Amaranthaceae species found in Brazil, identifying those endemics to Brazil and the ones found in the Neotropical Savannah (Cerrado), level of threat, habit, popular name (mostly in Portuguese) and some of the knowledge about the species.
\r\n\t
\r\n\tGenetic predisposition is converted into a pathological phenotype only under the effect of environmental factors.
\r\n\tMultifactorial disorders are considered to be the most common features that affect people, such as diabetes, high blood pressure, coronary heart disease, and cancer, as well as some of the common isolated birth defects, including cleft lip or palate, neural tube defects, congenital heart disease, and clubfoot.
\r\n\t
\r\n\tMultifactorial inheritance did not follow a simple Mendelian pattern. However, the recurrence risk of multifactorial disorders is higher in relatives of affected individuals than in the general population. The empirical risks of a multifactorial disorder are based on large population studies.
\r\n\t
\r\n\tIt is important to understand the multifactorial transmission model for proper genetic counseling and for avoiding environmental factors, a measure that could ensure the prophylaxis of these common diseases.
\r\n\tThis book intends to provide valuable evidence-based information, a comprehensive overview of this complex pathology. The aim will be to highlight the importance of collaboration and multidisciplinary teams for multifactorial disease management in an easy-to-follow format.
Brazil is the first in a ranking of 17 countries in megadiversity of plants, having 17,630 endemic species among a total of 31,162 Angiosperm species [1], distributed in five Biomes. One of them is the Cerrado, which is recognized as a World Priority Hotspot for Conservation because it has around 4,400 endemic plants – almost 50% of the total number of species – and consists largely of savannah, woodland/savannah and dry forest ecosystems [2,3]. It is estimated that Brazil has over 60,000 plant species and, due to the climate and other environmental conditions, some tropical representatives of families which also occur in the temperate zone are very different in appearance [4].
\n\t\t\tThe Cerrado Biome is a tropical ecosystem that occupies about 2 million km² (from 3-24 Lat. S and from 41-43 Long. W), located mainly on the central Brazilian Plateau, which has a hot, semi-humid and markedly seasonal climate, varying from a dry winter season (from April to September) to a rainy summer (from October to March) [5-7]. The variety of landscape – from tall savannah woodland to low open grassland with no woody plants - supports the richest flora among the world’s savannahs (more than 7,000 native species of vascular plants) and a high degree of endemism [6,8]. This Biome is the most extensive savannah region in South America (the Neotropical Savannah) and it includes a mosaic of vegetation types, varying from a closed canopy forest (“cerradão”) to areas with few grasses and more scrub and trees (“cerrado sensu stricto”), grassland with scattered scrub and few trees (“campo sujo”) and grassland with little scrub and no trees (“campo limpo”) [3,9]. Among the grassland areas there are some flat areas with rocky soil, called “campos rochosos”, which are considered Cerrado areas because of their flora, especially when located in Chapada Diamantina (Bahia State), a transition area between Cerrado and Caatinga Biomes.
\n\t\t\tAlthough the Cerrado is considered a Hotspot for the conservation of global biodiversity, with plant species completely adapted to survive adverse conditions of soil and climate, only 30% of this Neotropical Savannah biodiversity is reasonably well known [8,10]. Coutinho [11] believes that the frequent occurrence of fire is one of the most important factors to determine this Biome´s vegetation, acting as a renewal element that selects structural and physiological characteristics. Nowadays it is believed that more than 40% of the original vegetation has already been converted into human-disturbed areas, due to the expansion of crops [12,13]. This process has accelerated the fragmentation of natural habitat, increasing the pressure on local biodiversity extinction and introducing exotic species, also amplifying soil erosion, water pollution and alterations in vegetation and hydrologic conditions [2,8,14].
\n\t\t\tThe Amaranthaceae family is composed of 2,360 species and here will be listed those that occur in Brazil, emphasizing the Cerrado species and including information on endemism, endangerment and economic or potential use. We also provide a list of the most important bibliographical references for those who are interested in studying the species of this family. Some aspects of morphology, leaf anatomy and ultrastructure will be shown for six species found in the Neotropical Savannah core area (Chapada dos Veadeiros) and some of these aspects, as well as taxonomy and ecology, will be discussed in order to propose the use of this plant family as an indicator of the diversity in open areas of this Biome.
\n\t\tThe Brazilian Amaranthaceae list (Table 1) was based on the research by the Brazilian taxonomists Marchioretto [15-21] and Siqueira [22-25] and on the most important taxonomic references to this Family both from the literature (Table 2) and Brazilian Herbaria (Table 3). All cited Herbaria are listed according to the Index Herbariorum [26,27].
\n\t\t\t\tThe species to be detailed were collected in a Conservation Unit named Reserva Particular do Patrimônio Natural Cara Preta (RPPN Cara Preta), located in Alto Paraíso, Goiás State, Brazil. After obtaining authorization from the NGO Oca Brasil, random walks were done in order to locate, photograph and mark species with a Global Positioning System device, and to collect and make exsiccates for Herbaria deposits, from September 2006 until March 2009. Although some plant leaves were collected during the vegetative stage, these specimens were visited until flowering to identify them correctly. All exsiccates were deposited in Brazilian Herbaria as standard control material (prioritizing PACA, UnB and IBGE Herbaria) and these species are included in Table 1.
\n\t\t\tCompletely expanded leaves, from 3rd to 5th node from the apex, of two to six specimens of each species were collected and sectioned. Part of the leaf medial region was fixed in ethanol, acetic acid and formaldehyde [28] for 24 hours and preserved in ethanol 70% until analysis to describe the anatomy and identify starch and crystal composition [28].
\n\t\t\t\tSome pieces of the leaf medial region were immediately submerged in a Karnovsky solution [29] of glutaraldehyde 2%, paraformaldehyde 2% and sucrose 3% in sodium cacodylate 0.05 M buffer for 12 to 24 hours and preserved in sodium cacodylate 0.05 M until processing for analysis under an electron microscope. For the latter analysis, these pieces were post-fixed in 2% osmium tetroxide and 1.6% potassium ferricyanide (1:1 v/v), followed by in-block staining with 0.5% uranyl acetate solution (overnight). These samples were then dehydrated in an acetone ascending series and slowly embedded in Spurr´s epoxy resin. Semi-thin and ultra-thin sections were obtained in ultramicrotome with glass and diamond knives. Semi-thin sections were stained with toluidine blue and analysed under the optical Zeiss Axiophot, and ultra-thin sections were analysed under the transmission electron microscope TEM JEOL JEM 1011.
\n\t\t\tThe Amaranthaceae family is composed of 2,360 species and 146 of them are found in Brazil (Table 1). Ninety-eight species within the family are found in the Cerrado and 73 spp. are endemic to Brazil, of which 13 are endemic to the Cerrado Biome (Table 1). Twenty Amaranthaceae species are exclusive to the Cerrado (Table 1).
\n\t\t\tAt least 22 Amaranthaceae species are referred to as being used in folk medicine (Table 1). In Brazil, only two of these species are already used as commercial drugs, as capsules containing their powdered roots, with studies to support their medicinal activity: Hebanthe eriantha (Poir.) Pedersen and Pfaffia glomerata (Spreng.) Pedersen (Table 1), both known as “Brazilian-ginseng”. However, there is neither registered success in isolating or synthesizing their components nor any economic studies about the viability of this kind of pharmaceutical procedure.
\n\t\t\tAlthough the species Gomphrena macrocephala St.-Hil. is not cited as medicinal (Table 1), the fructan content in its roots has been determined [30] because this species was considered synonymous with G. officinalis Mart. [31]. Later, it was determined that G. officinalis was synonymous with G. arborescens L.f. and not with G. macrocephala [22]. Studying G. arborescens, fructan was also determined as the principal carbohydrate in its subterranean system [32]. This species is used in popular medicine to heal respiratory diseases (asthma and bronchitis), to reduce fever and as a tonic [33-35]. An in vivo study (in cats) with the use of fructans isolated from Arctium lappa L. (Asteraceae) reported a cough-suppressing activity [36], and the presence of fructan in G. arborescens roots can partially justify the use of this species as a medicinal plant.
\n\t\t\tMost members of Brazilian Amaranthaceae are only known by taxonomists and 42 species are in danger of extinction according to Brazilian regional lists; 14 of them are recognized as endangered by the Brazilian Ministry of the Environment (MMA – “Ministério do Meio Ambiente”) (Table 1). Most of the endangered species are classified according to the IUCN Red List of vulnerability categories, some even with the same criteria, and there is a wide range of research still to be done.
