Spectral effects of light-emitting diodes on plant growth, visual color quality, and photosynthetic photon efficacy: White versus blue plus red radiation.

Arrays of blue (B, 400-500 nm) and red (R, 600-700 nm) light-emitting diodes (LEDs) used for plant growth applications make visual assessment of plants difficult compared to a broad (white, W) spectrum. Although W LEDs are sometimes used in horticultural lighting fixtures, little research has been published using them for sole-source lighting. We grew seedlings of begonia (Begonia ×semperflorens), geranium (Pelargonium ×horturum), petunia (Petunia ×hybrida), and snapdragon (Antirrhinum majus) at 20°C under six sole-source LED lighting treatments with a photosynthetic photon flux density (PPFD) of 160 µmol∙m-2∙s-1 using B (peak = 447 nm), green (G, peak = 531 nm), R (peak = 660 nm), and/or mint W (MW, peak = 558 nm) LEDs that emitted 15% B, 59% G, and 26% R plus 6 µmol∙m-2∙s-1 of far-red radiation. The lighting treatments (with percentage from each LED in subscript) were MW100, MW75R25, MW45R55, MW25R75, B15R85, and B20G40R40. At the transplant stage, total leaf area, and fresh and dry weight were similar among treatments in all species. Surprisingly, when petunia seedlings were grown longer (beyond the transplant stage) under sole-source lighting treatments, the primary stem elongated and had flower buds earlier under MW100 and MW75R25 compared to under B15R85. The color rendering index of MW75R25 and MW45R55 were 72, and 77, respectively, which was higher than those of other treatments, which were ≤64. While photosynthetic photon efficacy of B15R85 (2.25 µmol∙J-1) was higher than the W light treatments (1.51-2.13 µmol∙J-1), the dry weight gain per unit electric energy consumption (in g∙kWh-1) of B15R85 was similar to those of MW25R75, MW45R55, and MW75R25 in three species. We conclude that compared to B+R radiation, W radiation had generally similar effects on seedling growth at the same PPFD with similar electric energy consumption, and improved the visual color quality of sole-source lighting.

Lamelloplasts and minichloroplasts in Begoniaceae: iridescence and photosynthetic functioning.

Iridoplasts (modified plastids in adaxial epidermal cells) reported from Begonia were originally hypothesized to cause iridescence, which was broadly accepted for decades. However, several species of Begonia with iridoplasts are not iridescent causing confusion. Here chloroplast ultrastructure was observed in 40 taxa of Begoniaceae to explore the phenomenon of iridescence. However, 22 Begonias and Hillebrandia were found to have iridoplasts, but only nine display visually iridescent blue to blue-green leaves. Unexpectedly, a new type of plastid, a 'minichloroplast,' was found in the abaxial epidermal cells of all taxa, but was present in adaxial epidermal cells only if iridoplasts were absent. Comparative ultrastructural study of iridoplasts and a shading experiment of selected taxa show that a taxon with iridoplasts does not inevitably have visual iridescence, but iridescence is greatly affected by the spacing between thylakoid lamellae (stoma spacing). Thus, we propose instead the name 'lamelloplast' for plastids filled entirely with regular lamellae to avoid prejudging their function. To evaluate photosynthetic performance, chlorophyll fluorescence (F v /F m ) was measured separately from the chloroplasts in the adaxial epidermis and lower leaf tissues by using leaf dermal peels. Lamelloplasts and minichloroplasts have much lower photosynthetic efficiency than mesophyll chloroplasts. Nevertheless, photosynthetic proteins (psbA protein of PSII, RuBisCo and ATPase) were detected in both plastids as well as mesophyll chloroplasts in an immunogold labeling. Spectrometry revealed additional blue to blue-green peaks in visually iridescent leaves. Micro-spectrometry detected a blue peak from single blue spots in adaxial epidermal cells confirming that the color is derived from lamelloplasts. Presence of lamelloplasts or minichloroplasts is species specific and exclusive. High prevalence of lamelloplasts in Begoniaceae, including the basal clade Hillebrandia, highlights a unique evolutionary development. These new findings clarify the association between iridescence and lamelloplasts, and with implications for new directions in the study of plastid morphogenesis.

High-throughput Transcriptome Sequencing Reveals the Role of Anthocyanin Metabolism in Begonia semperflorens Under High Light Stress.

