in treatments with nutrient stress. These fitness tradeoffs are consistent with Cyanogenesis frequencies in natural populations, where we find clinal variation in the proportion of plants producing cyanogenic glucosides along the precipitation gradient. These results suggest that multiple selective pressures interact to maintain this adaptive polymorphism and that modelling adaptation will require knowledge of environment-specific fitness effects.
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recurrent gene deletions and the evolution of adaptive Cyanogenesis polymorphisms in white clover trifolium repens l
Molecular Ecology, 2013Co-Authors: Kenneth M Olsen, Nicholas J Kooyers, Linda L SmallAbstract:Understanding the molecular evolution of genes that underlie intraspecific polymorphisms can provide insights into the process of adaptive evolution. For adaptive polymorphisms characterized by gene presence ⁄absence (P ⁄A) variation, underlying loci commonly show signatures of long-term balancing selection, with gene-presence and gene-absence alleles maintained as two divergent lineages. We examined the molecular evolution of two unlinked P ⁄A polymorphisms that underlie a well-documented adaptive polymorphism for Cyanogenesis (hydrogen cyanide release with tissue damage) in white clover. Both cyanogenic and acyanogenic plants occur in this species, and the ecological forces that maintain this chemical defence polymorphism have been studied for several decades. Using a sample of 65 plants, we investigated the molecular evolution of sequences flanking the two underlying Cyanogenesis genes: Ac ⁄ac (controlling the presence ⁄absence of cyanogenic glucosides) and Li ⁄li (controlling the presence ⁄absence of their hydrolysing enzyme, linamarase). A combination of genome walking, PCR assays, DNA sequence analysis and Southern blotting was used to test whether these adaptive P ⁄A polymorphisms show evidence of long-term balancing selection, or whether gene-absence alleles have evolved repeatedly through independent deletion events. For both loci, we detect no signatures of balancing selection in the closest flanking genomic sequences. Instead, we find evidence for variation in the size of the deletions characterizing gene-absence alleles. These observations strongly suggest that both of these polymorphisms have been evolving through recurrent gene deletions over time. We discuss the genetic mechanisms that could account for this surprising pattern and the implications of these findings for mechanisms of rapid adaptive evolution in white clover.
Ian E Woodrow - One of the best experts on this subject based on the ideXlab platform.
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constitutive polymorphic Cyanogenesis in the australian rainforest tree ryparosa kurrangii achariaceae
Phytochemistry, 2007Co-Authors: Bruce L Webber, Rebecca Elizabeth Miller, Ian E WoodrowAbstract:Abstract Cyanogenesis, the liberation of volatile hydrogen cyanide from endogenous cyanide-containing compounds, is a proven plant defence mechanism and the particular cyanogens involved have taxonomic utility. The cyclopentenoncyanhydrin glycoside gynocardin was the only cyanogen isolated from foliar tissue of the rare Australian rainforest tree, Ryparosa kurrangii (Achariaceae). Mechanical damage simulating foliar herbivory did not induce a significant increase in the expression of Cyanogenesis over a 24 h period, indicating cyanogenic herbivore defence in R. kurrangii is constitutive. The cyanogenic potential of mature leaves was quantitatively polymorphic between trees in a natural population, ranging from 0.54 to 4.77 mg CN g −1 dry wt leaf tissue.
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frequency of Cyanogenesis in tropical rainforests of far north queensland australia
Annals of Botany, 2006Co-Authors: Rebecca Elizabeth Miller, Rigel Jensen, Ian E WoodrowAbstract:� Background and Aims Plant Cyanogenesis is the release of toxic cyanide from endogenous cyanide-containing compounds, typically cyanogenic glycosides. Despite a large body of phytochemical, taxonomic and ecological work on cyanogenic species, little is known of their frequency in natural plant communities. This study aimed to investigate the frequency of Cyanogenesis in Australian tropical rainforests. Secondary aims were to quantify the cyanogenic glycoside content of tissues, to investigate intra-plant and intra-population variation in cyanogenic glycoside concentration and to appraise the potential chemotaxonomic significance of any findings in relation to the distribution of Cyanogenesis in related taxa. � Methods All species in six 200m 2 plots at each of five sites across lowland, upland and highland tropical rainforest were screened for Cyanogenesis using Feigl‐Anger indicator papers. The concentrations of cyanogenic glycosides were accurately determined for all cyanogenic individuals. � Key Results Over 400 species from 87 plant families were screened. Overall, 18 species (4� 5%) were cyanogenic, accounting for 7� 3% of total stem basal area. Cyanogenesis has not previously been reported for 17 of the 18 species, 13 of which are endemic to Australia. Several species belong to plant families or orders in which Cyanogenesis has been little reported, if at all (e.g. Elaeocarpaceae, Myrsinaceae, Araliaceae and Lamiaceae). A number of species contained concentrations of cyanogenic glycosides among the highest ever reported for mature leaves—up to 5� 2mgCNg � 1 d.wt, for example, in leaves of Elaeocarpus sericopetalus. There was significant variation in cyanogenic glycoside concentration within individuals; young leaves and reproductive tissues typically had higher cyanogen content. In addition, there was substantial variation in cyanogenic glycoside content within populations of single species. � Conclusions This study expands the limited knowledge of the frequency of Cyanogenesis in natural plant communities, includes novel reports of Cyanogenesis among a range of taxa and characterizes patterns in intra-plant and intra-population variation of cyanogensis.