\n\t\t\t\n\t\t\t\t\t\t\tSpecies\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tBioma and level of endemism\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tSpecies Threat Level\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tHabit, popular name and species knowledge\n\t\t\t\t\t\t | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAchyranthes\n\t\t\t\t\t\t\taspera L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; plant used as indigenous medicine in Ethiopia with chemistry study [37] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAchyranthes\n\t\t\t\t\t\t\tindica (L.) Mill. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tadscendens Suess. | \n\t\t\t\t\t\tCerrado exclusive | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Shrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\talbida (Moq.) Griseb. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\taquatica (D.Parodi) Chodat | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tbahiensis Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb or subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tbettzichiana (Regel) G.Nicholson | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb; popularly named "anador"; folk medicinal plant, used as analgesic and antipyretic [39] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera brasiliana (L.) Kuntze | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "perpétua-do-mato, periquito-gigante, penicilina" or Brazilian joyweed; folk medicinal plant, used as diuretic, digestive, depurative, bequic, astringent and antidiarrhoeal; ornamental plant; C3 photosynthesis structure [40-42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera decurrens J. C. Siqueira | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Januária - MG) | \n\t\t\t\t\t\tCR [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tdendrotricha C.C.Towns. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Shrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tflavida Suess. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\thirtula (Mart.) R.E.Fr. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EN [44] | \n\t\t\t\t\t\tHerb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera januariensi J. C. Siqueira | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Januária - MG) | \n\t\t\t\t\t\tCR [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tkurtzii Schinz | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tlittoralis P.Beauv. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb; called "periquito-da-praia" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tmalmeana R.E.Fr. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EN [44] | \n\t\t\t\t\t\tHerb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tmarkgrafii Suess. | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Serra de Grão Mogol - MG) \n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera martii (Moq.) R.E. Fries | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tmicrantha R.E.Fr. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tHerb; called "periquito-da-serra" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tminutiflora Suess. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tmulticaulis Kuntze | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tparonychioides A.St.-Hil. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44,46] | \n\t\t\t\t\t\tHerb; called "periquito-roseta, periquito"; C3-C4 intermediary photosynthesis structure; C4 photosynthesis physiology; ornamental plant[38,41,42,45,47] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tphiloxeroides (Mart.) Griseb. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "perna-de-saracura, carrapicho-de-brejo" and alligatorweed [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tpilosa Moq. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tpraelonga A.St.-Hil. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | CR [44] | \n\t\t\t\t\t\tHerb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tpuberula D.Dietr. | \n\t\t\t\t\t\tCerrado exclusive | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tpulchella Kunth | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tpungens Kunth | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "erva-de-pinto"; folk medicinal plant, used to treat syphilis and skin diseases; C4 photosynthesis physiology [38,39] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tramosissima (Mart.) Chodat | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tregelii (Seub.) Schinz | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\treineckii Briq. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tHerb; called "periquito-de-reineck" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\trufa (Mart.) D.Dietr. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\tsessilis (L.) R.Br. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tLC [48] | \n\t\t\t\t\t\tHerb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera tenella Colla\n\t\t\t\t\t\t | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tHerb; called "apaga-fogo, carrapichinho, corrente, folha-de-papagaio, periquito, periquito-figueira, perpétua-do-mato, sempre-viva"and joyweed; folk medicinal plant, used as diuretic; this species is naturally infected by a potyvirus; C3-C4 photosynthesis physiology and structure [38,39,40,45,47,49,50] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAlternanthera\n\t\t\t\t\t\t\ttetramera R.E.Fr. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tblitum L. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb; called "caruru"; folk medicinal plant, used to fight anemia; C4 photosynthesis physiology [38,39,51] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tcaudatus L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "rabo-de-gato, cauda-de-raposa, disciplina-de-freira, rabo-de-raposa"; folk medicinal plant, used to treat pulmonary diseases and as emoliente; C4 photosynthesis physiology; ornamental plant [33,38,39,41] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tcruentus L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "caruru-vermelho, veludo, bredo-de-jardim, crista-de-galo"; folk medicinal plant, used as emollient and laxative; C4 photosynthesis physiology [33,38,39,51] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tdeflexus L. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb; called "caruru-rasteiro"; C4 photosynthesis physiology [38,51] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\thybridus L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "caruru, bredo" and smooth pigweed; C4 photosynthesis physiology [38,51] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tmuricatus (Moq.) Hieron. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb;, C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tretroflexus L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\trosengurtii Hunz. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EN [44] | \n\t\t\t\t\t\tHerb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tspinosus L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "caruru-bravo, caruru-de-espinho, bredo-de-espinho, caruru-de-porco”; folk medicinal plant, used to combat eczema and as emollient, laxative and antiblenorragic; C4 photosynthesis physiology [33,38,39] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tAmaranthus\n\t\t\t\t\t\t\tviridis L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "caruru-bravo, caruru-verdadeiro, cururu, caruru-de-soldado, caruru-de-folha-miúda, amaranto-verde"; folk medicinal plant, used as emollient and diuretic desobstruente; C4 photosynthesis physiology [33,38-40,51] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tBlutaparon\n\t\t\t\t\t\t\tportulacoides (A.St.-Hil.) Mears | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tHerb; called “capotiraguá"; folk medicinal plant, used to combat leukorrhea; C4 photosynthesis physiology [38,39] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tBlutaparon\n\t\t\t\t\t\t\tvermiculare (L.) Mears | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tCelosia\n\t\t\t\t\t\t\targentea L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "celosia-branca, celósia-plumosa, crista-de-galo, crista-de-galo-plumosa, suspiro, veludo-branco"; folk medicinal plant, used to combat diarrhea and as anthelmintic and astringent; ornamental plant [39,41,52] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tCelosia\n\t\t\t\t\t\t\tcorymbifera Didr. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tCelosia\n\t\t\t\t\t\t\tgrandifolia Moq. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EN [44] | \n\t\t\t\t\t\tHerb, subshrub; called "bredo-do-mato" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tChamissoa\n\t\t\t\t\t\t\tacuminata Mart. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | VU [44] | \n\t\t\t\t\t\tSubshrub; called "mofungo-rabudo" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tChamissoa\n\t\t\t\t\t\t\taltissima (Jacq.) Kunth | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tSubshrub; called "mofungo-gigante" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tChenopodium\n\t\t\t\t\t\t\talbum L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tChenopodium\n\t\t\t\t\t\t\tambrosioides L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "erva-de-santa-maria, erva-santa, quenopódio" [40] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tChenopodium\n\t\t\t\t\t\t\tmurale L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tCyathula\n\t\t\t\t\t\t\tachyranthoides (Kunth) Moq. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tCyathula\n\t\t\t\t\t\t\tprostrata Blume | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tFroelichia\n\t\t\t\t\t\t\thumboldtiana (Roem. & Schult.) Seub. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tFroelichia\n\t\t\t\t\t\t\tinterrupta (L.) Moq. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tFroelichia procera (Seub.) Pedersen | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; called "ervaço"; C4 photosynthesis physiology [38,41] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tFroelichia\n\t\t\t\t\t\t\tsericea (Roem. & Schult.) Moq. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tFroelichia\n\t\t\t\t\t\t\ttomentosa (Mart.) Moq. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tFroelichiella grisea R.E. Fries | \n\t\t\t\t\t\tBraziliann Cerrado endemic (Chapada dos Veadeiros - GO) | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tHerb; C3 photosynthesis structure [42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena agrestis Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\tEN [46] | \n\t\t\t\t\t\tHerb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena arborescens L.f. | \n\t\t\t\t\t\tCerrado exclusive | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub; called "perpétua, perpétua-do-campo, perpétua-do-mato, paratudo-do-campo, paratudo-erva, raiz-do-padre"; folk medicinal plant, used as tonic, to reduce fever and against respiratory deseases; potential use as ornamentalplant; roots are fructan-rich; C4 photosynthesis physiology/structure [32,35,38,40,42,49,53,54] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tbasilanata Suess. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena celosoides Mart. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tcentrota E.Holzh. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tchrestoides C.C.Towns. | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Chapada Diamantina - BA) | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena claussenii Moq. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tdebilis Mart. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tdemissa Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; folk medicinal plant, used to combat the flu; C4 photosynthesis physiology [38,49] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena desertorum Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tduriuscula Moq. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tEN [43] | \n\t\t\t\t\t\tSubshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena elegans Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\tVU [46] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena gardnerii Moq. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tglobosa L. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; called "gonfrena, perpétua, perpétua-roxa, sempre-viva, suspiro, suspiro-roxo"; folk medicinal plant used to fight respiratory diseases; C4 photosynthesis physiology; ornamental plant [38,40,45,55,56] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tgraminea Moq. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tSubshrub; called "perpétua-gramínea"; C4 photosynthesis physiology [38,45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\thatschbachiana Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena hermogenesii J.C. Siqueira | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Chapada dos Veadeiros - GO) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C3 photosynthesis physiology; C4 photosynthesis structure [38,42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena hillii Suess. | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Paraíso do Norte - TO) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tincana Mart. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tlanigera Pohl ex Moq. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology and structure [38,42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena leucocephala Mart. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tmacrocephala A.St.-Hil. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; roots are fructan-rich; C4 photosynthesis physiology [30,38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tmarginata Seub. | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Diamantina - MG) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena matogrossensis Suess. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tmicrocephala Moq. | \n\t\t\t\t\t\tendemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena mollis Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; called "erva-mole, erva-rosa"; folk medicinal plant, used as tonic and carminative [39] \n\t\t\t\t\t\t | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena moquini Seub. | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Serra do Cipó - MG) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tnigricans Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tparanensis R.E.Fr. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub, C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tperennis L. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | VU [44] | \n\t\t\t\t\t\tSubshrub; called "perpétua-sempreviva"; C4 photosynthesis physiology [38,45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena pohlii Moq. | \n\t\t\t\t\t\tCerrado exclusive | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; called "infalível, paratudo, paratudinho, paratudo-amarelinho"; roots are used in folk medicine against respiratory deseases; C4 photosynthesis physiology and structure [38,39,42,49] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena prostrata Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology and structure [38,42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tpulchella Mart. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EN [44] | \n\t\t\t\t\t\tSubshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tpulvinata Suess. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena regeliana Seub. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena riparia Pedersen | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tCR [43] | \n\t\t\t\t\t\tSubshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena rudis Moq. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\trupestris Nees | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tscandens (R.E.Fr.) J.C.Siqueira | \n\t\t\t\t\t\tendemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tscapigera Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tschlechtendaliana Mart. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EN [44] | \n\t\t\t\t\t\tSubshrub; called "perpétua-schlechtendal"; C4 photosynthesis physiology [38,45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tsellowiana Mart. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena\n\t\t\t\t\t\t\tserturneroides Suess. | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; C4 photosynthesis physiology [38] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena vaga Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tSubshrub; called "thoronoé"; folk medicinal plant, used as analgesic [57] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tGomphrena virgata Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; called "cangussú-branco, vergateza"; folk medicinal plant, antiletargic; C4 photosynthesis physiology and structure[33,38,42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHebanthe\n\t\t\t\t\t\t\teriantha (Poir.) Pedersen | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tEN [44], VU [58] | \n\t\t\t\t\t\tSubshrub, shrub; called "corango-açu, ginseng-brasileiro, picão-de-tropeiro,solidonia, suma"; folk medicinal plant, used to combat colic and enteritis; most of its chemical constituents are known and roots of this plant are already used by pharmaceutical companies [40,59] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHebanthe\n\t\t\t\t\t\t\tgrandiflora (Hook.) Borsch & Pedersen | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Bush scandentia | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHebanthe\n\t\t\t\t\t\t\toccidentallis (R.E.Fr.) Borsch & Pedersen | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub scandentia | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHebanthe\n\t\t\t\t\t\t\tpulverulenta Mart. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [58] | \n\t\t\t\t\t\tSubshrub scandentia; called "corango-veludo" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHebanthe\n\t\t\t\t\t\t\treticulata (Seub.) Borsch & Pedersen | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Subshrub, shrub scandentia | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHebanthe\n\t\t\t\t\t\t\tspicata Mart. | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Shrub erect or scadentia | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tHerbstia\n\t\t\t\t\t\t\tbrasiliana (Moq.) Sohmer | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | EX [46] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tIresine\n\t\t\t\t\t\t\tdiffusa Humb. & Bonpl. ex Willd. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; called "bredinho-difuso" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tIresine\n\t\t\t\t\t\t\tpoeppigiana Klotzsch | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tLecosia\n\t\t\t\t\t\t\tformicarum Pedersen | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tLecosia\n\t\t\t\t\t\t\toppositifolia Pedersen | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tCR [43] | \n\t\t\t\t\t\tHerb or subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPedersenia\n\t\t\t\t\t\t\targentata (Mart.) Holub | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | Herb | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\tacutifolia (Moq.) O.Stützer | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb or subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\taphylla Suess. | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Gouveia - MG) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\targyrea Pedersen | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tHerb or subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\tcipoana Marchior. et al.\n\t\t\t\t\t\t | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Itambé do Mato Dentro - MG) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\tdenudata (Moq.) Kuntze | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub, shrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia elata R.E.Fr. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia glabrata Mart. | \n\t\t\t\t\t\tCerrado exclusive | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub; called "corango-sempreviva" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia glomerata (Spreng.) Pedersen | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tHerb, subshrub; called "anador, canela-velha, ginseng-brasileiro, finseng, páfia, paratudo, corango-sempreviva"; folk medicinal plant, most of its chemical constituents are known and roots of this plant are already used by pharmaceutical companies; butanolic extract showed antihyperglycemic potential in vivo; C3 photosynthesis physiology and structure [38,40,42,45,60] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia gnaphaloides (L.f.) Mart. | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\tVU [44] | \n\t\t\t\t\t\tHerb, subshrub, called "corango-de-seda", C3 photosynthesis physiology and structure [38,42,45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\thirtula Mart. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia jubata Mart. | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub; called "marcela-branca, marcela-do-campo, marcela-do-cerrado"and kytertenim; roots are used in folk medicine against intestinal problems [39,49] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia minarum Pedersen | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\trupestris Marchior. et al.\n\t\t\t\t\t\t | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Rio Pardo de Minas - MG) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia sarcophylla Pedersen | \n\t\t\t\t\t\tBrazilian Cerrado endemic (Niquelândia - GO) | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub; nickel hyperaccumulator, it is one of the first species to recolonize the ground with high concentrations of total Ni in the soil ("/1%) [61] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\tsericantha (Mart.) Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\tsiqueiriana Marchior. & Miotto | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia townsendii Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\tVU [43] | \n\t\t\t\t\t\tSubshrub; C3 photosynthesis physiology and structure [38,42] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\ttuberculosa Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia tuberosa (Spreng.) Hicken | \n\t\t\t\t\t\tCerrado | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Herb, subshrub; called "corango-de-batata" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPfaffia\n\t\t\t\t\t\t\tvelutina Mart. | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tPseudoplantago friesii Suess\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | PE [44] | \n\t\t\t\t\t\tPopular name is "caruru-açu" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tQuaternella confusa Pedersen | \n\t\t\t\t\t\tCerrado exclusive, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Shrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tQuaternella\n\t\t\t\t\t\t\tephedroides Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Shrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tQuaternella\n\t\t\t\t\t\t\tglabratoides (Suess.) Pedersen | \n\t\t\t\t\t\tEndemic to Brazil | \n\t\t\t\t\t\tEN [44] | \n\t\t\t\t\t\tSubshrub; called "corangão" [45] | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tXerosiphon\n\t\t\t\t\t\t\tangustiflorus (Mart.) Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tXerosiphon aphyllus (Pohl ex Moq.) Pedersen | \n\t\t\t\t\t\tCerrado, endemic to Brazil | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | Subshrub | \n\t\t\t\t\t
Amaranthaceae species found in Brazil, identifying those endemics to Brazil and the ones found in the Neotropical Savannah (Cerrado), level of threat, habit, popular name (mostly in Portuguese) and some of the knowledge about the species.
Taxonomy is the science that aims to identify and characterize species. It includes the study of the plant´s behaviour in nature and is based on plant morphology. The use of other data, such as anatomy studies, genetic characters, ecology and geographic pattern, aims to include and define affinities and parental relations among plant groups. Only by knowing the species is it possible for Botany to contribute to other scientific areas, including to the conservation of species in situ, not only of plants but also of animals.
\n\t\t\t\tIt is not easy to correctly identify Brazilian Amaranthaceae species. Different species can be very alike in habit and vegetative morphology. The correct identification depends almost exclusively on some flower details, whose small dimensions make it especially difficult to work in the field, demanding a highly specialized work, only partially carried out for this family (15-22).
\n\t\t\t\tBrazilian species of this family are predominantly herbs, shrubs or climbing plants. They can be annual or perennial, with erect, prostrate, decumbent or scandent stem. In species from the Neotropical Savannah or from rocky fields, the underground organ is thickened and composed of roots and a xylopodium – a portion of the subterranean system which is responsible for the re-sprouting after a fire or other environmental stress [62]. The leaf arrangement can be opposite, alternate or with a basal aggregation of leaves. Leaves are exstipulate, glabrous or pubescent, with entire lamina and margins. Inflorescences can be cymoses, in spikes, in heads, corymboses or paniculates, axillary or axial. Flowers are bisexual or monoecious and small. The perianth is undifferentiated, actinomorphic, with five distinct or partially connated sepals. Flowers are associated with dry and papery bracts. Fruits are dry, usually a single-seeded achene or capsules with few seeds [15-22]. A short list of the most important Brazilian Herbaria to visit in order to study Amaranthaceae taxonomy is presented on Table 2 and the literature used to identify the species of this family is presented in Table 3.
