The role of carotenoids and their derivatives in mediating interactions between insects and their environment

Carotenoids are long conjugated isoprenoid molecules derived mainly from plants and microbial organisms. They are highly diverse, with over 700 identified structures, and are widespread in nature. In addition to their fundamental roles as light-harvesting molecules in photosynthesis, carotenoids serve a variety of functions including visual and colouring pigments, antioxidants and hormone precursors. Although the functions of carotenoids are relatively well studied in plants and vertebrates, studies are severely lacking in insect systems. There is a particular dearth of knowledge on how carotenoids move among trophic levels, influence insect multitrophic interactions and affect evolutionary outcomes. This review explores the known and potential roles that carotenoids and their derivatives have in mediating the ecological interaction of insects with their environment. Throughout the review, we highlight how the fundamental roles of carotenoids in insect physiology might be linked to ecological and evolutionary processes.     

Antioxidant activity of carotenoids

Carotenoids are pigments which play a major role in the protection of plants against photooxidative processes. They are efficient antioxidants scavenging singlet molecular oxygen and peroxyl radicals. In the human organism, carotenoids are part of the antioxidant defense system. They interact synergistically with other antioxidants; mixtures of carotenoids are more effective than single compounds. According to their structure most carotenoids exhibit absorption maxima at around 450 nm. Filtering of blue light has been proposed as a mechanism protecting the macula lutea against photooxidative damage. There is increasing evidence from human studies that carotenoids protect the skin against photooxidative damage.     

Carotenoid biotechnology in plants for nutritionally improved foods

Carotenoids participate in light harvesting and are essential for photoprotection in photosynthetic plant tissues. They also furnish non-photosynthetic flowers and fruits with yellow to red colors to attract animals for pollination and dispersal of seeds. Although animals can not synthesize carotenoids de novo , carotenoid-derived products such as retinoids (including vitamin A) are required as visual pigments and signaling molecules. Dietary carotenoids also provide health benefits based on their antioxidant properties. The main pathway for carotenoid biosynthesis in plants and microorganisms has been virtually elucidated in recent years, and some of the identified biosynthetic genes have been successfully used in metabolic engineering approaches to overproduce carotenoids of interest in plants. Alternative approaches that enhance the metabolic flux to carotenoids by upregulating the production of their isoprenoid precursors or interfere with light-mediated regulation of carotenogenesis have been recently shown to result in increased carotenoid levels. Despite spectacular achievements in the metabolic engineering of plant carotenogenesis, much work is still ahead to better understand the regulation of carotenoid biosynthesis and accumulation in plant cells. New genetic and genomic approaches are now in progress to identify regulatory factors that might significantly contribute to improve the nutritional value of plant-derived foods by increasing their carotenoid levels.     

Making extra room for carotenoids in plant cells: New opportunities for biofortification

Plant carotenoids are essential for photosynthesis and photoprotection and provide colors in the yellow to red range to non-photosynthetic organs such as petals and ripe fruits. They are also the precursors of biologically active molecules not only in plants (including hormones and retrograde signals) but also in animals (including retinoids such as vitamin A). A carotenoid-rich diet has been associated with improved health and cognitive capacity in humans, whereas the use of carotenoids as natural pigments is widespread in the agrofood and cosmetic industries. The nutritional and economic relevance of carotenoids has spurred a large number of biotechnological strategies to enrich plant tissues with carotenoids. Most of such approaches to alter carotenoid contents in plants have been focused on manipulating their biosynthesis or degradation, whereas improving carotenoid sink capacity in plant tissues has received much less attention. Our knowledge on the molecular mechanisms influencing carotenoid storage in plants has substantially grown in the last years, opening new opportunities for carotenoid biofortification. Here we will review these advances with a particular focus on those creating extra room for carotenoids in plant cells either by promoting the differentiation of carotenoid-sequestering structures within plastids or by transferring carotenoid production to the cytosol.     

Metabolic engineering for the microbial production of carotenoids and related products with a focus on the rare C50 carotenoids

Carotenoids, a subfamily of terpenoids, are yellow- to red-colored pigments synthesized by plants, fungi, algae, and bacteria. They are ubiquitous in nature and take over crucial roles in many biological processes as for example photosynthesis, vision, and the quenching of free radicals and singlet oxygen. Due to their color and their potential beneficial effects on human health, carotenoids receive increasing attention. Carotenoids can be classified due to the length of their carbon backbone. Most carotenoids have a C40 backbone, but also C30 and C50 carotenoids are known. All carotenoids are derived from isopentenyl pyrophosphate (IPP) as a common precursor. Pathways leading to IPP as well as metabolic engineering of IPP synthesis and C40 carotenoid production have been reviewed expertly elsewhere. Since C50 carotenoids are synthesized from the C40 carotenoid lycopene, we will summarize common strategies for optimizing lycopene production and we will focus our review on the characteristics, biosynthesis, glycosylation, and overproduction of C50 carotenoids.     

Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids

Plant compounds that are perceived by humans to have color are generally referred to as 'pigments'. Their varied structures and colors have long fascinated chemists and biologists, who have examined their chemical and physical properties, their mode of synthesis, and their physiological and ecological roles. Plant pigments also have a long history of use by humans. The major classes of plant pigments, with the exception of the chlorophylls, are reviewed here. Anthocyanins, a class of flavonoids derived ultimately from phenylalanine, are water-soluble, synthesized in the cytosol, and localized in vacuoles. They provide a wide range of colors ranging from orange/red to violet/blue. In addition to various modifications to their structures, their specific color also depends on co-pigments, metal ions and pH. They are widely distributed in the plant kingdom. The lipid-soluble, yellow-to-red carotenoids, a subclass of terpenoids, are also distributed ubiquitously in plants. They are synthesized in chloroplasts and are essential to the integrity of the photosynthetic apparatus. Betalains, also conferring yellow-to-red colors, are nitrogen-containing water-soluble compounds derived from tyrosine that are found only in a limited number of plant lineages. In contrast to anthocyanins and carotenoids, the biosynthetic pathway of betalains is only partially understood. All three classes of pigments act as visible signals to attract insects, birds and animals for pollination and seed dispersal. They also protect plants from damage caused by UV and visible light.     

Recent progress in structural studies of carotenoids in animals and plants

About 750 naturally occurring carotenoids had been reported as of 2004. Furthermore, annually, more than 20 new structures of carotenoids are reported. Improvements of analytical instruments such as NMR, MS, HPLC, etc., have made it possible to perform the structural elucidation of very minor carotenoids in nature. Interesting new structural carotenoids can still be identified in aquatic animals and higher plants. The present paper provides a review of new structural carotenoids isolated from aquatic animals and higher plants by our group over the last five years.     

植物类胡萝卜素生物合成及功能

详述了植物类胡萝卜素生物合成途径,并从突破类胡萝卜素合成途径中上游瓶颈限制、类胡萝卜素代谢各分支途径的改造、提高植物细胞对类胡萝卜素物质积累能力三个方面探讨了类胡萝卜素生物合成酶基因在植物基因工程中的研究现状,最后对植物类胡萝卜素代谢的研究前景进行了展望。     

Physiological roles of plastid terminal oxidase in plant stress responses

The plastid terminal oxidase (PTOX) is a plastoquinol oxidase localized in the plastids of plants. It is able to transfer electrons from plastoquinone (PQ) to molecular oxygen with the formation of water. Recent studies have suggested that PTOX is beneficial for plants under environmental stresses, since it is involved in the synthesis of photoprotective carotenoids and chlororespiration, which could potentially protect the chloroplast electron transport chain (ETC) from over-reduction. The absence of PTOX in plants usually results in photo-bleached variegated leaves and impaired adaptation to environment alteration. Although PTOX level and activity has been found to increase under a wide range of stress conditions, the functions of plant PTOX in stress responses are still disputed now. In this paper, the possible physiological roles of PTOX in plant stress responses are discussed based on the recent progress.     

Metabolic engineering of ketocarotenoid formation in higher plants

Although higher plants synthesize carotenoids, they do not possess the ability to form ketocarotenoids. In order to generate higher plants capable of synthesizing combinations of ketolated and hydroxylated carotenoids the genes responsible for the carotene 4,4' oxygenase and 3,3' hydroxylase have been transformed into tomato and tobacco. The gene products were produced as a polyprotein. Subsequent cleavage of the polyprotein, targeting of the two enzymes to the plastid and enzyme activities have been shown for both gene products. Metabolite profiling has shown the formation of ketolated carotenoids from beta-carotene and its hydroxylated intermediates in tobacco and tomato leaf. In the nectary tissues of tobacco flowers a quantitative increase (10-fold) as well as compositional changes were evident, including the presence of astaxanthin, canthaxanthin and 4-ketozeaxanthin. Interestingly, in this tissue the newly formed carotenoids resided predominantly as esters. These data are discussed in terms of metabolic engineering of carotenoids and their sequestration in higher plant tissues.     

Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism

The xanthophyll cycle has a major role in protecting plants from photooxidative stress, although the mechanism of its action is unclear. Here, we have investigated Arabidopsis plants overexpressing a gene encoding beta-carotene hydroxylase, containing nearly three times the amount of xanthophyll cycle carotenoids present in the wild-type. In high light at low temperature wild-type plants exhibited symptoms of severe oxidative stress: lipid peroxidation, chlorophyll bleaching, and photoinhibition. In transformed plants, which accumulate over twice as much zeaxanthin as the wild-type, these symptoms were significantly ameliorated. The capacity of non-photochemical quenching is not significantly different in transformed plants compared with wild-type and therefore an enhancement of this process cannot be the cause of the stress tolerant phenotype. Rather, it is concluded that it results from the antioxidant effect of zeaxanthin. 80-90% of violaxanthin and zeaxanthin in wild-type and transformed plants was localized to an oligomeric LHCII fraction prepared from thylakoid membranes. The binding of these pigments in intact membranes was confirmed by resonance Raman spectroscopy. Based on the structural model of LHCII, we suggest that the protein/lipid interface is the active site for the antioxidant activity of zeaxanthin, which mediates stress tolerance by the protection of bound lipids.     

Impact and interaction of lipophilic antioxidants in mutants and transgenic plants

Carotenoids and tocopherols are lipophilic antioxidants with important functions in plants and humans. Due to their nutritional value and putative health benefits, they have become a focus of intensive research. The identification of all genes of the carotenoid and tocopherol biosynthesis has enabled the manipulation of their biosynthetic pathways, aiming for quantitative and qualitative improvement. In plants, carotenoids and tocopherols are of crucial importance because of their protective abilities, which help to keep them alive even under light stress conditions. A wealth of information has accumulated concerning the responses of plants to various environmental stress factors. Here, we summarize some of the recent data concentrating on the impact and possible interaction of lipophilic antioxidants in mutants and transgenic plants with altered status of lipophilic antioxidants.     

The biosynthesis and nutritional uses of carotenoids

Carotenoids are isoprenoid molecules that are widespread in nature and are typically seen as pigments in fruits, flowers, birds and crustacea. Animals are unable to synthesise carotenoids de novo, and rely upon the diet as a source of these compounds. Over recent years there has been considerable interest in dietary carotenoids with respect to their potential in alleviating age-related diseases in humans. This attention has been mirrored by significant advances in cloning most of the carotenoid genes and in the genetic manipulation of crop plants with the intention of increasing levels in the diet. The aim of this article is to review our current understanding of carotenoid formation, to explain the perceived benefits of carotenoids in the diet and review the efforts that have been made to increase carotenoids in certain crop plants.     

Carotenoids and Environmental Stress in Plants: Significance of Carotenoid-Mediated Modulation of Membrane Physical Properties

Carotenoids, apart of their antenna function in photosynthesis, play an important role in the mechanisms protecting the photosynthetic apparatus against various harmful environmental factors. They protect plants against overexcitation in strong light and dissipate the excess of absorbed energy, they scavenge reactive oxygen species formed during photooxidative stress and moderate the effect of extreme temperatures. One of the important factors involved in the protective action of carotenoids is their influence on the molecular dynamics of membranes. To obtain complex information about interactions between carotenoids and lipids in a membrane, different techniques were used. In this review, the data resulting from EPR–spin label spectrometry, ³¹P- and ¹³C-NMR, differential scanning calorimetry, and computer simulation of the membrane molecular dynamics are presented. The effects of selected, structurally different carotenoid species on various physical parameters of model and natural membranes are described and their relevance to protection against some environmental stresses are discussed.     

Protective effect of jasmonic acid and potassium against cadmium stress in peas (Pisum sativum L.)

A combination of mineral nutrients and plant growth regulators should be assessed to improve crop performance under various abiotic stresses. There is a need to include plant growth regulators in fertilization regime of various crops along with essential mineral nutrients, especially when they are irrigated with polluted water with higher levels of heavy metals. The performance of pea was evaluated under cadmium (Cd) stress coupled with potassium (K) and jasmonic acid (JA) supplementation. The Cd stress (50 μM) was applied to soil (sandy loam) grown pea plants as basal dose after a month of sowing. The control and stressed plants were then supplemented with K (5 M), JA (0.5 mM) and their collective application along with control as distilled water. Cd stress showed a marked reduction in growth pattern, however, the collective supplementation sufficiently improved the growth pattern of stressed peas plants as evidenced by improvement in shoot length (cm), root length (cm), number of leaves per plant, leaf area (cm²), plant fresh and dry weight (gm). Potassium application under Cd stress significantly enhanced internodal distance (cm) while the number of seeds per pod and relative water contents remained nonsignificant. The applied treatment (JA + K) under Cd stress prominently improved enzymatic activities, which were measured as nitrate reductase activity (NRA), nitrite reductase activity (NiRA), superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT). Cd stress impacted the biochemical profile by enhancing antioxidant capacity (AC), antioxidant activity (AA), total phenols (TP), while reducing total soluble protein (TSP), chlorophyll ‘a’, chlorophyll ‘b’ and carotenoids. The combined application of JA and K under Cd stress enhanced AC, AA, TP, Chl a and b, TSP and carotenoids. The results indicate that foliar application of JA and K efficiently negated the harmful effects of Cd stress on peas.     

