Genus Clusia Research Articles

Biological Activities of Species of the Genus Clusia L (Clusiaceae): A General Approach.

The genus Clusia L. is highly diverse in Central and South America, comprising about 300 species, including trees and shrubs, hemiepiphytes, epiphytes, and lianas. This genus deserves attention due to its wide range of biological activities. Clusia belongs to the Clusiaceae family, chemically characterized by the presence of xanthones, benzophenones, flavonoids, coumarins, terpenoids, and other substances with bioactive activity already described. This review aims to highlight the biological activity associated to extracts and isolated substances from species of the Clusia genus, including anti-HIV, antimicrobial, antioxidant, antinociceptive, antitumor, leishmanicidal, modulator of inflammatory processes, neutralization of toxic effects caused by snake bites, and others. This review gathered information on biological activities associated with different types of extracts and isolated substances of the genus Clusia, traditional use, chemical profile, and biological properties of plants of the genus, published in the last 23 years (1998 to 2021) and that can provide support for future research. The paper aims to provide an overview of existing knowledge about the biological properties of the genus Clusia plant species.

A multiplex approach of MS, 1D-, and 2D-NMR metabolomics in plant ontogeny: A case study on Clusia minor L. organs (leaf, flower, fruit, and seed).

The genus Clusia L. is mostly recognised for the production of prenylated benzophenones and tocotrienol derivatives. The objective of this study was to map metabolome variation within Clusia minor organs at different developmental stages. In total 15 organs/stages (leaf, flower, fruit, and seed) were analysed by UPLC-MS and 1H- and heteronuclear multiple-bond correlation (HMBC)-NMR-based metabolomics. This work led to the assignment of 46 metabolites, belonging to organic acids(1), sugars(2) phenolic acids(1), flavonoids(3) prenylated xanthones(1) benzophenones(4) and tocotrienols(2). Multivariate data analyses explained the variability and classification of samples, highlighting chemical markers that discriminate each organ/stage. Leaves were found to be rich in 5-hydroxy-8-methyltocotrienol (8.5 μg/mg f.w.), while flowers were abundant in the polyprenylated benzophenone nemorosone with maximum level detected in the fully mature flower bud (43 μg/mg f.w.). Nemorosone and 5-hydroxy tocotrienoloic acid were isolated from FL6 for full structural characterisation. This is the first report of the NMR assignments of 5-hydroxy tocotrienoloic acid, and its maximum level was detected in the mature fruit at 50 μg/mg f.w. Seeds as typical storage organ were rich in sugars and omega-6 fatty acids. To the best of our knowledge, this is the first report on a comparative 1D-/2D-NMR approach to assess compositional differences in ontogeny studies compared with LC-MS exemplified by Clusia organs. Results derived from this study provide better understanding of the stages at which maximal production of natural compounds occur and elucidate in which developmental stages the enzymes responsible for the production of such metabolites are preferentially expressed.

Elevated nocturnal respiratory rates in the mitochondria of CAM plants: current knowledge and unanswered questions.

Crassulacean acid metabolism (CAM) is a metabolic adaptation that has evolved convergently in 38 plant families to aid survival in water-limited niches. Whilst primarily considered a photosynthetic adaptation, CAM also has substantial consequences for nocturnal respiratory metabolism. Here, we outline the history, current state and future of nocturnal respiration research in CAM plants, with a particular focus on the energetics of nocturnal respiratory oxygen consumption. Throughout the 20th century, research interest in nocturnal respiration occurred alongside initial discoveries of CAM, although the energetic and mechanistic implications of nocturnal oxygen consumption and links to the operation of the CAM cycle were not fully understood. Recent flux balance analysis (FBA) models have provided new insights into the role that mitochondria play in the CAM cycle. Several FBA models have predicted that CAM requires elevated nocturnal respiratory rates, compared to C3 species, to power vacuolar malic acid accumulation. We provide physiological data, from the genus Clusia, to corroborate these modelling predictions, thereby reinforcing the importance of elevated nocturnal respiratory rates for CAM. Finally, we outline five unanswered questions pertaining to nocturnal respiration which must be addressed if we are to fully understand and utilize CAM plants in a hotter, drier world.

First records of the druid fly genus Clusia Haliday, 1838 (Diptera, Clusiidae), with two new species from China

The druid fly genus Clusia was firstly recorded from China, including two new species: C. luteimacula sp. nov. from Yintiaoling Nature Reserve of Chongqing and C. sinensis sp. nov. from Wanglang of Sichuan and Mt. Taibai of Shaanxi. A key to all species of Clusia globally is presented.