\n\t\t\t\tIndex | \n\t\t\t\t\t\t\tHerbarium Name | \n\t\t\t\t\t\t\tInstitution and municipality | \n\t\t\t\t\t\t
ALCB | \n\t\t\t\t\t\t\tHerbário da Universidade Federal da Bahia | \n\t\t\t\t\t\t\tUFBA/Campus de Ondina, Salvador, Bahia, Brazil | \n\t\t\t\t\t\t
BHCB | \n\t\t\t\t\t\t\tHerbário da Universidade Federal de Minas Gerais | \n\t\t\t\t\t\t\tUFMG, Belo Horizonte, Minas Gerais, Brazil | \n\t\t\t\t\t\t
BOTU | \n\t\t\t\t\t\t\tHerbário da Universidade Estadual Paulista | \n\t\t\t\t\t\t\tUNESP, Botucatu, São Paulo, Brazil | \n\t\t\t\t\t\t
CEN | \n\t\t\t\t\t\t\tHerbário da EMBRAPA Recursos Genéticos e Biotecnologia | \n\t\t\t\t\t\t\tEMBRAPA/CENARGEN, Brasília, Distrito Federal, Brazil | \n\t\t\t\t\t\t
CEPEC | \n\t\t\t\t\t\t\tHerbário do Centro de Pesquisas do Cacau | \n\t\t\t\t\t\t\tCEPEC, Itabuna, Bahia, Brazil | \n\t\t\t\t\t\t
CESJ | \n\t\t\t\t\t\t\tHerbário da Universidade Federal de Juiz de Fora | \n\t\t\t\t\t\t\tUFJF, Juiz de Fora, Minas Gerais, Brazil | \n\t\t\t\t\t\t
CPAP | \n\t\t\t\t\t\t\tHerbário do Centro de Pesquisas Agropecuárias do Pantanal | \n\t\t\t\t\t\t\tCPAP, Corumbá, Mato Grosso do Sul, Brazil | \n\t\t\t\t\t\t
ESA | \n\t\t\t\t\t\t\tHerbário da Universidade de São Paulo | \n\t\t\t\t\t\t\tESALQ/USP, Piracicaba, São Paulo, Brazil | \n\t\t\t\t\t\t
GUA | \n\t\t\t\t\t\t\tHerbário Alberto Castellanos | \n\t\t\t\t\t\t\tFEEMA/INEA, Rio de Janeiro, Rio de Janeiro, Brazil | \n\t\t\t\t\t\t
HTO | \n\t\t\t\t\t\t\tHerbário da Universidade Federal do Tocantins | \n\t\t\t\t\t\t\tUFTO, Porto Nacional, Tocantins, Brazil | \n\t\t\t\t\t\t
HUEFS | \n\t\t\t\t\t\t\tHerbário da Universidade Estadual de Feira de Santana | \n\t\t\t\t\t\t\tUFES, Feira de Santana, Bahia, Brazil | \n\t\t\t\t\t\t
IAC | \n\t\t\t\t\t\t\tHerbário do Instituto Agronômico de Campinas | \n\t\t\t\t\t\t\tIAC, Campinas, São Paulo, Brazil | \n\t\t\t\t\t\t
IBGE | \n\t\t\t\t\t\t\tHerbário da Reserva Ecológica do IBGE | \n\t\t\t\t\t\t\tIBGE/RECOR, Brasília, Distrito Federal, Brazil | \n\t\t\t\t\t\t
JPB | \n\t\t\t\t\t\t\tHerbário da Universidade Federal da Paraíba | \n\t\t\t\t\t\t\tUFPB, Cidade Universitária, João Pessoa, Paraíba, Brazil | \n\t\t\t\t\t\t
MBM | \n\t\t\t\t\t\t\tHerbário do Museu Botânico Municipal | \n\t\t\t\t\t\t\tPrefeitura Municipal/SMA, Curitiba, Paraná, Brazil | \n\t\t\t\t\t\t
PACA | \n\t\t\t\t\t\t\tHerbarium Anchieta | \n\t\t\t\t\t\t\tInstituto Anchietano de Pesquisas/UNISINOS, São Leopoldo, Rio Grande do Sul, Brazil | \n\t\t\t\t\t\t
RB | \n\t\t\t\t\t\t\tHerbário do Jardim Botânico do Rio de Janeiro | \n\t\t\t\t\t\t\tJBRJ, Rio de Janeiro, Rio de Janeiro, Brazil | \n\t\t\t\t\t\t
SP | \n\t\t\t\t\t\t\tHerbário do Instituto de Botânica | \n\t\t\t\t\t\t\tSecretaria de Meio Ambiente, São Paulo, São Paulo, Brazil | \n\t\t\t\t\t\t
SPF | \n\t\t\t\t\t\t\tHerbário da Universidade de São Paulo | \n\t\t\t\t\t\t\tUSP, São Paulo, São Paulo, Brazil | \n\t\t\t\t\t\t
UB | \n\t\t\t\t\t\t\tHerbário da Universidade de Brasília | \n\t\t\t\t\t\t\tUnB, Brasília, Distrito Federal, Brazil | \n\t\t\t\t\t\t
UEC | \n\t\t\t\t\t\t\tHerbário da Universidade Estadual de Campinas | \n\t\t\t\t\t\t\tUNICAMP, Campinas, São Paulo, Brazil | \n\t\t\t\t\t\t
UFG | \n\t\t\t\t\t\t\tHerbário da Universidade Federal de Goiás | \n\t\t\t\t\t\t\tUFG, Goiânia, Goiás, Brazil | \n\t\t\t\t\t\t
VIC | \n\t\t\t\t\t\t\tHerbário da Universidade Federal de Viçosa | \n\t\t\t\t\t\t\tUFV, Viçosa, Minas Gerais, Brazil | \n\t\t\t\t\t\t
List of the most important Herbaria references for researchers interested in studying the Brazilian Amaranthaceae
[15-21] Revisions of Brazilian Froelichia,\n\t\t\t\t\t\t\t\tFroelichiella, Hebanthe and Pfaffia; species list and phytogeography | \n\t\t\t\t\t\t
[22-25] Revision of Brazilian Gomphrena; species list na phytogeography | \n\t\t\t\t\t\t
[45] Amaranthaceae from Santa Catarina State, Brazil | \n\t\t\t\t\t\t
[63] Restoring the Hebanthe genera | \n\t\t\t\t\t\t
[64,65] Brazilian Amaranthaceae species and the Family in the World | \n\t\t\t\t\t\t
[66] Revision of Amaranthaceae in the World | \n\t\t\t\t\t\t
[67-71] Studies in South American Amaranthaceae | \n\t\t\t\t\t\t
[72] Amaranthaceae in Flora Brasiliensis | \n\t\t\t\t\t\t
[73] Studies of Pfaffia and Alternanthera genera | \n\t\t\t\t\t\t
[74,75] Amaranthaceae in Central and South America | \n\t\t\t\t\t\t
[51,52,56,76] Amaranthaceae from Rio Grande do Sul State, Brazil | \n\t\t\t\t\t\t
List of the most important bibliographical references for researchers interested in studying the Brazilian Amaranthaceae
The Reserva Particular do Patrimônio Natural (RPPN) Cara Preta, in Alto Paraíso, Goiás State, is a good representative of Neotropical Savannah vegetation, at about 1,500 meters of altitude and showing rocky slopes with Cerrado sensu stricto (Figure 1), grassland with scattered scrubs and few trees and grassland with few scrubby plants and no trees (Figure 2). The Pfaffia genus was restricted to a rocky slope and the other species were found in a level field of sandy soils, usually covered by Poaceae and Cyperaceae. It was very difficult to find all the species. It was only possible because of frequent visits to RPPN Cara Preta, using GPS to mark the local after finding any probable member of the family in order to be able to accompany them until the flowering stage. The area was monitored for one and a half year and only Gomphrena hermogenesii J.C. Siqueira and Pfaffia townsendii Pedersen (Figure 3) were localized, the first one always in vegetative stage. A key event to help finding all six species was a fire that burned out the vegetation in August of the year 2008: without the competition of the grasses, the Amaranthaceae species regrew and flowered rapidly, in order to spread their seeds before the grasses could fully recover (Figures 4-8).
\n\t\t\t\t\n\t\t\t\t\tPfaffia townsendii is a shrub species with persistent aerial portions that flowers throughout the year (Figure 3). The herb G. hermogenesii is endemic to Chapada dos Veadeiros and also has permanent aerial portions (about 10-20 cm high), but it was commonly found in vegetative stage under the grass leaves; its flowering stage was stimulated by fire (Figure 4). Froelichiella grisea R.E.Fr. (Figure 5), G. lanigera Pohl. ex Moq. (Figure 6), G. prostrata Mart. (Figure 7) and P. gnaphaloides (L.f.) Mart. (Figure 8) species were recorded in the flowering stage at RPPN Cara Preta around 20 days after a fire that burned out all the vegetation in the area, which is evidence of the pirophytic behaviour of most Neotropical Savannah Amaranthaceae. Five of these species had never been recorded in this RPPN before and one of them was last recorded in 1966 (F. grisea), according to Herbaria data. Figures 1-8 are reproduced [77] with the authorization of the Biota Neotropica Editor, Dr. Carlos Joly.
\n\t\t\t\t\n\t\t\t\t\t\t\tFigures 1-8) Photographs of the environment and of the studied species at Reserva Particular do Patrimônio Natural (RPPN) Cara Preta, Alto Paraíso, Goiás State, Brazil. Fig. 1. Rocky slope where were found the species Pfaffia townsendii Pedersen and P. gnaphaloides (L. f.) Mart. Fig. 2. Humid rocky grassland where were found the species Froelichiella grisea R.E.Fr., Gomphrena hermogenesii J.C. Siqueira, G. lanigera Pohl. ex Moq. and G. prostrata Mart. Fig. 3. P. townsendii. Fig. 4. G. hermogenesii. Fig. 5. F. grisea. Fig. 6. G. lanigera. Fig. 7. G. prostrata. Fig. 8. P. gnaphaloides.
Five species are herb to subshrub, and only P. townsendii is a shrub (Figure 3). Well-developed tuberous subterranean systems were found in F. grisea (Figure 5) and G. hermogenesii, while in G. lanigera and P. gnaphaloides the underground organ was less developed, also tuberous. G. prostrata and P. townsendii presented a well-developed and lignified underground organ. Leaves of F. grisea and G. hermogenesii are opposite and alternate in the other studied species. F. grisea and G. lanigera can present a basal aggregation of leaves. Leaves are always tomentose, with exception of the adaxial face of F. grisea, which can be glabrous. Inflorescence is axial in all these species, spikes in F. grisea and G. lanigera and heads in the other studied species. Flowers are yellowish in F. grisea, G. hermogenesii and G. lanigera, with a tendency to turn red in the first and last one. In G. prostrata, P. gnaphaloides and P.townsendii flowers are white, turning beige in the last species. All the species have flowers associated with dry and papery bracts that persist alongside their dry fruits, usually a single-seeded achene, favouring anemocoric dispersion.
\n\t\t\t\tThe fastest lifespan was observed in G. lanigera, which took around 20 days to regrowth and finish the flowering phase. In Figure 6, G. lanigera was about 20 days old and fruits were almost mature, indicating proximity to the seed dispersal phase. Pfaffia townsendii alone showed behaviour that was independent of fire, since even G. hermogenesii only flowered after being burned to the ground and regrowing from its xylopodium. The other four species were found after the occurrence of fire, all of them in the flowering stage.
