Phenotypic plasticity in light-induced flavonoids varies among tissues in Silene littorea (Caryophyllaceae)

Plants respond to environmental stimuli in a diversity of ways including the production of secondary metabolites. Biosynthesis of plant phenolics, including flavonoids, is frequently activated in response to a variety of abiotic and biotic stressors (e.g. extreme temperatures, high radiation, pathogens, etc.). This induced reaction is typically assumed to be a plastic response, but the components attributable to plasticity vs genetic variance in these components are poorly understood. Here, we investigate the variation in flavonoid production (anthocyanins and flavones) in petals and in photosynthetic tissues (calyces, leaves and stems) of Silene littorea. We performed a common garden experiment with maternal families from three populations in which plants were exposed to different light treatments (sun exposure and shade). The concentrations of anthocyanins in photosynthetic tissues increased when plants were exposed to sun, except for leaves that showed very low quantities of anthocyanins in both light treatments; yet flavones are produced constitutively in both sun and shade treatments. The synthesis of both anthocyanins and flavones is mostly plastic, with 25 to 43% of total phenotypic variance explained by light environment. We found significant environmental effects in anthocyanin biosynthesis in calyces and stems, and in flavone production in all photosynthetic tissues. Petals showed considerably less plasticity in anthocyanin production in contrast with the accumulation of these compounds in calyces and stems. Flavones exhibited less than half of the degree of phenotypic plasticity compared to anthocyanins in calyces and stems. Overall, these results provide new insights into the degree of tissue-specific plasticity and flavonoid-specific response. Variable plasticity between flavonoids types in petals and photosynthetic tissues may allow this annual plant to differentially respond to changing light environments, while maintaining constitutive petal color in response to pollinators

UV radiation increases flavonoid protection but decreases reproduction in \u3ci\u3eSilene littorea\u3c/i\u3e

Plants respond to changes in ultraviolet (UV) radiation both morphologically and physiologically. Among the variety of plant UV-responses, the synthesis of UV-absorbing flavonoids constitutes an effective non-enzymatic mechanism to mitigate photoinhibitory and photooxidative damage caused by UV stress, either reducing the penetration of incident UV radiation or acting as quenchers of reactive oxygen species (ROS). In this study, we designed a UV-exclusion experiment to investigate the effects of UV radiation in Silene littorea. We spectrophotometrically quantified concentrations of both anthocyanins and UV-absorbing phenolic compounds in petals, calyces, leaves and stems. Furthermore, we analyzed the UV effect on the photosynthetic activity in hours of maximum solar radiation and we tested the impact of UV radiation on male and female reproductive performance. We found that anthocyanin concentrations showed a significant decrease of about 20% with UV-exclusion in petals and stems, and a 30% decrease in calyces. The concentrations of UV-absorbing compounds under UV-exclusion decreased by approximately 25% in calyces and stems, and 12% in leaves. Photochemical efficiency of plants grown under UV decreased at maximum light stress, reaching an inhibition of 58% of photosynthetic activity, but their ability to recover after light-stress was not affected. In addition, exposure to UV radiation did not affect ovule production or seed set per flower, but decreased pollen production and total seed production per plant by 31% and 69%, respectively. Our results demonstrate that UV exposure produced opposing effects on the accumulation of plant phenolic compounds and reproduction. UV radiation increased the concentration of phenolic compounds, suggesting a photoprotective role of plant phenolics against UV light, yet overall reproduction was compromised

Stability of petal color polymorphism: the significance of anthocyanin accumulation in photosynthetic tissues

Background: Anthocyanins are the primary source of colour in flowers and also accumulate in vegetative tissues, where they have multiple protective roles traditionally attributed to early compounds of the metabolic pathway (flavonols, flavones, etc.). Petal-specific loss of anthocyanins in petals allows plants to escape from the negative pleiotropic effects of flavonoid and anthocyanins loss in vegetative organs, where they perform a plethora of essential functions. Herein, we investigate the degree of pleiotropy at the biochemical scale in a pink-white flower colour polymorphism in the shore campion, Silene littorea. We report the frequencies of pink and white individuals across 21 populations and underlying biochemical profiles of three flower colour variants: anthocyanins present in all tissues (pink petals), petal-specific loss of anthocyanins (white petals), and loss of anthocyanins in all tissues (white petals). Results: Individuals lacking anthocyanins only in petals represent a stable polymorphism in two populations at the northern edge of the species range (mean frequency 8–21%). Whereas, individuals lacking anthocyanins in the whole plant were found across the species range, yet always at very low frequencies (\u3c 1%). Biochemically, the flavonoids detected were anthocyanins and flavones; in pigmented individuals, concentrations of flavones were 14–56x higher than anthocyanins across tissues with differences of \u3e 100x detected in leaves. Loss of anthocyanin pigmentation, either in petals or in the whole plant, does not influence the ability of these phenotypes to synthesize flavones, and this pattern was congruent among all sampled populations. Conclusions: We found that all colour variants showed similar flavone profiles, either in petals or in the whole plant, and only the flower colour variant with anthocyanins in photosynthetic tissues persists as a stable flower colour polymorphism. These findings suggest that anthocyanins in photosynthetic tissues, not flavonoid intermediates, are the targets of non-pollinator mediated selection