Chromoplast biogenesis and carotenoid accumulation

Chromoplasts are special organelles that possess superior ability to synthesize and store massive amounts of carotenoids. They are responsible for the distinctive colors found in fruits, flowers, and roots. Chromoplasts exhibit various morphologies and are derived from either pre-existing chloroplasts or other non-photosynthetic plastids such as proplastids, leucoplasts or amyloplasts. While little is known about the molecular mechanisms underlying chromoplast biogenesis, research progress along with proteomics study of chromoplast proteomes signifies various processes and factors important for chromoplast differentiation and development. Chromoplasts act as a metabolic sink that enables great biosynthesis and high storage capacity of carotenoids. The formation of chromoplasts enhances carotenoid metabolic sink strength and controls carotenoid accumulation in plants. The objective of this review is to provide an integrated view on our understanding of chromoplast biogenesis and carotenoid accumulation in plants.     

The current concepts of functional role of carotenoids in the eukaryotic chloroplasts

Current state of knowledge of functional role of carotenoids in algal and higher plant chloroplasts is reviewed. Basic functions of carotenoids are shown to be light-protective, light-absorbing, and structural, as well as participating in photochemical processes of photosystems I and II. Such xanthophylls as neoxanthin, fucoxanthin, peridinin and alloxanthin, which have allenic or acetylenic bond, mostly function as light-absorbers. They transmit absorbed energy to chlorophyll b. Other xanthophylls occupying certain strictly specified loci in light-absorbing chlorophyll-a/b-protein complexes of photosystems have either structural function (lutein) or light-protective function (zeaxanthin, antheraxanthin, violaxanthin). Carotenoids of xanthophyll cycles preserve chlorophylls and lipids of photosynthetic membranes from photodestruction at overlighting in the presence of oxygen. In eukaryotic chloroplasts, three types of xanthophyll cycles were found: violaxanthin, lutein-5,6-epoxide, and diadinoxanthin. The similarities and dissimilarities between epoxidation and de-epoxidation reactions of these cycles are discussed in detail in the present work. The pattern of occurrence of xanthophyll cycles among higher plants and freshwater and marine algae is outlined.     

Transformation of beta-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco

Inhibition of lycopene cyclization decreased the salt tolerance of the euhalophyte Salicornia europaea L. We isolated a β-lycopene cyclase gene SeLCY from S. europaea and transformed it into Arabidopsis with stable expression. Transgenic Arabidopsis on post-germination exhibited enhanced tolerance to oxidative and salt stress. After 8 and 21 d recovery from 200 mM NaCl treatment, transgenic lines had a higher survival ratio than wild-type (WT) plants. Three-week-old transgenic plants treated with 200 mM NaCl showed better growth than the WT with higher photosystem activity and less H(2)O(2) accumulation. Determination of endogenous pigments of Arabidopsis treated with 200 mM NaCl for 0, 2 or 4 d demonstrated that the transgenic plants retained higher contents of carotenoids than the WT. Furthermore, to compare the difference between SeLCY and AtLCY from Arabidopsis, we used viral vector mediating ectopic expression of SeLCY and AtLCY in Nicotiana benthamiana. Although LCY genes transformation increased the salt tolerance in tobacco, there is no significant difference between SeLCY- and AtLCY-transformed plants. These findings indicate that SeLCY transgenic Arabidopsis improved salt tolerance by increasing synthesis of carotenoids, which impairs reactive oxygen species and protects the photosynthesis system under salt stress, and as a single gene, SeLCY functionally showed no advantage for salt tolerance improvement compared with AtLCY.     

Photosynthetic pigments of tomato under conditions of biotic stress and effects of furostanol glycosides

Adaptogenic effect of furostanol glycosides (FG) on biosynthesis of photosynthetic pigments in tomato plants (Lycopersicon esculentum Mill.) were studied under conditions of biotic stress caused by root-knot nematode (Meloidogyne incognita Kofoid et White). Treatment of plants with 5 x 10(-4) M FG was accompanied by an increase in the rate of biosynthesis of pigments (particularly, chlorophyll b and carotenoids), which was observed against the background of a decrease in the relative contribution of beta-carotene and an increase in the relative contribution of pigments of violaxanthin cycle (VXC) to the overall pool of carotenoids. It was suggested that FG stimulated phytoimmunity by shifting metabolism of carotenoids toward enhanced biosynthesis of VXC pigments. These pigments play a protective role and facilitate stabilization of photosynthetic apparatus, which is particularly important under stress conditions.