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Origin of Cultivated Citrus (Rutaceae) Documented by the Contents of Internal Transcribed Spacer Sequences (ITS) in Nuclear Ribosomal DNA

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Origin of Cultivated Citrus (Rutaceae) Documented by the Contents of Internal Transcribed Spacer Sequences (ITS) in Nuclear Ribosomal DNA J. Jpn. Bot. 88: 222–238 (2013) Origin of Cultivated Citrus (Rutaceae) Documented by the Contents of Internal Transcribed Spacer Sequences (ITS) in Nuclear Ribosomal DNA a, a b c Hiroki YAMAJI *, Kenji KONDO , Takeshi KUNIGA , Hirohisa NESUMI , b a a Toshio YOSHIDA , Kazunori HASHIMOTO and Osami TAKEDA aBotanical Raw Materials Research Department, Botanical Raw Materials Division, Tsumura & Co., 3586, Yoshiwara, Ami-machi, Ibaraki, 300-1192 JAPAN; bCitrus Research Station, National Institute of Fruit Tree Science, National Agriculture and Food Research Organization, 485-6, Nakamachi, Okitsu, Shimizu-ku, Shizuoka, 424-0292 JAPAN; cShikoku Research Center, Nation Agricultural Research Center for Western Region, Senyû, Zentsûji, Kagawa, 765-8508 JAPAN *Corresponding author: [email protected] (Accepted on May 23, 2013) In Citrus cultivars, mandarins, pummelos, citrons, and kumquat/papeda groups were estimated to contribute as parental species for almost Citrus cultivars in precedent studies. In order to verify the hypothesis and to estimate the parental wild species of each Citrus cultivar, this study documented variation of the internal transcribed spacer (ITS) ribotypes of nuclear ribosomal DNA in 61 accessions of 33 species two varieties belonging to major Citrus cultivars, wild Citrus, and related genera. Six species and one variety, e.g., C. deliciosa, C. medica, C. maxima, had non-additive or almost non-additive sequences, probably consisting of a single ribotype. They were thought to have developed not through hybridization but by selection, and were probably putative parental wild species of Citrus cultivars or their direct descendants. In contrast, most Citrus cultivars, e.g., C. limon, C. sinensis, C. aurantium, showed additive states in a number of sites, and consisted of 2–4 major phylogenetically distinct ribotypes. They were estimated as hybrid origin. In the Citrus species examined in this study, 18 ribotypes were recognized, and were classified into nine phylogenetically distinct groups. Among them, four groups were regarded as correspondent to mandarins, pummelos, citrons, and kumquat/papeda groups as well as precedent hypotheses. To the contrary, the rest five groups were probably not included in any putative parental species estimated in precedent studies. Therefore, in addition to foregoing four parental species, at most five putative parental species are presumably existent or were probably existent in the past, and participated in the development of cultivars of Citrus. Origins of major Citrus cultivars were discussed based on ribotype combinations. Key words: Citrus cultivar, hybrid origin, internal transcribed spacer (ITS) of nuclear ribosomal DNA. Species belonging to Citrus L. (Rutaceae) and Poncirus Raf.) are the most popular fruits and its allied genera (e.g., Fortunella Swingle of the world (Iwamasa 1976, 1999), and many —222— August 2013 The Journal of Japanese Botany Vol. 88 No. 4 223 kinds are cultivated for various purposes. et al. 1993) suggested the basic, true species The taxonomy of these species has been a hypothesis proposed by Scora (1975) and challenge for botanists because the number of Barrett and Rhodes (1976). Moreover, Torres et species recognized in Citrus s. str. differs among al. (1978) have estimated parental combinations systems. Swingle (1946) and Swingle and Reece using isozyme patterns; C. aurantifolia (1967) recognized 16 species that are wild or (Christm.) Swing. and C. limon have been naturally hybridized. They did not recognize suggested to be a hybrid of species belonging to almost all artificially created cultivars as taxa. subgenus Papeda and C. medica, C. sinensis and In contrast, Tanaka (1954, 1977) has treated C. aurantifolia, respectively. Also, C. aurantium artificially created cultivars as species equally has been estimated to be a hybrid between C. with the wild ones, and recognized as many as maxima and C. reticulata (Scora 1975, Torres 162 species. Such discrepancies between the et al. 1978). These findings are also supported previous taxonomic systems are due to whether by chemical variations in polymethoxyflavones they recognize cultivars as taxa. Furthermore (Mizuno et al. 1991). as causative role for confusion, Swingle (1946) Federici et al. (1998) have estimated the and Swingle and Reece (1967) assigned species phylogenetic relationships of Citrus and its names to representative cultivated species from related genera using RFLP and RAPD analyses, ancient days such as Citrus aurantium L., C. and showed that most species described as sinensis (L.) Osb., and C. limon (L.) Burm. f. hybrids in the preceding reports had no unique as in wild species while the other cultivars were fragments but high heterozygosity indices. described without taxonomic position. Such However, this study is difficult to interpret imbalanced treatments are due to lack of clarity because they postulated hybridism of each over of hybridism. If they are hybrid origin, species in advance. Araújo et al. (2003) showed which wild species participated as parent of each a phylogenetic relationship of subfamily cultivar? based on noncoding sequences of chloroplast Thus, the number and identities of parental DNA. In their results, Citrus did not compose wild species that have contributed to the a monophyletic clade but instead a clade development of Citrus cultivars is the center of with Poncirus, Fortunella, and Microcitrus. controversy. Chemotaxonomic (Scora 1975) and Bayer et al. (2009) also reported Citrus was numerical taxonomic (Barrett and Rhodes 1976) paraphyletic with seven related genera based examinations have indicated that three species, on three noncoding region of chloroplast DNA. citron (C. medica L.), pummelo (C. maxima However, this study did not document reticulate (Burm.) Merr.), and mandarin (C. reticulata evolution of Citrus including a putative artificial Blanco), are the parental species, which are hybridization event because chloroplast genomes defined by Swingle and Reece (1967). Other are commonly inherited only maternally. cultivated Citrus species in subgenus Citrus Among the precedent studies, Barkley et are believed to be hybrids derived from these al. (2006) is the most comprehensive both parental species , belonging to subgenus Papeda, in sample size and in number of molecular or the other related genera (Barkley et al. 2006). markers. They used 24 simple sequence repeat Recent molecular analyses can reveal (SSR) markers on as many as 370 Citrus the processes of crossbreeding and reticulate accessions. In this study, a Model-based evolution of plants more explicitly (Arnold clustering approach identified five populations; 1997). For Citrus cultivars, the results of mandarins, pummelos, citrons, trifoliates, fraction I protein analysis (Handa et al. 1986) and kumquat/papeda group. Among the five and mitochondrial DNA analysis (Yamamoto populations, trifoliates (Poncirus) were supposed 224 植物研究雑誌 第 88 巻 第 4 号 2013 年 8 月 not to contribute to many Citrus cultivars. These estimated through classification of the ribotypes. basic species coincide with those of Scora Li et al. (2010) conducted cloning analysis (1975) and Barrett and Rhodes (1976). Both for ITS region for 30 accessions in addition to the phylogenetic and model-based clustering AFLP, three intergenic region sequence analysis analyses supported the hypothesis that there are of cpDNA. This study showed that five old only a few naturally occurring species of Citrus, cultivars; C. aurantifolia, C. limon, C. paradisi, and most of these Citrus cultivars arose through C. sinensis and C. aurantium were hybrid origin, various hybridization events between the and as with Barkley et al. (2006), four parental naturally occurring species. However, Barkley et species; mandarin, citron, papeda and pummelo alʼs (2006) study seems predetermined because participated to generate these cultivars. However, it selected putative non-hybrid strains to estimate Li et al. (2010) did not consider phylogenetically phylogenetic relationships. distinct ribotypes from the putative four species. Therefore, we searched for hidden, preserved Moreover, as only Poncirus was accepted as molecular traits of original species from putative outgroup; it probably misled phylogenetic hybrids, cultivated Citrus species. Among relationships of ribotypes because six other the many molecular markers, the internal genera formed a monophyletic clade with a part transcribed spacer (ITS) regions of nuclear of Citrus based on cpDNA sequences (Araújo et ribosomal DNA (nrDNA) can in many cases al. 2003, Bayer et al. 2009). provide direct evidence of hybridization, Our goals in the present study are (1) to reticulate evolution, and putative parental document variation of ribotypes in major Citrus species (Baldwin et al. 1995, Sang et al. 1995, cultivars in the world and in Japan in comparison Wendel et al. 1995, Soltis et al. 1998, Yamaji et with an evident hybrid cultivar, wild species and al. 2005, 2007). This information is available related genera, (2) to estimate nature and number because the ITS sequences exist in nrDNA as of parental species that have participated in a tandem multicopy array, maintaining more the development of Citrus cultivars based on than two different ribotypes and traces of past phylogenetic relationship of their ribotypes, (3) hybridization as heterozygosity of different to verify effectivity of ITS analysis for parental ribotypes. Therefore, even in diploid hybrids like estimation of diploid hybrids between
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