On flavonoid accumulation in different plant parts: variation patterns among individuals and populations in the shore campion (Silene littorea)

The presence of anthocyanins in flowers and fruits is frequently attributed to attracting pollinators and dispersers. In vegetative organs, anthocyanins and other non-pigmented flavonoids such as flavones and flavonols may serve protective functions against UV radiation, cold, heat, drought, salinity, pathogens, and herbivores; thus, these compounds are usually produced as a plastic response to such stressors. Although, the independent accumulation of anthocyanins in reproductive and vegetative tissues is commonly postulated due to differential regulation, the accumulation of flavonoids within and among populations has never been thoroughly compared. Here, we investigated the shore campion (Silene littorea, Caryophyllaceae) which exhibits variation in anthocyanin accumulation in its floral and vegetative tissues. We examined the in-situ accumulation of flavonoids in floral (petals and calyxes) and vegetative organs (leaves) from 18 populations representing the species\u27 geographic distribution. Each organ exhibited considerable variability in the content of anthocyanins and other flavonoids both within and among populations. In all organs, anthocyanin and other flavonoids were correlated. At the plant level, the flavonoid content in petals, calyxes, and leaves was not correlated in most of the populations. However, at the population level, the mean amount of anthocyanins in all organs was positively correlated, which suggests that the variable environmental conditions of populations may play a role in anthocyanin accumulation. These results are unexpected because the anthocyanins are usually constitutive in petals, yet contingent to environmental conditions in calyxes and leaves. Anthocyanin variation in petals may influence pollinator attraction and subsequent plant reproduction, yet the amount of anthocyanins may be a direct response to environmental factors. In populations on the west coast, a general pattern of increasing accumulation of flavonoids toward southern latitudes was observed in calyxes and leaves. This pattern corresponds to a gradual increase of UV-B radiation and temperature, and a decrease of rainfall toward the south. However, populations along the southern coast exposed to similar climatic stressors showed highly variable flavonoid contents, implying that other factors may play a role in flavonoid accumulation

UV radiation increases phenolic compound protection but decreases reproduction in Silene littorea

Plants respond to changes in ultraviolet (UV) radiation both morphologically and physiologically. Among the variety of plant UV-responses, the synthesis of UV-absorbing flavonoids constitutes an effective non-enzymatic mechanism to mitigate photoinhibitory and photooxidative damage caused by UV stress, either reducing the penetration of incident UV radiation or acting as quenchers of reactive oxygen species (ROS). In this study, we designed a UV-exclusion experiment to investigate the effects of UV radiation in Silene littorea. We spectrophotometrically quantified concentrations of both anthocyanins and UV-absorbing phenolic compounds in petals, calyces, leaves and stems. Furthermore, we analyzed the UV effect on the photosynthetic activity in hours of maximum solar radiation and we tested the impact of UV radiation on male and female reproductive performance. We found that anthocyanin concentrations showed a significant decrease of about 20% with UV-exclusion in petals and stems, and a 30% decrease in calyces. The concentrations of UV-absorbing compounds under UV-exclusion decreased by approximately 25% in calyces and stems, and 12% in leaves. Photochemical efficiency of plants grown under UV decreased at maximum light stress, reaching an inhibition of 58% of photosynthetic activity, but their ability to recover after light-stress was not affected. In addition, exposure to UV radiation did not affect ovule production or seed set per flower, but decreased pollen production and total seed production per plant by 31% and 69%, respectively. Our results demonstrate that UV exposure produced opposing effects on the accumulation of plant phenolic compounds and reproduction. UV radiation increased the concentration of phenolic compounds, suggesting a photoprotective role of plant phenolics against UV light, yet overall reproduction was compromised.This work was supported by the Spanish Government MINECO projects (CGL2012-37646 and CGL2015-63827-P) and a Predoctoral Training Program grant to JCDV (BES-2013–062610)