\n\t\t\t\tIn the Taxonomy and Morphology areas, studies of the genera Achyranthes, Alternanthera, Amaranthus, Blutaparon, Celosia, Chamissoa, Chenopodium, Cyathula, Iresine, Lecosia, Pedersenia, Pseudoplantago, Quaternella and Xerosiphon still need to be done, not only covering the revision of the Brazilian species, biogeography and morphological evolution, but also molecular biology to establish synonyms and to delimit variations among individuals of each species.
\n\t\t\tLeaves of the six studied species have anatomical variation among the genera and are more similar between species of the same genus. Transverse sections show that G.\n\t\t\t\t\thermogenesii (Figure 9), G. lanigera (Figure 10) and G. prostrata (Figure 11) have large nonglandular trichomes covering the single layered epidermis, dorsiventral mesophyll with upper palisade parenchyma and spongy parenchyma near the lower epidermis. All these three species are amphistomatic, and a complete well-developed parenchymatous sheath with thicker cell walls surrounds the vascular bundles (Kranz cells), in which starch accumulates. Calcium oxalate druses were found in the mesophyll. The leaf anatomy of the three Gomphrena spp. is compatible with the C4 photosynthesis pathway.
\n\t\t\t\t\n\t\t\t\t\tPfaffia gnaphaloides (Figure 12) and P. townsendii (Figure 13) have more undulating surfaces and a thinner leaf blade in relation to the Gomphrena species. Trichomes are also more frequent and thinner and the mesophyll is dorsiventral. The parenchymatous sheath has thinner walls than the neighbouring cells in Pfaffia species. Both species had elevated stomata on the lower epidermis and only P. gnaphaloides had few stomata on the upper epidermis. Starch was distributed in all mesophyll cells and calcium oxalate druses were rare. The anatomy of Pfaffia spp. leaves is compatible with C3 photosynthesis metabolism.
\n\t\t\t\t\n\t\t\t\t\tFroelichiella grisea (Figure 14) has the only isobilateral mesophyll among the studied species, with palisade parenchyma near both upper and lower epidermis. Palisade cells are shorter near the lower epidermis. The parenchymatic vascular bundle is not conspicuous and organelles in these cells are positioned towards the outer cell walls, in the same way as they are found in the other mesophyll cells. Calcium oxalate druses were more common near the midrib, and the reaction to starch was similar to that of all the mesophyll cells. Its leaf anatomy is compatible with C3 photosynthesis metabolism. Figures 9-14 [77] were reproduced with the authorization of the Biota Neotropica Editor, Dr. Carlos Joly.
\n\t\t\t\t\n\t\t\t\t\tGomphrena trichomes are similar to the ones described for G. arborescens [32,54,78]. Although it is expected that stomata are reduced on the upper surface of land plants, the Cerrado Gomphrena species G. arborescens, G. pohlii and G. virgata have a similar number of stomata on both surfaces [78], subjecting them to a greater water loss, which is compensated by the well-developed subterranean systems that guarantee water supply during the lifespan of their leaves. The size and number of stomata on both leaf surfaces of G. hermogenesii, G. lanigera and G. prostrata is still to be verified, but simple observation indicates that it should be similar to the phenomena observed in the first cited species, since they also have a relatively well-developed subterranean system.
\n\t\t\t\t\n\t\t\t\t\t\t\tFigures 9-14) Micrographies of the middle leaf transversal sections of the studied Amaranthaceae species. Fig. 9. Gomphrena hermogenesii - leaf blade thickness from medium to thick, dorsiventral mesophyll and complete parenchymatous bundle sheath, with thick cell walls and collateral vascular bundles. Fig. 10. G. lanigera - medium leaf blade, dorsiventral mesophyll and complete parenchymatous bundle sheath, with thick cell walls and collateral vascular bundles. Fig. 11. G. prostrata – thin to medium leaf blade, dorsiventral mesophyll and complete parenchymatous bundle sheath, with thick cell walls and collateral vascular bundles. Fig. 12. Pfaffia gnaphaloides – thin leaf blade, dorsiventral mesophyll, less defined parenchymatous bundle sheath and collateral vascular bundles. Fig. 13. P. townsendii – only hypostomatous leaf species, thin leaf blade, dorsiventral mesophyll, less defined parenchymatous bundle sheath and collateral vascular bundles. Fig. 14. Froelichiella grisea - thick leaf blade, isobilateral mesophyll with elongated palisade parenchyma under the adaxial epidermis, less defined bundle sheath and collateral vascular bundles. Legend: eab = abaxial epidermis; ead = adaxial epidermis; pl = spongy parenchyma; pp = palisade parenchyma; arrowhead = stoma; circle = druse; arrow = parenchymatous bundle sheath. Bar = 100 µm.
The leaf anatomy of the three Gomphrena spp. is similar to that of G. arborescens L.f. [54], G. cespitosa, G. dispersa, G. nitida, G. sonorae [79] and G. conica, G. flaccida [80] among others, most of them arranged in a Gomphrena atriplicoid-type of Kranz anatomy [81,82]. As expected, there was no significant variation in these species’ leaf anatomy due to the life cycle stage, although older leaves collected during the vegetative stage have a thicker cuticle covering both epidermis surfaces, especially in G. hermogenesii species. The leaf anatomy observed in the two Pfaffia spp. is similar to that described in P. jubata [83], which also lacks the Kranz anatomy. There is no previous study about the anatomy of F. grisea leaves and its genus is monoespecif.
\n\t\t\t\tThere are still a number of studies to be done in the field of anatomy and histology of Brazilian Amaranthaceae plants. Most of the medicinal species need to be analyzed and validated for their use as drugs, including anatomic description and an investigation of the secondary compounds of the used organs, by histology and by chromatography. Due to the difficulties in correctly identifying the species in the field, anatomical and morphological markers should be defined to guarantee these species’ identity even during the vegetative stage. Besides that, anatomical studies can improve the taxonomy data and explain some morphological characters of this plant family, like the anatomical variations in the leaf that are connected to photosynthesis, or the secondary thickening and xylopodium development in underground organs, which is a character for the Cerrado species. The anatomy of few Brazilian Amaranthaceae species has been described, with the exception of some from the Gomphrena and Pfaffia genera [83-86].
\n\t\t\tLeaves of the six studied species have less ultrastructural variation among the species of the same genus. Froelichiella\n\t\t\t\t\tgrisea organelles are equally distributed among chlorenchyma tissues, usually near the cell walls. The chloroplasts of this species are always granal (Figure 15), even in the vascular cells, with large starch granules (usually one or two per organelle) in all tissues. Plastoglobuli are small and less numerous in mesophyll chloroplasts (Figure 15), but guard cell chloroplasts usually have just one large plastoglobulus and less conspicuous grana. Mitochondria and peroxisomes (Figure 15) were found in mesophyll and bundle sheath cells. Leaf ultrastructure is compatible with C3 photosynthesis metabolism.
\n\t\t\t\tMesophyll cell chloroplasts of Gomphrena species have conspicuous grana, rare starch granules and variable size of plastoglobuli: G. hermogenesii has larger ones in relation to G. lanigera and G. prostrata. Bundle sheath chloroplasts are completely devoid of grana or have few stacked thylakoids (Figure 16) in all studied Gomphrena species, but always have large starch granules and plastoglobuli. The larger the starch granules, the more deformed the chloroplasts’ typical lens shape, as shown in G. hermogenesii (Figure 16). Mitochondria are usually numerous in bundle sheath cells and are always near chloroplasts, grouped next to the inner cell wall (towards the vascular bundle). Peroxisomes are rare, and a few were observed near chloroplasts in palisade and spongy parenchyma cells, but not in the bundle sheath cells. Phloem companion cells are mitochondria-rich in all Gomphrena species, as shown in G. prostrata (Figure 17). The presence of dimorphic chloroplasts, disposition of the organelles and the occurrence of Kranz syndrome seen in the leaf anatomy indicate that the C4 photosynthesis pathway operates in the three studied Gomphrena spp.
\n\t\t\t\t\n\t\t\t\t\tPfaffia species organelles are equally distributed among chlorenchyma tissues, usually near the cell walls. Pfaffia chloroplasts are granal even in the vascular cells, showing large starch granules and a similar size in all mesophyll cells, as can be observed in the palisade parenchyma of P. townsendii (Figure 18). Mitochondria and peroxisomes are common near chloroplasts (Figure 18). Phloem companion cells are mitochondria-rich and chloroplasts are smaller and granal, as in the other species of this study. Along with the aspects of Pfaffia anatomy described previously, their ultrastructure is compatible with the C3 photosynthesis pathway.
\n\t\t\t\t\n\t\t\t\t\tPfaffia gnaphaloides (Figure 19) and G. hermogenesii (Figure 20) leaves, collected during the flowering stage, were colonized by two distinct forms of microorganisms: (i) a smaller organism was found in the intercellular spaces (ics) of the spongy parenchyma (Figure 19); (ii) a larger and distinctly eukaryotic organism was found within distinct cells, with some morphological alterations suggesting an infectious process (Figures 19-20).
\n\t\t\t\tThe external envelopae membranae system of the chloroplasts is disrupted in infected cells (Figure 20) and a size reduction was observed in the chloroplast plastoglobuli. All morphological characteristics observed in the intracellular microorganism suggest that it should be an obligate biotroph endophytic fungus belonging to the Ascomycete division (Figure 20). The invading fungus may be using the plastoglobuli lipids as its primary source of carbon and energy; the reduction of the plastoglobuli could also be due to its mobilization by the host plants in response to the stress caused by these biotic interactions. The complete identification of the fungus and its effect on the plants depends on its isolation from the environment/hosts and complementary studies.