Leaf vein density correlates with crassulacean acid metabolism, but not hydraulic capacitance, in the genus Clusia.

Many succulent species are characterized by the presence of Crassulacean acid metabolism (CAM) and/or elevated bulk hydraulic capacitance (CFT). Both CAM and elevated CFT substantially reduce the rate at which water moves through transpiring leaves. However, little is known about how these physiological adaptations are coordinated with leaf vascular architecture. The genus Clusia contains species spanning the entire C3-CAM continuum, and also is known to have >5-fold interspecific variation in CFT. We used this highly diverse genus to explore how interspecific variation in leaf vein density is coordinated with CAM and CFT. We found that constitutive CAM phenotypes were associated with lower vein length per leaf area (VLA) and vein termini density (VTD), compared to C3 or facultative CAM species. However, when vein densities were standardized by leaf thickness, this value was higher in CAM than C3 species, which is probably an adaptation to overcome apoplastic hydraulic resistance in deep chlorenchyma tissue. In contrast, CFT did not correlate with any xylem anatomical trait measured, suggesting CAM has a greater impact on leaf transpiration rates than CFT. Our findings strongly suggest that CAM photosynthesis is coordinated with leaf vein densities. The link between CAM and vascular anatomy will be important to consider when attempting to bioengineer CAM into C3 crops.

Dissecting succulence: Crassulacean acid metabolism and hydraulic capacitance are independent adaptations in Clusia leaves.

Succulence is found across the world as an adaptation to water-limited niches. The fleshy organs of succulent plants develop via enlarged photosynthetic chlorenchyma and/or achlorophyllous water storage hydrenchyma cells. The precise mechanism by which anatomical traits contribute to drought tolerance is unclear, as the effect of succulence is multifaceted. Large cells are believed to provide space for nocturnal storage of malic acid fixed by crassulacean acid metabolism (CAM), whilst also buffering water potentials by elevating hydraulic capacitance (CFT ). The effect of CAM and elevated CFT on growth and water conservation have not been compared, despite the assumption that these adaptations often occur together. We assessed the relationship between succulent anatomical adaptations, CAM, and CFT , across the genus Clusia. We also simulated the effects of CAM and CFT on growth and water conservation during drought using the Photo3 model. Within Clusia leaves, CAM and CFT are independent traits: CAM requires large palisade chlorenchyma cells, whereas hydrenchyma tissue governs interspecific differences in CFT . In addition, our model suggests that CAM supersedes CFT as a means to maximise CO2 assimilation and minimise transpiration during drought. Our study challenges the assumption that CAM and CFT are mutually dependent traits within succulent leaves.

Physiological ecology of Mexican CAM plants: history, progress, and opportunities

In Mexico, plants with crassulacean acid metabolism (CAM) are part of the Mexican culture, have different uses and are even emblematic. Unfortunately, only a small fraction of the Mexican CAM plants has been studied physiologically. For this review, the following questions were considered: What ecophysiological studies have been conducted with CAM species native to Mexico? What ecophysiological processes in Mexican CAM plants are the most studied? What type of ecophysiological studies with CAM plants are still needed? A database of scientific studies on CAM plant species from Mexico was documented, including field and laboratory works for species widely distributed, and those studies made outside Mexico with Mexican species. Physiological processes were grouped as germination, photosynthesis, and water relations. Most studies were done for CAM species of Cactaceae, Bromeliaceae, Asparagaceae and Orchidaceae, andmost ecophysiological studies have been done on germination of cacti. Field and laboratory studies on photosynthesis and water relations were mostly for terrestrial cacti and epiphytic bromeliads. There were few physiological studies with CAM seedlings in Mexico and few studies using stable isotopes of water and carbon of CAM plants in the field. More field and laboratory studies of physiological responses and plasticity of CAM plants to multiple stress factors are required to model plant responses to global climate change. In general, more physiological studies are essential for all CAM species and for species of the genus Clusia , with C3-CAM and CAM members, which can become ecologically important under some climate change scenarios.

Updating the occurrence of crassulacean acid metabolism (CAM) in the genus Clusia through carbon isotope analysis of species from Colombia.

Clusia is a widely distributed neotropical genus with 321 currently described species. This remarkable genus is the only one known to contain trees sensu stricto with CAM photosynthesis. To survey the occurrence of CAM in Clusia species from Colombia, we determined the leaf stable carbon isotope composition (δ13C) of 568 specimens from 114 species deposited in 12 Colombian herbaria. In the vast majority of specimens, δ13C values indicated that C3 photosynthesis was the principal contributor to carbon gain. δ13C values typical of strong CAM (less negative than -20‰) were observed in only five species, in four of them for the first time. All samples with CAM-type isotopic signatures were collected below 1,000 m a.s.l., whereas species with predominantly C3 occurred from sea level to 3,500 m a.s.l. Together with information already available in the literature, we conclude that CAM is present in 22% (35/156) of the species of Clusia investigated thus far.