Begonia semperflorens is an ornamental perennial herb. The leaves of B. semperflorens turn red under increased light, which increases the ornamental value of the plant. The color of the leaves is determined by anthocyanin metabolism. In B. semperflorens leaves, anthocyanin metabolism is sensitive to external environmental conditions such as temperature, light and hormone levels. To explore this process in detail and to assess gene expression under high light stress, transcriptome analysis was performed by RNA sequencing using the sequencing-by-synthesis method. A total of 83 699 unigenes were isolated, and 51 754 unigenes were annotated using the NR, Swiss-Prot, KEGG, COG, KOG, GO and Pfam databases. Furthermore, many of the differentially expressed genes were related to factors associated with anthocyanin metabolism, which influences the expression of leaf color.

Stomatal clustering in Begonia associates with the kinetics of leaf gaseous exchange and influences water use efficiency.

Stomata are microscopic pores formed by specialized cells in the leaf epidermis and permit gaseous exchange between the interior of the leaf and the atmosphere. Stomata in most plants are separated by at least one epidermal pavement cell and, individually, overlay a single substomatal cavity within the leaf. This spacing is thought to enhance stomatal function. Yet, there are several genera naturally exhibiting stomata in clusters and therefore deviating from the one-cell spacing rule with multiple stomata overlaying a single substomatal cavity. We made use of two Begonia species to investigate whether clustering of stomata alters guard cell dynamics and gas exchange under different light and dark treatments. Begonia plebeja, which forms stomatal clusters, exhibited enhanced kinetics of stomatal conductance and CO2 assimilation upon light stimuli that in turn were translated into greater water use efficiency. Our findings emphasize the importance of spacing in stomatal clusters for gaseous exchange and plant performance under environmentally limited conditions.

Photonic multilayer structure of Begonia chloroplasts enhances photosynthetic efficiency.

Enhanced light harvesting is an area of interest for optimizing both natural photosynthesis and artificial solar energy capture1,2. Iridescence has been shown to exist widely and in diverse forms in plants and other photosynthetic organisms and symbioses3,4, but there has yet to be any direct link demonstrated between iridescence and photosynthesis. Here we show that epidermal chloroplasts, also known as iridoplasts, in shade-dwelling species of Begonia5, notable for their brilliant blue iridescence, have a photonic crystal structure formed from a periodic arrangement of the light-absorbing thylakoid tissue itself. This structure enhances photosynthesis in two ways: by increasing light capture at the predominantly green wavelengths available in shade conditions, and by directly enhancing quantum yield by 5-10% under low-light conditions. These findings together imply that the iridoplast is a highly modified chloroplast structure adapted to make best use of the extremely low-light conditions in the tropical forest understorey in which it is found5,6. A phylogenetically diverse range of shade-dwelling plant species has been found to produce similarly structured chloroplasts7-9, suggesting that the ability to produce chloroplasts whose membranes are organized as a multilayer with photonic properties may be widespread. In fact, given the well-established diversity and plasticity of chloroplasts10,11, our results imply that photonic effects may be important even in plants that do not show any obvious signs of iridescence to the naked eye but where a highly ordered chloroplast structure may present a clear blue reflectance at the microscale. Chloroplasts are generally thought of as purely photochemical; we suggest that one should also think of them as a photonic structure with a complex interplay between control of light propagation, light capture and photochemistry.

Short-day signals are crucial for the induction of anthocyanin biosynthesis in Begonia semperflorens under low temperature condition.

The leaves of Begonia semperflorens accumulate anthocyanins and turn red in autumn in sub-temperate areas. This induction of anthocyanin biosynthesis in autumn has been attributed to the effects of low temperature, but the effects of different light regimes on this process are still being debated. In the present work, short days were found to be necessary for anthocyanin biosynthesis at low temperature. Under the same low-temperature conditions, Begonia seedlings grown under the short-day condition accumulated more carbohydrates and abscisic acid (ABA), which both induce anthocyanin biosynthesis. However, fewer carbohydrates and more gibberellin (GA) accumulated under the long-day conditions to maintain growth, which blocked anthocyanin biosynthesis and resulted in a lack of increases in the activities of dihydroflavonol 4-reductase (DFR) and flavonoid-3-O-glucosyl transferase (UFGT). Consequently, carbon flux, which was altered due to the blockade of anthocyanin synthesis, was channelled into the production of quercetin and phenolic acids but not lignin.

The evolution of sex ratio differences and inflorescence architectures in Begonia (Begoniaceae).