\n\t\t\t\tThe rare peroxisomes in Gomphrena spp. leaf cells and their presence among all chlorenchyma tissues of the Pfaffia spp. leaf cells is compatible with their possible photosynthesis metabolisms. Along with the presence of Kranz syndrome and dimorphic chloroplasts, the absence of peroxisome indicates that Gomphrena spp. perform photosynthesis via the C4 pathway. In Gomphrena species, CO2 concentration in the bundle sheath cells must be efficient, leading to a significant reduction in the oxygenase function of its RuBisCO enzyme. This leaves the species virtually free of the photorespiration process, aided by the large walls of the bundle sheath cells. Although a carbon isotope ratio study [38] indicates that G. hermogenesii is not a C4 species, this species also has Kranz anatomy and ultrastructure compatible with C4 metabolism, as do all the other studied Gomphrena spp. [42]. The distribution of its key photosynthetic enzymes will be carried out using immuno-cytochemistry, in our laboratory, in order to complete these data.
\n\t\t\t\t\n\t\t\t\t\t\t\tFigures 15-20) Citological aspects of Amaranthaceae species as seen through a Transmission Electron Microscope. Fig.15. Froelichiella grisea palisade parenchyma cell. Fig. 16. Gomphrena hermogenesii bundle sheath cell. Fig. 17. G. prostrata phloem companion cell and bundle sheath cell on top. Fig. 18\n\t\t\t\t\t\t\t. Pfaffia townsendii palisade parenchyma cells.Fig. 19. P. gnaphaloides spongy parenchyma cells and invading microorganisms (black arrows). Fig. 20. G. hermogenesii bundle sheath cell and the invading Ascomycete fungus (black arrow) and the disrupted chloroplasts with smaller plastoglubuli. Legend: black arrow = invading organism; white arrow = mitochondria; ellipsis = septum with a simple pore; bsc = bundle sheath cell; cw = cell wall; ics = intercellular space; n = nucleus of the microorganism; N = nucleus of the plant species; p = peroxisome; pc = palisade parenchyma cell; pg = plastoglobulus in a chloroplast; s = starch granule in a chloroplast; sc = spongy parenchyma cell.
This chapter presents data on Amaranthaceae species, with no pretension to explain the full potential of this plant family for scientific studies, but rather to provide a basic tool for those interested in amplifying studies on the species of this family. Based on our results, we are convinced of the importance of studying this family further, not only as a tool in the better preservation of endemic species, but also to explore its undoubted economic importance more fully. Basic research is still needed, with the aim of applying knowledge on these species to technological advances, especially in growing crops - since C4 species have a faster metabolism and growing capacity, as observed in the species found in the RPPN Cara Preta - and to explore medicinal molecules of these plants. C4 species are also important to balance CO2 in the atmosphere because of their efficiency in the transformation of carbon into biomass; in Cerrado Amaranthaceae species, this storage is basically underground in their well-developed subterranean roots and xylopodium.
\n\t\t\tThe number of medicinal plants among the Brazilian Amaranthaceae species may well be higher than already reported (Table 1), because Cerrado inhabitants are particularly interested in the highly developed subterranean systems of some medicinal species [34,49,58] which can be collected at any time of the year, even from species whose aerial portions are not persistent. Due to the morphological similarity among Amaranthaceae species in the Neotropical Savannah, their collectors can easily mistake one species for another during the vegetative stage, which confirms the need for further and more complete studies of the known medicinal and endangered species, at least.
\n\t\t\tPreparation of plant samples for transmission electron microscopy also proved to be useful in studying the morphology of fungi inside plant cells, as well as aspects of host-parasite interaction. This kind of study could be recommended for plants considered toxic to herbivores and to any medicinal plant consumed by humans, in order to give more information about the real source of poisoning or medicinal effect and for fine quality control. In both studied species (G. hermogenesii and P. gnaphaloides) the external macro aspects of the plants did not indicate the presence of the endophytic fungus.
\n\t\t\tRPPN Cara Preta is a small Private Conservation Unit (only 1.5% of the area of the Chapada dos Veadeiros National Park, a government-preserved area of 65,038 hectares). Both Conservation Units are separated only by a road, in Alto Paraíso municipality of Goiás State, Brazil. The latter site is registered by UNESCO as a natural protected Cerrado zone. RPPN Cara Preta has 245 species representing 47 family plants [75,86], which is 9.2% of the 2,661 plant species of Chapada dos Veadeiros [87], a good diversity of plants in relation to the occupied area. There are six Amaranthaceae species in the RPPN – 25% of the 27 species found in the National Park [87]. Considering that the RPPN Cara Preta Utilization Planning Report [86] indicated the presence of three endemic species, plus two Amaranthaceae species not reported initially [75], this Conservation Unit has 2% of endemic species – which is more than expected. According to [2,12], the Cerrado Biome is one of the priority hotspots for conservation because it has, among others, 4,400 endemic plants (1.5% of the Earth’s 300,000 species). The Amaranthaceae family in RPPN Cara Preta can be considered a taxon indicator of the good diversity of the Neotropical Savannah. This taxon could be considered a plant diversity indicator in other works on flora in open areas of the Cerrado Biome. Because of the predominant habit (herbs and shrubs) and survival strategies, the presence of species from this family among the collected species clearly indicates a well performed collection effort.
\n\t\t\tThere are a number of important factors indicating that this plant family deserves more studies for a greater understanding by researchers working in Brazil, and we recap them as follows: the Cerrado Biome holds 98 of the 146 Brazilian Amaranthaceae species (almost 70% of the total species) (Table 1); their pirophytic behavior and survival strategies (fast regrowth and seed dispersal before the complete recovery of grasses after fire) are coherent with the Biome’s characteristics; their morphology shows exceptional adaptation to the seasonal climate and open areas (hairy aerial portions, partial or total loss of the aerial portions during the dry season, well-developed underground system with xylopodium, dry fruit dispersal by wind); their metabolism (evolution of C4 and intermediary C3-C4 photosynthesis) may have importance for biomass conversion and CO2 balance; and, finally, many of these plants are already used in medicines by Cerrado inhabitants and there may be much wider medicinal potential in other species of this family.
\n\t\tWe would like to thank CAPES, CNPq and FINEP for financial support; NGO Oca Brasil and Herbaria IBGE, UB and PACA for access authorization and research infrastructure; the aditional collectors for help in searching for and collecting the species at RPPN Cara Preta; and Susan Casement Moreira for the English review.
\n\t\tPhospholipids are major constituent of cellular membrane hence they have excellent biocompability. They are amphiphilic molecules which usually built by glycerol backbone with two different polarity groups attached to it. On the one hand is the hydrophilic group renowned as the head group which then becomes the basis of species classification of phospholipids, such as phosphatidylcholine (PC), phosphatidyletanolamine (PE), and phosphatidylserine (PS). On the other hand is the hydrophobic fatty acyl chains distinguished as the tails. The variation of the length and the saturation, the bonding position of fatty acyl chains to glycerol backbone as well as the head group type become a crucial part of their application, for instance in drug delivery systems.
The development of phospholipids based drug delivery systems have been proven prominent by the emergence of many phospholipid-related drug formulation. Among of them are doxorubicin in stealth liposomes for cancer treatment, which has been on the market since 1995 [1, 2]; Verteporfin in cationic liposomes for molecular degeneration [3] and vincristine in conventional liposome for Non-Hodgkin lymphoma [2]. They have been used in clinic, and achieve good results. Many more phospholipids based liposomal preparation have been developed to find better therapeutic results [4, 5, 6]. Furthermore various sources, synthetic and natural, have been explored [2, 7].
The isolation of phospholipids from natural sources cost lower than synthesizing them hence the preference is the isolation of natural phospholipids. For natural origin, the more pure they are, the greater the value is [8]. Phospholipids from natural origin can be refined into diverse levels, comprising food and pharmaceutical grade [2, 9]. In term of natural phospholipids, different source enhance the species variety of phospholipids [7]. Egg yolk and soybean phospholipids mainly consist of phosphatidylcholine species but they have differences in the tail portions which influence their physical, chemical properties and their applications. Other natural phospholipids that currently are being explored extensively are sunflower [10, 11, 12], candlenut [13], jack bean [14], sesame [13, 15, 16, 17] and coconut [13, 15, 16, 18, 19, 20, 21, 22].
Coconut is one of the native plantations in tropical countries and produces mainly copra and coconut oil. Exploration of coconut by-products such as coconut phospholipids needs to be done to increase the added value of these coconut plantations. Previous studies have found that dried coconut contain phospholipids from cephaline species with their fatty acyl chains are dodecanoic and octanoic acyl chains [15]. Purification with eluent chloroform: methanol (9:1) follows by identification using thin layer chromatography (TLC) also detects the presence of phosphatidylcholine (PC), phosphatidyletanolamine (PE), and phosphatidylserine (PS) species in coconut phospholipids (CocoPLs) [20, 21].
