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Molecular Systematics of Abelmoschus (Malvaceae) And Molecular systematics of Abelmoschus (Malvaceae) and genetic diversity within the cultivated species of this genus based on nuclear ITS and chloroplast rpL16 sequence data Olaf Werner, Mahmoud Magdy & Rosa María Ros Genetic Resources and Crop Evolution An International Journal ISSN 0925-9864 Volume 63 Number 3 Genet Resour Crop Evol (2016) 63:429-445 DOI 10.1007/s10722-015-0259-x 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Genet Resour Crop Evol (2016) 63:429–445 DOI 10.1007/s10722-015-0259-x RESEARCH ARTICLE Molecular systematics of Abelmoschus (Malvaceae) and genetic diversity within the cultivated species of this genus based on nuclear ITS and chloroplast rpL16 sequence data Olaf Werner . Mahmoud Magdy . Rosa Marı´a Ros Received: 7 January 2015 / Accepted: 27 April 2015 / Published online: 9 May 2015 Ó Springer Science+Business Media Dordrecht 2015 Abstract The genus Abelmoschus includes several species. The genetic diversity within A. esculentus crop plants which are especially important in SE Asia and A. caillei is low if compared with A. manihot. The and several African countries. However, the system- evidence presented here does not allow us to draw any atic treatment of this genus is difficult, in part because conclusions about the geographic origin (Africa vs. hybridization between different forms seems to be Asia) of A. esculentus. frequent. In this study we present nuclear internal transcribed spacer ITS and chloroplast rpL16 se- Keywords Abelmoschus caillei Á Abelmoschus quences with the aim of reconstructing phylogenetic esculentus Á Abelmoschus tetraphyllus Á Crop plants Á relationships within Abelmoschus, and its relationship Phylogenetic relationships Á Taxonomy with the genus Hibiscus and other related Malvaceae. Based on our analysis of nuclear ITS and chloroplast rpL16 sequence data, Abelmoschus is resolved as a monophyletic clade. Abelmoschus tetraphyllus is Introduction clearly separated from A. manihot but closely related to A. ficulneus and should not be treated as a Depending on the treatment, the genus Abelmoschus subspecies of A. manihot. None of the wild species Medik. may include from 6 (van Borssum-Waalkes included in this study can be confirmed as an ancestor 1966) to 14 (Hochreutiner 1924) species. The center of of A. esculentus or A. caillei. Neither A. esculentus nor its distribution lies in South East Asia, but A. ficulneus A. caillei can be distinguished from each other by the (L.) Wight and Arn. is found in Africa, Asia and markers used for this study, although the evidence Australia (Siemonsma 1982; Charrier 1984; Lamont does not exclude the possibility of a hybrid origin of A. 1999), and A. moschatus Medik. subsp. tuberosus caillei involving A. esculentus and an unknown (Span.) Borss.-Waalk. is found in the tropical regions of Northern Australia. Although Medikus established the genus in 1787, it was not until the work of & O. Werner ( ) Á R. M. Ros Hochreutiner (1924), which clearly defined key mor- Departamento de Biologı´a Vegetal (Bota´nica), Universidad de Murcia, Campus de Espinardo, phological characteristics (essentially the caducous 30100 Murcia, Spain calyx), that the genus was generally accepted. Within e-mail: [email protected] the genus, there are still several unresolved taxonomic problems (Hamon and van Sloten 1995); e.g., the M. Magdy Genetic Department, Faculty of Agriculture, Ain Shams nature of some infraspecific categories of A. moscha- University, 68 Hadayek Shubra, 11241 Cairo, Egypt tus and A. manihot (L.) Medik., the position of A. 123 Author's personal copy 430 Genet Resour Crop Evol (2016) 63:429–445 caillei (A. Chev.) Stevels within the genus, and the Academies 2006). The total world area occupied by relationship of A. esculentus (L.) Moench to the okra culture in 2012 rose to 1,085,146 ha and suggested wild forms, A. tuberculatus Pal et Singh and production reached 8,359,944 tonnes (Food and A. ficulneus. Agriculture Organization of the United Nations Four species, A. caillei, A. esculentus, A. manihot 2014), India and Nigeria being the main producers. and A. moschatus, are cultivated and are now Two recent reviews (Benchasri 2012; Kumar et al. distributed through tropical and subtropical regions 2010) provide detailed descriptions of the chemical of the world, with the exception of the first, which is composition of okra leaves, unripe pods and seeds and restricted to West Africa (Siemonsma 1982). Accord- possible uses for different plant parts. One of the most ing to Mansfeld´s World Database of Agricultural and important aspects is the amino acid composition of the Horticultural Crops (http://mansfeld.ipk-gatersleben. seeds, which are