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Cyanogenesis in the australian tropical rainforest endemic brombya platynema rutaceae chemical characterisation and polymorphism
Functional Plant Biology, 2006Co-Authors: Rebecca Elizabeth Miller, Judy Simon, Ian E WoodrowAbstract:This study examined two aspects of Cyanogenesis in Brombya platynema F. Muell. (Rutaceae), a subcanopy tree endemic to tropical rainforest in far north Queensland, Australia. First, cyanogenic glycosides in foliage were fractionated and identified. The rare meta-hydroxylated cyanogenic glycoside, holocalin, was identified as the principal cyanogen, and traces of prunasin and amygdalin were detected. This is the first characterisation of cyanogenic constituents within the genus, and to the authors' knowledge, only the third within the Rutaceae, and the order Rutales. Second, variation in cyanogenic glycoside content within a population of B. platynema in lowland tropical rainforest was quantified. Both qualitative and quantitative polymorphism for Cyanogenesis was identified. Interestingly, ∼57% of individuals were considered acyanogenic, with concentrations of cyanogenic glycosides less than 8 µ gC N g −1 DW. Among cyanogenic individuals there was substantial quantitative variation in cyanogenic glycoside concentration, which varied from 10.5 to 1285.9 µ gC N g −1 DW. This high frequency of acyanogenic individuals is contrasted with the apparent absence of the aCyanogenesis among populations of other tropical rainforest tree species. In the high herbivory environment of the tropical rainforest, this frequency of aCyanogenesis among cyanogenic tropical tree taxa is unique.
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novel aspects of Cyanogenesis in eucalyptus camphora subsp humeana
Functional Plant Biology, 2006Co-Authors: Elizabeth H J Neilson, Jason Q D Goodger, Ian E WoodrowAbstract:Cyanogenesis is the release of cyanide from certain organisms upon tissue disruption. Tissue disruption, such as that caused by folivory, brings cyanogenic glycosides into contact with catabolic enzymes and toxic HCN is subsequently released. The process provides a measure of defence against generalist herbivores. Within the genus Eucalyptus, several species have been identified as cyanogenic and all of these store cyanide exclusively in the form of the cyanogenic glycoside prunasin. Here we report for the first time Cyanogenesis in Eucalyptus camphora subsp. humeana L.A.S. Johnson & K.D. Hill. We found that foliage contains at least five different cyanogenic glycosides, three of which were purified and identified (prunasin, sambunigrin and amygdalin). Two natural populations of E. camphora trees were screened for Cyanogenesis, and quantitative polymorphism was measured at both sites. Trees varied in their capacity for Cyanogenesis from 0.014 to 0.543 mg CN g–1 DW in one population and from 0.011 to 0.371 mg CN g–1 DW in the other. A progeny trial, testing both Cyanogenesis and carbon-based defence (namely total phenolics and condensed tannins), was performed with seed sourced from two cyanogenic, open-pollinated maternal trees. Interestingly, the seedlings exhibited markedly lower levels of Cyanogenesis and condensed tannins than the adult population, with some individuals completely lacking one or both of the chemical defences. Total phenolic concentrations, however, were significantly higher in the seedlings than in the parental population from which the seed was sourced. Eucalyptus camphora is relatively unique among cyanogenic trees having multiple foliar cyanogenic glycosides and an apparently marked ontogenetic regulation of cyanogenic capacity.
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Cyanogenesis in eucalyptus polyanthemos seedlings heritability ontogeny and effect of soil nitrogen
Tree Physiology, 2004Co-Authors: Jason Q D Goodger, Peter K Ades, Ian E WoodrowAbstract:: Cyanogenic plants release cyanide from endogenous cyanide-containing compounds (generally cyanogenic glycosides) and thus have an effective means of chemical defense. The capacity for Cyanogenesis can be highly variable, even among individuals within a population. The genetic, environmental and developmental factors determining this variability are poorly understood, particularly in tree species. We used Eucalyptus polyanthemos Schauer subsp. vestita L. Johnson & K. Hill to quantify aspects of the regulation of cyanogenic capacity, which in this species is determined by foliar cyanogenic glycoside concentration. A half-sibling progeny trial, based on seed collected from open-pollinated trees covering a range of cyanogenic capacities, was used to assess the heritability of Cyanogenesis in E. polyanthemos. Narrow sense heritability (h(2) +/- 1 SE) was estimated to be 0.82 +/- 0.20 from an intra-class correlation and 0.78 +/- 0.11 from a standardized progeny-parent regression. Foliar cyanogenic glycoside concentrations were on average about 70% lower in seedlings than in maternal trees, suggesting that there is a developmental delay in the accumulation of cyanogenic capacity in this species. The high h(2) values indicate that cyanogenic capacity is largely genetically determined and that environmental factors have little effect. To test this supposition, we grew seedlings at two soil nitrogen (N) concentrations (N influences cyanogenic capacity in some species) and found no appreciable effect on cyanogenic glycoside concentration, biomass partitioning or relative growth rate. Highly cyanogenic seedlings grew more slowly than seedlings with lower cyanogenic capacities, and relative growth rate was positively associated with net assimilation rate in seedlings in both N treatments.