In the matter of its application, coconut liposomes (CocoPLs liposomes) have been used in the encapsulation of hydrophilic agent namely carboxyfluoresence and vitamin C and resulted in that CocoPLs liposomes has high efficiency of encapsulation [16, 19, 22]. The addition of cholesterol improves the encapsulation efficiency and low storage temperature reduces CocoPLs liposomes leakage. The results advocated the CocoPLs potency as drug delivery material. Moreover since we have established that CocoPLs consist of many phospholipid species therefore it would be valuable to study the component of the species and their capability as drug delivery system. In this study we explore the isolation and purification of coconut phospholipid species specifically coconut phosphatidylethanolamine (CocoPEs) and utilization of their liposomes (CocoPEs liposomes) for vitamin C encapsulation with various cholesterol concentrations. To our knowledge this is the first study of such.
Materials used in this study were ripe coconut meat purchased from local market, TLC silica gel 60 F254 plate, silica gel powder 60 G for thin layer chromatography, various solvents and regents for analytical grade.
Isolation technique was carried out based on the previous method used [20, 21]. Briefly coconut meat powder was macerated in a chloroform: methanol (2:1, v/v) mixture. The filtrate obtained was washed using 0.9% NaCl. The lipid was evaporated until thick coconut lipid extract were obtained. The extract was then subjected to solvent partition using n-hexane and ethanol 87%. The lower phase was evaporated to yield brownish yellow extract of CocoPLs.
About 5 g of CocoPLs was mixed with 5 g of silica gel in a small amount of chloroform: methanol (9:1, v/v) solution to form a silica slurry. The slurry was then stirred until the mixture was dried and formed fine powder of CocoPLs-SG.
A total of 80 mg of silica gel was poured into a chromatography column and compressed by vacuum. The column was rinsed using chloroform:methanol (9:1, v/v) eluent and vacuumed until all the eluent was eluted. The CocoPLs-SG powder was poured onto the column. Then the column was subjected to compression. Elution was performed using 10 ml of chloroform:methanol (9:1, v/v) solution. Fraction eluted from the column was collected into clean vials. The fraction was analyzed using TLC plate. The spot on the TLC plate was identified with 10% H2SO4 and ninhydrin. Elution was repeated every 10 ml of the eluent until the TLC plate did not show any spot when subjected to identification. The CocoPLs fractions contained ethanolamine species were gathered into an evaporating flask and evaporated at 40°C to obtain dark brownish gel of CocoPEs.
Both CocoPLs and CocoPEs obtained were characterized using FT-IR (Prestige 21 Shimadzu), GC-MS (Shimadzu QP2010S), and LCMSMS (Waters Xevo TQD) and DSC (Shimadzu DSC-60A). The FTIR was employed to probe the phospholipids functional groups. The GC-MS was used to determine the phospholipids fatty acyl chains. The LC-MS/MS was for identifying the chemical component of CocoPEs and the DSC analysis was carried out to explore the CocoPEs phase behavior.
In this research, vitamin C (VC) was used as a model for hydrophilic drug to be encapsulated in coconut liposome [13, 16, 17, 22]. Stock solution of 500 ppm CocoPEs with cholesterol concentration (0%, 10%, 20%, 30%, 40% w/w) were made. A total of 2 mL of each stock solution was diluted with chloroform to 10 mL and poured into a test tube. The liquid solution was evaporated using N2 gas flow to form a thin layer. After that hydration process was carried out. Around 10 mL of phosphate buffer solution was added to the thin film. The mixture was subjected to freeze-thawing process until the thin film was dispersed completely. The dispersions contained empty coconut liposome and was used as control. Other set of dispersions were prepared by adding 8 ppm (C0) VC solution in phosphate buffer pH 7.4 to each 2 mL stock solution and followed by similar process to obtained encapsulated VC in coconut liposome dispersion. The VC concentration in the filtrates obtained after all coconut liposome dispersions were centrifuged were analyzed using UV-Vis spectrophotometer at 265 nm. The concentration of VC was calculated from the filtrate absorbance and represented as Cliposome+VC and Cempty liposome in equation 2. In addition we used CocoPLs as comparison. The encapsulation efficiency of VC in coconut liposome was determined based on Eqs. (1) and (2):
where EE is the encapsulation efficiency; C0 is the initial concentration of VC; and Ct is the unencapsulated VC concentration.
A brownish yellow gel of CocoPLs was obtained from dried coconut meat (
CocoPLs.
In the separation process using vacuum column chromatography, CocoPLs was eluted continuously using chloroform:methanol (9:1, v/v). Each fraction of 10 mL eluent was collected and subjected to identification. As much as 520 fractions were obtained to elute CocoPEs from the CocoPLs samples completely. Identification by TLC using 10% H2SO4 and ninhydrin spotting agent [23] resulted in that CocoPEs were present in the 105th to the 520th fraction.
The fraction contained CocoPEs were then combined and evaporated to remove the eluent that resulted in dark brown CocoPEs gel (
CocoPEs.
The functional groups identification of CocoPLs and CocoPEs was conducted by FTIR spectra analysis. The FTIR spectra of both CocoPLs and CocoPEs were displayed on Figure 3. To analyze further the spectra were scrutinized using a deconvolution program [21, 24], at wavenumbers 3500–2800 cm−1 and 1800–700 cm−1 as presented in Figure 4.
CocoPLs and CocoPEs absorption spectra.
Deconvolution results: (a) CocoPLs at wavenumbers 1800–700 cm−1; (b) CocoPLs at wavenumbers 3500–2800 cm−1; (c) CocoPEs at wavenumbers 1800–700 cm−1; (d) CocoPEs at wavenumbers 3500–2800 cm−1.
The absorption data obtained from both FTIR spectra and deconvolution analysis were compared (see Table 1) to the specific infrared absorption area for phospholipids proposed by Stuart [25] and Hudiyanti et al. [20, 21]. The presence of a typical spectrum of phospholipids was clearly revealed. Significant differences between CocoPLs and CocoPEs spectra was disclosed by the typical absorption of choline and ethanolamine groups on both spectra of CocoPLs and CocoPEs. The choline group absorptions; (CH3)3N+ asymmetric bending and (CH3)3N+ asymmetry stretching; were not present on the CocoPEs spectra. The typical absorption that indicate the presence of ethanolamine species by N-H vibration absorptions was displayed on CocoPLs and CocoPEs spectra. This evident indicated that CocoPLs contained choline and ethanolamine species while CocoPEs did not contain choline species. From The FTIR spectra point of view this data disclosed that the CocoPEs separation from CocoPLs was successful.
No. | Absorption type | References [15, 20, 21, 25] (cm−1) | CocoPLs (cm−1) | CocoPEs (cm−1) | CocoPLs Deconvolution (cm−1) | CocoPEs Deconvolution (cm−1) |
---|---|---|---|---|---|---|
1. | N-H vibration | 3471 | 3394 | 3379 | 3403 | 3373 |
2. | =C-H stretching | 3010 | — | — | 3001 | 3002 |
3. | CH3 asymmetric stretching | 2956 | — | — | 2958 | 2956 |
4. | CH2 asymmetric stretching | 2920 | 2924 | 2924 | 2923 | 2919 |
5. | CH3 symmetric stretching | 2870 | — | — | 2885 | 2890 |
6. | CH2 symmetric stretching | 2850 | 2854 | 2854 | 2850 | 2848 |
7. | C=O stretching, sn-1 chain trans-conformation | 1730 | 1735 | 1735 | 1738 | 1739 |
8. | (CH3)3N+asymmetric bending | 1485 | — | — | 1493 | — |
9. | CH2 scissoring | 1473, 1472, 1468, 1463 | — | — | — | — |
10. | CH3 asymmetric bending | 1460 | 1458 | 1458 | 1461 | 1464 |
11. | (CH3)3N+ symmetric bending | 1405 | — | — | — | — |
12. | CH3 symmetric bending | 1378 | 1373 | 1373 | 1376 | 1378 |
13. | CH3 rocking ribbon progression | 1400–1200 | — | — | 1333 | 1266 |
14. | PO2−asymmetric stretching | 1228 | 1226 | 1242 | 1225 | 1222 |
15. | CO-O-C asymmetric stretching | 1170 | 1165 | — | 1150 | 1165 |
16. | PO2− symmetric stretching | 1085 | — | 1080 | 1106 | 1107 |
17. | CO-O-C symmetric stretching | 1070 | 1072 | — | 1071 | 1070 |
18. | C-O-P stretching | 1047 | — | — | 1020 | 1003 |
19. | (CH3)3N+asymmetric stretching | 972 | — | — | 973 | — |
20. | P-O asymmetric stretching | 820 | 817 | — | 813 | 819 |
21. | CH2 rocking | 730, 720, 718 | 717 | 725 | 714 | 713 |
Typical Absorption of CocoPLs and CocoPEs functional groups.
Bold entries represented the typical absorption of choline and ethanolamine groups on both spectra of CocoPLs and CocoPEs.
The fatty acyl chains content of CocoPLs and CocoPEs was analyzed by GC-MS. The CocoPLs chromatogram was presented on Figure 5. A total of nine peaks was recognized. Seven peaks were with abundance above 1%. The chromatogram suggested that there were at least 9 types of fatty acyl chains present on the CocoPLs. The MS reading revealed the identity of these fatty acyl chains. Three fatty acyl chains worth mentioning with the abundance more than 10%, i.e., lauric acid, palmitic acid and oleic acid which were indicated by peak number 3 (abundance of 11.31%); peak number 5 (15.26%); and peak number 7 (55.18%). The result was in agreement with previous research [15, 20, 21]. The seven fatty acyl chains recognized in CocoPLs was displayed on Table 2.
CocoPLs chromatogram.