Clusia suborbicularis is not a synonym of Clusia flava: Molecular and metabolomic evidence

AbstractThe genus Clusia (Clusiaceae) is notorious for its difficult taxonomy; most species are dioecious, with distantly related species having similar morphology, and closely related species having cryptic morphological differences. Because of this, Clusia spp. are often misidentified or, as in the case of C. suborbicularis and C. flava, considered to be the same species. Chemometric analyses of the HPLC metabolic profiles from bark extracts of C. suborbicularis and C. flava, combined with molecular evidence from ITS molecular markers were used to establish the metabolomic similarities and phylogenetic relationship between C. suborbicularis and C. flava, previously identified on the basis of their morphological characteristics. The principal component analyses of the HPLC metabolic profiles of bark extracts from individuals of C. suborbicularis and C. flava showed significant differences, suggesting they should be recognized as distinct species. This assumption was confirmed by phylogenetic reconstructions based on the molecular marker ITS. Furthermore, a theoretical geographical distribution analysis suggests C. suborbicularis could be considered a native species to the Yucatán Peninsula. The results from this investigation support C. suborbicularis as a distinct species, and not a synonym of C. flava. The identification of these two species represents a relevant contribution for the cataloguing, conservation and bioprospecting of Clusia spp. occurring in the Yucatán Peninsula.

Chemical constituents isolated from Clusia criuva subsp. Criuva and their chemophenetics significance

Clusia criuva belongs to the Clusiaceae family and it is endemic to the rupestrian fields in Chapada Diamantina National Park (Brazil). Phytochemical investigation of C. criuva trunks led to the isolation of five triterpenoids [winchic acid (1), betulinic acid (2), lupeol (3), friedelin (4), and friedelinol (5)], four steroids [lanosterol (6), stigmasterol (7), β-sitosterol (8), and sitostenone (9)], seven polyprenylated benzophenone derivatives [propolone A (10), propolone B (11), propolone C (12), propolone D (13), sampsonione B (14), hyperisampsin E (15), and hyperisampsin F (16)], four xanthones [neriifolone C (17), 6-deoxyisojacareubin (18), osajaxanthone F (19), and brasilixanthone B (20)], two biphenyls [aucuparina (21) and 2,2-dimethyl-5-hydroxy-7-phenylchromene (22)], and two tocotrienol derivatives [2Z- and 2E-δ-tocotrienoloic acids (23 and 24)]. Compounds 1, 11, 12, 15, and 16 were isolated for the first time in the Clusiaceae family, compounds 17, 19 and 21 were isolated for the first time in the genus Clusia, whereas 2–10, 13, 14, 18, 20, 22–24 were isolated for the first time in Clusia criuva. Compounds 1, 2, 11, 12, 13 and 15 showed potent in vitro cytotoxic activity against GL-15 glioblastoma-derived human cell line. Chemophenetics significance of these compounds is described herein.

Crassulacean acid metabolism (CAM) supersedes the turgor loss point (TLP) as an important adaptation across a precipitation gradient, in the genus Clusia.

As future climates continue to change, precipitation deficits are expected to become more severe across tropical ecosystems. As a result, it is important that we identify plant physiological traits that act as adaptations to drought, and determine whether these traits act synergistically or independently of each other. In this study, we assessed the role of three leaf-level putative adaptations to drought: crassulacean acid metabolism (CAM), the turgor loss point (TLPΨ) and water storage hydrenchyma tissue. Using the genus Clusia as a model, we were able to explore the extent to which these leaf physiological traits co-vary, and also how they contribute to species' distributions across a precipitation gradient in Central and South America. We found that CAM is independent of the TLPΨ and hydrenchyma depth in Clusia. In addition, we provide evidence that constitutive CAM is an adaptation to year-long water deficits, whereas facultative CAM appears to be more important for surviving acute dry seasons. Finally, we find that the other leaf traits tested did not correlate with environmental precipitation, suggesting that the reduced transpirational rates associated with CAM obviate the need to adapt the TLPΨ and hydrenchyma depth in this genus.