rich in tryptophan and sulfur- de/apex/f?p=185:3:9797333538778; Ochsmann et al. containing amino acids, and, unlike the proteins of 1999) other species like A. angulosus Wight et Arn., A. cereals and pulses, are balanced in both lysine and crinitus Wall., and A. ficulneus are also used as crop tryptophan amino acids (National Research Council of plants. There are several uses for the cultivated spe- the National Academies 2006). cies. For example, A. moschatus is used as a vegetable While wild and cultivated forms coexist within both (leaves, unripe seed pods) (Facciola 2001; Manandhar A. manihot and A. moschatus, the origins of A. 2002; National Research Council of the National esculentus and A. caillei are not well established. Academies 2006). The seeds possess a musky odor, Cytogenetic data (Siemonsma 1982) suggest that A. and perfumers know them as ambrette (‘‘abel- esculentus is an amphidiploid possessing a genome in moschus’’ from the Arabic ‘‘father of musk’’, with common with A. tuberculatus and a complementary ‘‘moschatus’’ also referring to a musky smell) (Na- genome, whose origin has not yet been established. tional Research Council of the National Academies This would imply an Asian origin of A. esculentus 2006) and use them as a perfume ingredient (Singh because A. tuberculatus is native to Uttar Pradesh, et al. 1996). The plant has also a wide variety of north India (Hamon and van Sloten 1995). Another medical uses (Agharkar 1991; Bown 1995), including hypothesis (Hamon and van Sloten 1995) suggests that the treatment of depression and anxiety, stomatitis and African populations of A. ficulneus are a possible gonorrhea. ancestor of A. esculentus, therefore making it of Abelmoschus manihot is cultivated for its leaves, African origin. but its immature pods are too prickly to be consumed Although Abelmoschus includes important crop (Hamon and van Sloten 1995). Pharmacological species and offers interesting pharmaceutical uses, effects, including anti-inflammatory, anti-viral, anti- there are very few data available related to its bacterial, wound healing, and anti-fungal activities, molecular systematics. A search of accessions avail- have been confirmed for this species (Todarwal et al. able at GenBank made on 19 November 2014 returned 2011). Several infraspecific taxa have been described, only 52 nucleotide sequences. Pfeil et al. (2002) and one of the most important being A. manihot var. Small (2004) added isolated DNA sequences of tetraphyllus Hochr. (Hochreutiner 1924) but the Abelmoschus specimens when they studied aspects taxonomic status of this entity remains unclear. For of the molecular systematic of Hibiscus L. Other example, van Borssum-Waalkes (1966) considered it researchers working with molecular markers have as a subspecies and Hamon and van Sloten (1995) centered their attention on variability found among recommended giving it species rank. Abelmoschus cultivars of specific geographical re- Okra (A. esculentus) is a widely used plant in gions. Gulsen et al. (2007) used SRAP to investigate tropical and subtropical countries all around the world. diversity and relationships within Turkish germplasm, Abelmoschus caillei, the West African okra or atypical and Sawadogo et al. (2009) used SSR markers to study okra (Martin et al. 1981), in contrast, is restricted to the genetic diversity of okra from Burkina Faso. western Africa. The pods, leaves, and seeds of these Salameh (2014) studied genetic relationships among two species are edible. Among their useful non-food 48 okra genotypes (mainly of A. esculentus) from products are mucilage, industrial fiber, and medicines different agro-ecological regions with AFLP markers. (National Research Council of the National In a RAPD-marker study by Prakash et al. (2011), two 123 Author's personal copy Genet Resour Crop Evol (2016) 63:429–445 431 samples of A. caillei were deeply nested within A. biogeography of angiosperms. For example, with esculentus samples. Interestingly, in a similar study maternal inheritance chloroplast DNA can only also using RAPD markers, Aladele et al. (2008) found migrate with the seed while nuclear genes may that these two species were clearly separated. migrate twice (in the pollen and the seed) (Petit et al. More recently, Schafleitner et al. (2013) used 1993). As a consequence, this can lead to a higher transcriptome data to develop SSR markers. Their differentiation between populations when analyses are study included three species, mainly A. esculentus based on chloroplast DNA markers as compared to from a vast geographical range alongside two samples nuclear markers, because of the higher levels of pollen of A. manihot and A. moschatus each. The clustering of flow.
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