Peak number | tR (min) | Fatty acyl chains | Area (%) |
---|---|---|---|
3. | 29.164 | Lauric acid, C12:0 (dodecanoic acid) | 11.31 |
4. | 34.037 | Myristic acid, C14:0 (tetradecanoic acid) | 5.71 |
5. | 38.497 | Palmitic acid, C16:0 (hexadecanoic acid) | 15.26 |
6. | 41.872 | Linoleic acid, C18:2 (9(Z),12(Z)-octadecadienoic acid) | 6.00 |
7. | 42.117 | Oleic acid, C18:1 (9(Z)-octadecenoic acid) | 55.18 |
8. | 42.482 | Stearic acid, C18:0 (octadecanoic acid) | 3.97 |
9. | 52.794 | Lignoceric acid, C24:0 (tetracosanoic acid) | 1.49 |
The fatty acyl chains of CocoPLs.
The chromatogram of CocoPEs was disclosed on Figure 6. The resulting chromatogram exposed the presence of five peaks with abundance above 1% which suggested the presence of five types of fatty acyl chains in the CocoPEs. Three of them had great abundance i.e. capric, linoleic and oleic acids as indicated by peak number 2, 3 and 4 and with abundance of 17.09%, 43.17% and 31.88% respectively. The MS reading of fatty acyl chains content in the CocoPEs was tabulated on Table 3.
CocoPEs chromatogram.
Peak number | tR (min) | Fatty acyl chains | Area (%) |
---|---|---|---|
2. | 38.566 | Capric acid, C10:0 (decanoic acid) | 17.09 |
3. | 42.041 | Linoleic acid, C18:2 (9(Z),12(Z)-octadecadienoic acid) | 43.17 |
4. | 42.198 | Oleic acid, C18:1 (9(Z)-octadecenoic acid) | 31.88 |
5. | 42.555 | Stearic acid, C18: 0 (octadecanoic acid) | 5.93 |
8. | 46.186 | Arachidic acid, C20:0 (eicosanoic acid) | 1.04 |
The Fatty acyl chains of CocoPEs.
Tables 2 and 3 revealed differences to some extent in fatty acyl chains composition between CocoPLs and CocoPEs. CocoPLs had more variation in fatty acyl chains type compared to CocoPEs. This fact plausible considering that CocoPEs was obtained from the separation of CocoPLs. The separation was mainly based on the common head group namely ethanolamine that reflected on the polarity of the separated CocoPEs molecules hence the choice of the separation eluent. More over fatty acyl chains profile were closely related to the position of phospholipid species in the bio-membrane bilayer [26, 27, 28]. Phosphatidylethanolamine (PE) species generally would be positioned in the inner leaflet of bilayer due to their molecular geometry, i.e. cylinder [2]. The PE species molecular shape was supported by more abundance composition of unsaturated fatty acyl chains in the CocoPEs extract, Table 3.
Based on the fatty acyl chains of the CocoPEs we conducted parent ion screening using LCMSMS. The CocoPEs parent ion spectrogram was presented on Figure 7. The spectrogram gave us a representation of the molecular species composing CocoPEs extract. At least 11 molecular species of CocoPEs were found. The CocoPEs molecular species was tabulated on Table 4. The molecular species was predicted based on the head group and combination of two fatty acyl chains for the nonpolar part of CocoPEs species. These similar species would govern the CocoPEs phase behavior and other properties as well.
CocoPEs spectrogram.
No. | m/z (M-H) | Molecular weight | CocoPEs molecular species | |
---|---|---|---|---|
Head group | Fatty acyl chains | |||
1. | 554 | 555 | Ethanolamine | Capric acid Capric acid |
2. | 662 | 663 | Ethanolamine | Capric acid Linoleic acid |
3. | 664 | 665 | Ethanolamine | Capric acid Oleic acid |
4. | 666 | 667 | Ethanolamine | Capric acid Stearic acid |
5. | 694 | 695 | Ethanolamine | Capric acid Arachidic acid |
6. | 770 | 771 | Ethanolamine | Linoleic acid Linoleic acid |
7. | 774 | 775 | Ethanolamine | Oleic acid Oleic acid |
8. | 776 | 777 | Ethanolamine | Oleic acid Stearic acid |
9. | 802 | 803 | Ethanolamine | Linoleic acid Arachidic acid |
10. | 806 | 807 | Ethanolamine | Stearic acid Arachidic acid |
11. | 834 | 835 | Ethanolamine | Arachidic acid Arachidic acid |
CocoPEs molecular species prediction.
Every phospholipid species has unique phase behavior that related to their molecular structure and phase behavior. The phase behavior of CocoPLs and CocoPEs were investigated by thermal analysis using DSC. The thermogram for CocoPLs, Figure 8, exhibited a small peak at 28.85°C and larger peak at 83.95°C. These peaks indicated that CocoPLs underwent phase changes as temperature changes. A pre-transition process from planar-shaped gel (Lb′) to the rippling phase (Pb′) was at a temperature of 28.85°C (Tp), then proceed with the main transition from gel (Lb′) to the liquid crystal phase (La) at a temperature of 83.95°C (Tm) [29, 30, 31]. Tp and Tm were the pre-transition and melting temperature correspondingly.
Thermal analysis of CocoPLs.
Different phase behavior of CocoPEs was exhibited in Figure 9. The thermogram for CocoPEs was more complex than CocoPLs indicated that CocoPEs had more complex phase transition than CocoPLs. CocoPEs displayed pre-transition process from planar-shaped gel (Lb′) to a rippling phase (Pb′) at a temperature of 25.29°C (Tp), followed by a major transition from gel (Lb′) to liquid crystal phase (La) at a temperature of 32.62°C (Tm), and then a transition from the liquid crystal phase (La) to hexagonal phase (H) at a temperature of 65.53°C (Th) [32]. The hexagonal phase formation was consistent to cylindrical molecular shape attributed to CocoPEs. The CocoPEs gradual change of phase was estimated because of the similar molecular species composing CocoPEs.
Thermal analysis of CocoPEs.
The phase behavior of CocoPEs dan CocoPLs above indicated that they were both had complex self-assembly structures which would be beneficial for future applications [2].
Phospholipids has long been known as drug delivery substance due to their liposome forming ability. Liposome was a spherical aggregation structure with bilayer phospholipid as its shell surrounding aqueous core. This unique structure was especially a perfect vehicle for delivering hydrophilic and hydrophobic drugs with storage and controlled release purposes. In this paper as a preliminary study for further application of coconut phospholipid as drug delivery material we used vitamin C as a hydrophilic drug model to be encapsulated in coconut liposomes. Vitamin C was a hydrophilic drug and would be encapsulated inside the aqueous core of liposome. The study lead to that encapsulation efficiency of vitamin C in CocoPEs were higher than CocoPLs i.e. 94.44% and 92.40% respectively, Figure 10.
Encapsulation efficiency of CocoPLs and CocoPEs liposomes with cholesterol composition variation.
In relation to their application as drug delivery, liposomes were usually made from phospholipid and a small amount of cholesterol. Cholesterol was added to the liposome membrane to control liposome rigidity and penetrability [33]. Therefore to explore the effect of cholesterol on the encapsulation efficiency of coconut liposomes we also prepared coconut liposomes with several different concentration of cholesterol namely 10%, 20%, 30% and 40%. The encapsulation efficiency of the liposomes were presented on Figure 10. The results suggested that addition of cholesterol up to 40% in the liposome’s membrane reduced the encapsulation efficiency of CocoPEs and CocoPLs liposomes. Furthermore CocoPEs liposomes demonstrated slighter reduction than CocoPLs liposomes. The encapsulation efficiency of CocoPEs diminished gradually as the cholesterol concentration increased while for CocoPLs liposomes the decline was arbitrary. Addition up to 30% of cholesterol only reduced the CocoPEs encapsulation efficiency to around 80% while CocoPLs was as low as 52%. Cholesterol effect on the encapsulation efficiency of CocoPEs liposomes more consistent than CocoPLs. We suspected it was due to the molecular composition of the phospholipid in the membrane. The molecular composition was represented by the composition of functional group and fatty acyl chains in the CocoPEs and CocoPLs, Tables 1–3. In the liposome membrane cholesterol interacted with CocoPEs and CocoPLs through their functional groups and fatty acyl chains. Cholesterol with small hydrophilic head group i.e., –OH and big and rigid hydrophobic steroid ring would interact better with small head group phospholipid species like CocoPEs than CocoPLs which had big spherical choline group and possibly other head groups as well. The composition of fatty acyl with double bonds also suspected would give more room for cholesterol hydrophobic moiety. The fatty acyl chains would assume “kink” structure at the double bond position [34, 35] and allocate more space hence more comfortable for cholesterol to integrate. With smaller number of fatty acyl chains type and higher concentration of double bond made cholesterol effect became more systematic in the CocoPEs liposome membrane. The data gave an insight about the application of CocoPEs as encapsulation material. CocoPEs was a good candidate for encapsulation hydrophilic material.
A total of (
DH and KA would like to express their gratitude of financial support by DIPA Selain APBN FSM UNDIP Riset Madya, 2018.
The authors declare that there is no conflict of interests regarding the publication of this chapter.
IntechOpen is the first native scientific publisher of Open Access books, with more than 116,000 authors worldwide, ranging from globally-renowned Nobel Prize winners to up-and-coming researchers at the cutting edge of scientific discovery. Established in Europe with the new headquarters based in London, and with plans for international growth, IntechOpen is the leading publisher of Open Access scientific books. The values of our business are based on the same ones that any scientist applies to their research -- we have created a culture of respect, collegiality and collaboration within an atmosphere that’s relaxed, friendly and progressive.
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