Novel polyprenylated benzophenone derivatives from Clusia burle-marxii

Three new caged polyprenylated benzophenone derivatives named burlemarxiones D-F (1–3) were isolated from the hexane extract of Clusia burle-marxii trunks. Burlemarxione D (1) contains the tetracyclo[8.3.1.03,11.05,10]tetradecane core skeleton also observed for burlemarxione A, its probable immediate precursor. However, two additional rings are formed to produce an unprecedented complex-caged core skeleton. These additional rings could be formed by a radical cyclization reaction of one prenyl group at C-5 with C-1 and C-33, followed by oxidative dehydrogenation (rearomatization) or by an intramolecular [4 + 2] radical cycloaddition (Diels-Alder reaction), followed by an enolization reaction (rearomatization). Burlemarxiones E and F were isolated after methylation with diazomethane that was necessary to avoid the interconversion of the pair of β-diketones in tautomeric equilibrium. The proposed biosynthetic pathway for burlemarxiones D-F involves the condensation of either lavandulyl pyrophosphate or 2-(1-methylvinyl)-hexa-5-enyl pyrophosphate with the acylphloroglucinol derivative 6-benzoyl-5-hydroxy-5-cyclohexen-1,3-dione, followed by consecutive prenylation reactions. Therefore, Clusia burle-marxii reinforces the claim that the genus Clusia is an important source of sophisticated caged polyprenylated benzophenone derivatives.

New perspectives on secretory structures inClusia(Clusiaceae – Clusiod clade): production of latex or resins?

The Clusioid clade is quite diverse, encompassing the five families Clusiaceae, Bonnetiaceae, Calophyllaceae, Hypericaceae, and Podostemaceae. However, its members have important synapomorphies, such as the presence of xanthones, polyisoprenylated benzophenones, and quinones, as well as schizogenous secretory ducts and cavities, and tenuinucellate ovules. Owing to the milky appearance of the exudate present in ducts of these families (except Bonnetiaceae), many authors have referred to this secretion as latex, while others have preferred to use the term resin. Faced with this confusion about the description of the exudate present in Clusiaceae, the aim of this study was to identify which classes of substances are being produced by those structures in the genus Clusia, compared with other members of Clusiaceae and the Clusioid clade in general. Furthermore, we describe the structure and distribution of the secretory ducts in species of Clusia, as well as a detailed histochemical study. These secretory ducts secrete an exudate of variable composition, but predominantly terpenic. We conclude that Clusia, as well as some representatives of the Clusioid clade, do not have latex but resiniferous secretory ducts.

Playing the Taxonomic Cupid: Matching Pistillate and Staminate Conspecifics in Dioecious Clusia (Clusiaceae)

Abstract—Dioecious reproduction, in which unisexual flowers are developed in separate individuals, is an uncommon characteristic that has evolved multiple times independently in angiosperms. Nearly all species in the neotropical genus Clusia are dioecious and most of them are incompletely known because only one sexual morph, either the staminate or the pistillate individual, has been described. Here we explored the variability in chloroplast regions atpF intron, matK, ndhA intron, petL-psbE, rpl16 intron, as well as the nrDNA ITS to evaluate conspecificity between staminate and pistillate individuals within the genus Clusia. Our results indicate that phylogenetic analyses using maximum likelihood and Bayesian inference based on nrDNA ITS data is a suitable approach to assess whether sexual morphs are conspecifics and to estimate species phylogenetic position within the genus. Staminate and pistillate individuals were effectively identified for Clusia araracuarae, C. lundellii, C. stenophylla, and C. uvitana. Distribution maps as well as full morphological descriptions for these species are provided along with comments on their phylogenetic relationships.

Taxonomic novelties in Clusia (Clusiaceae) from Venezuela

Although a comprehensive taxonomic treatment of the genus Clusia in the Venezuelan Guayana was published 20 years ago, much taxonomic work remains to be done regarding the genus in the region, including description of new species. In this paper we describe and illustrate five new species of Clusia sect. Oedematopus (Clusia dickinsoniana, C. donramonii, C. peterstevensii, C. punctata and C. tetramera), which are characterized by their small flowers without resin or nectar secretion.

Clusia hirsuta, a New Species from Clusia sect. Retinostemon and the First Description of Trichomes in the Genus

Clusia hirsuta Hammel (Clusiaceae), a new species from the Pacific wet forest in Colombia and Ecuador, is described. Trichomes are reported here for the first time in the genus and described using micromorphological techniques. Morphological and molecular data are used to establish the phylogenetic position of this newly described taxon within the genus Clusia L.