PREMISE OF THE STUDY: A major benefit conferred by monoecy is the ability to alter floral sex ratio in response to selection. In monoecious species that produce flowers of a given sex at set positions on the inflorescence, floral sex ratio may be related to inflorescence architecture. We studied the loci underlying differences in inflorescence architecture between two monoecious Begonia species and related this to floral sex ratios. METHODS: We performed trait comparisons and quantitative trait locus (QTL) mapping in a segregating backcross population between Central American Begonia plebeja and B. conchifolia. We focused on traits related to inflorescence architecture, sex ratios, and other reproductive traits. KEY RESULTS: The inflorescence branching pattern of B. conchifolia was more asymmetric than B. plebeja, which in turn affects the floral sex ratio. Colocalizing QTLs of moderate effect influenced both the number of male flowers and the fate decisions of axillary meristems, demonstrating the close link between inflorescence architecture and sex ratio. Additional QTLs were found for stamen number (30% variance explained, VE) and pollen sterility (12.3% VE). CONCLUSIONS: One way in which Begonia species develop different floral sex ratios is through modifications of their inflorescence architecture. The potential pleiotropic action of QTL on inflorescence branching and floral sex ratios may have major implications for trait evolution and responses to selection. The presence of a single QTL of large effect on stamen number may allow rapid divergence for this key floral trait. We propose candidate loci for stamen number and inflorescence branching for future characterization.

Carbohydrate accumulation may be the proximate trigger of anthocyanin biosynthesis under autumn conditions in Begonia semperflorens.

Many plant leaves appear red in the autumn, and many papers have focused on the environmental factors and role of anthocyanin in this process. However few papers have examined the substances that are induced during this process. We hypothesised that excess sugar accumulation directly induces anthocyanin accumulation under autumn conditions. Using two methods (restricting phloem movement and exogenous sucrose feeding), we found that both surplus photosynthate and exogenous sucrose could induce anthocyanin biosynthesis, corresponding to up-regulation of several enzymes involved in anthocyanin biosynthesis (phenylalanine ammonia lyase, chalcone isomerase, dihydroflavonol 4-reductase and flavonoid 3-O-glucosyl transferase) and in transport (glutathione S-transferase). Our results suggest that excess carbohydrate may be the proximate trigger for induction of anthocyanin biosynthesis in autumn, but only when carbohydrates are accumulated for storage.

How to cheat when you cannot lie? Deceit pollination in Begonia gracilis.

Mimicry between rewarding and non-rewarding flowers within individuals has been accepted as a strategy favored by selection to deceive pollinators. It has been proposed that this mechanism relies on the exploitation of pollinator's sensory biases, but field evidence is still scarce. In this study, we describe the mechanism of deceit pollination in the monoecious herb Begonia gracilis, a species with exposed rewarding structures (pollen) and intersexual mimicry. Specifically, we test the role of mimicry and exploitation of sensory biases on the reproductive success of male (pollination visitation) and female flowers (probability of setting fruits). We show that pollinators' perception of the amount of reward provided by male flowers is influenced by the independent variation in the sizes of the androecium and the perianth. Large rewarding structures and small perianths were preferred by pollinators, suggesting a central role of the relative size of the rewarding structure on pollinators' foraging decisions. Hence, rewarding male flowers cheat pollinators by exploiting their sensory biases, a strategy followed by non-rewarding female flowers. We suggest that intersexual mimicry operates through the functional resemblance of male flowers' deceit strategy. Artificial manipulation of the flowers supports our findings in natural conditions. Overall, we propose that the continuous and independent variation in the size of the perianth and the reproductive organs among male and female flowers could itself be adaptive.

Genome size variation in Begonia.

The genome sizes of a Begonia collection comprising 37 species and 23 hybrids of African, Asiatic, Middle American, and South American origin were screened using flow cytometry. Within the collection, 1C values varied between 0.23 and 1.46 pg DNA. Genome sizes were, in most cases, not positively correlated with chromosome number, but with pollen size. A 12-fold difference in mean chromosome size was found between the genotypes with the largest and smallest chromosomes. In general, chromosomes from South American genotypes were smaller than chromosomes of African, Asian, or Middle American genotypes, except for B. boliviensis and B. pearcei. Cytological chromosome studies in different genotypes showed variable chromosome numbers, length, width, and total chromosome volume, which confirmed the diversity in genome size. Large secondary constrictions were present in several investigated genotypes. These data show that chromosome number and structure exhibit a great deal of variation within the genus Begonia, and likely help to explain the large number of taxa found within the genus.

Optical effects of abaxial anthocyanin on absorption of red wavelengths by understorey species: revisiting the back-scatter hypothesis.

A red/purple coloration of lower (abaxial) leaf surfaces is commonly observed in deeply-shaded understorey plants, especially in the tropics. However, the functional significance of red abaxial coloration, including its role in photosynthetic adaptation, remains unclear. The objective of this study was to test the back-scatter hypothesis for abaxial leaf coloration, which posits that red pigments internally reflect/scatter red light transmitted by the upper leaf surface back into the mesophyll, thereby enhancing photon capture in light-limited environments. Abaxially red/non-red variegated leaves of Begonia heracleifolia (Cham. & Schltdl.) were used to compare reflectance spectra and chlorophyll fluorescence profiles of abaxially anthocyanic (red) and acyanic (non-red) tissues under red light. Photosynthetic gas exchange in response to red light was also compared for abaxially red/non-red leaf sections. The results did not support a back-scattering function, as anthocyanic leaf surfaces were not more reflective of red light than acyanic surfaces. Anthocyanic tissues also did not exhibit any increases in the mesophyll absorbance of red light, or increased photosynthetic gas exchange under red light at any intensity, relative to acyanic tissues. These results suggest that abaxial anthocyanins do not significantly enhance the absorption of red light in the species tested, and alternative functions are discussed.

Evaluation of herbicide combinations for livid amaranth (Amaranthus blitum) control in tuberous begonia (Begonia x tuberhybrida).

In the past years livid amaranth (Amaranthus blitum) is observed increasingly in begonia production fields. Control of weeds in begonia is generally done by a combined application of the soil herbicides isoxaben + simazin followed 10 days later by application of the contact herbicide bentazone. This treatment usually controls the weed population sufficiently with exception of amaranth. In 2003 a field trial was conducted to evaluate control of livid amaranth in tuberous begonia with isoxaben, simazin. S-metolachloor, phenmedipham + desmedipham and bentazone. These herbicides were used as combinations of soil treatment and contact herbicides. The results suggest that a soil treatment of isoxaben + S-metolachloor significantly reduces livid amaranth compared to isoxaben + simazin, without a pronounced negative effect on tuber yield. Application of phenmedipham + desmedipham however did not improve control of livid amaranth compared to bentazone.

Sex choice in plants: facultative adjustment of the sex ratio in the perennial herb Begonia gracilis.

Sex allocation theory predicts that reproducing individuals will increase their fitness by facultatively adjusting their relative investment towards the rarer sex in response to population shifts in operational sex ratio (OSR). The evolution of facultative manipulation of sex ratio depends on the ability of the parents to track the conditions favouring skewed sex allocation and on the mechanism controlling sex allocation. In animals, which have well-developed sensorial mechanisms, facultative adjustment of sex ratios has been demonstrated on many occasions. In this paper, we show that plants have mechanisms that allow them to evaluate the population OSR. We simulated three different conditions of population OSR by manipulating the amount of pollen received by the female flowers of a monoecious herb, and examined the effect of this treatment on the allocation to male vs. female flowers. A shortage of pollen on the stigmas resulted in a more male-skewed sex allocation, whereas plants that experienced a relatively pollen rich environment tended to produce a more female-skewed sex allocation pattern. Our results for Begonia gracilis demonstrate that the individuals of this species are able to respond to the levels of pollination intensity experienced by their female flowers and adjust their patterns of sex allocation in accordance to the expectations of sex allocation theory.

Antioxidant metabolism during acclimation of Begonia x erythrophylla to high light levels.

This study examined the influence of high light levels on antioxidant metabolism and the photosynthetic properties of Begonia x erythrophylla leaves. The pigment composition of shaded leaves and those developing in full sunlight was typical of shade- and sun-leaves, respectively. After 28 d in full sunlight, the preformed leaves of shade plants transferred to full sunlight (transferred-leaves) showed photo-bleaching with lower Chl (a + b) content and Chl a : Chl b ratios than shade-leaves, with Chl (a + b) : carotenoid ratios not significantly different. The variable/maximal fluorescence (Fv/Fm) of sun-leaves was not significantly different from that of shade-leaves, but transferred-leaves had reduced Fv : Fm ratios. Light response curves for the electron transport rate (ETR), the oxidation state of photosystem II (qP) and non-photochemical quenching (NPQ) showed significant differences between the three leaf types, with transferred-leaves not able to acclimate completely to full sunlight, having lower ETR, qP and NPQ values at high light levels than sun-leaves. Transfer to full sunlight caused a rapid increase in H2O2 and lipid hyperoxides, and a slight increase in protein oxidation. Ascorbate and glutathione levels decreased rapidly, as did the size of the total glutathione pool and, in addition to the general oxidation of proteins, rapid decreases in both the initial and total activities of chloroplastic fructose-1,6-bisphosphatase and glyceraldehyde-3-phosphate dehydrogenase were observed. These results suggest that a more oxidizing cellular environment is the likely cause of the photo-bleaching observed upon transfer of shade-leaves to full sunlight. Acclimation of transferred-leaves to full sunlight involved gradual increases in the activities of enzymes involved in antioxidant metabolism, including superoxide dismutase, catalase, glutathione reductase, ascorbate peroxidase, dehydroascorbate reductase and monodehydroascorbate reductase, but the levels of these enzymes still remained at levels lower than those found in sun-leaves.