Manipulus Guttiferarum, II. First record of Clusia ucamira (Clusiaceae) from Venezuelan Guayana

As part of a review in progress on the genus Clusia Linnaeus in Venezuela, Clusia ucamira J.E. Nascim. & Bittrich is reported for the first time for that country. Clusia ucamira is quickly distinguished from similar species of Clusia sect. Oedematopus (Planchon & Triana) Pipoly by its hemiepiphitic habit, strongly coriaceous and conspicuously revolute leaves, with a very prominent midvein in the abaxial surface. With this range extension, Clusia ucamira is known, besides from the Amazon basin, from terra firme forest in the Amazonas state of Venezuela, where it grows in oligotrophic soils derived from materials from the Guayana Shield. In Venezuela, this species is to be considered Least Concerned (LC), according to the IUCN Red List categories.

A new Amazon species of Clusia sect. Brachystemon (Clusiaceae)

In this paper we describe and illustrate a new species of the genus Clusia (Clusiaceae) and compare it with morphologically most similar species. The new species, Clusia rubrifructa, occurs in Amazon lowland forests of Brazil, Colombia and Peru.

Features of CAM-cycling expressed in the dry season by terrestrial and epiphytic plants of Clusia arrudae Planchon & Triana in two rupestrian savannas of southeastern Brazil in comparison to the C3-species Eremanthus glomerulatus Less.

In rupestrian savannas in southeastern Brazil Clusia arrudae Planchon & Triana in the dry season performed CAM-cycling with very little gas exchange in the early morning followed by a long depression during the rest of the day. CAM-cycling is considered as a survival strategy under drought and the productivity of the plant which is quite abundant must rely on performance of C 3 -photosynthesis in more favorable seasons. In rupestrian savannas in the Serra do Cipo (19°14′48.9″S, 43°30′36.0″W) at 1300 m a.s.l. and in the Serra de Sao Jose (21°08′S, 44°17′W) at 1010–1030 m a.s.l. in southeastern Brazil Clusia arrudae Planchon & Triana is abundant. As CAM is frequent in the genus Clusia we supposed that it would perform CAM as a drought adaptation at the very dry rupestrian savanna sites in the dry season. At the Serra do Cipo site as control we studied the obligate C3-species Eremanthus glomerulatus Less. Both species are sympatric at this site. Eremanthus glomerulatus performed C3-photosynthesis with a midday depression. The patterns of C. arrudae were completely different so that genuine C3-photosynthesis was excluded, but they were also not typical of CAM. The stomata were almost closed during the night. Some stomatal opening and net CO2 uptake occurred in the early morning hours followed by a long depression with stomatal closure throughout the rest of the day. Nevertheless, photo inhibition was limited and photosynthetic electron transport rate remained high during this time indicating that photosynthetic excitation energy was required and suggesting that CO2 assimilation was continuing behind closed stomata based on internal sources of CO2. There was some nocturnal accumulation of organic acids (malic and citric acids) which could represent a source of CO2 during the light period. Overall, the observations can be best explained by the performance of CAM-cycling by C. arrudae. However, leaf carbon gain of C. arrudae was much inferior to that of E. glomerulatus. CAM-cycling appears to be a strategy for protection from photoinhibitory damage and survival under strong conditions of drought. Steeper more vertical leaf positions observed would assist reducing overheating during stomatal closure at high irradiance. The abundance of C. arrudae suggests that the plant must have other means to sustain productivity such as full C3-photosynthesis in the more favorable seasons.

Climate‐resilient agroforestry: physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy

Global climate change threatens the sustainability of agriculture and agroforestry worldwide through increased heat, drought, surface evaporation and associated soil drying. Exposure of crops and forests to warmer and drier environments will increase leaf:air water vapour-pressure deficits (VPD), and will result in increased drought susceptibility and reduced productivity, not only in arid regions but also in tropical regions with seasonal dry periods. Fast-growing, short-rotation forestry (SRF) bioenergy crops such as poplar (Populus spp.) and willow (Salix spp.) are particularly susceptible to hydraulic failure following drought stress due to their isohydric nature and relatively high stomatal conductance. One approach to sustaining plant productivity is to improve water-use efficiency (WUE) by engineering crassulacean acid metabolism (CAM) into C3 crops. CAM improves WUE by shifting stomatal opening and primary CO2 uptake and fixation to the night-time when leaf:air VPD is low. CAM members of the tree genus Clusia exemplify the compatibility of CAM performance within tree species and highlight CAM as a mechanism to conserve water and maintain carbon uptake during drought conditions. The introduction of bioengineered CAM into SRF bioenergy trees is a potentially viable path to sustaining agroforestry production systems in the face of a globally changing climate.