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(Piperales) I. Plastid DNA Phylogeny and Chromosome Number of Peperomia Subgenus Micropiper

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(Piperales) I. Plastid DNA Phylogeny and Chromosome Number of Peperomia Subgenus Micropiper ISSN 1346-7565 Acta Phytotax. Geobot. 70 (1): 1–17 (2019) doi: 10.18942/apg.201815 Biosystematic Studies on the Family Piperaceae (Piperales) I. Plastid DNA Phylogeny and Chromosome Number of Peperomia subgenus Micropiper * Yukihiro h. kobaYashi , shizuka Fuse and Minoru n. TaMura Department of Botany, Graduate School of Science, Kyoto University, Kitashirakawa-oiwake-cho, Sakyo-ku, Kyoto 606-8502, Japan. * [email protected] (author for correspondence) To evaluate the evolutionary relationships among species of Peperomia subg. Micropiper, a phylogenet- ic analysis based on the DNA sequences of plastid regions atpB-rbcL, psbK-I, rpL16, rpS16, trnG, trnK (including matK), trnL-L-F, and trnS-G was conducted using 20 species, in addition to four outgroup species. The trnK sequences of 46 species and trnL-L-F sequence of one species were quoted from Gen- Bank and also included in the analysis. The results showed that P. subg. Micropiper includes seven major clades, which are also supported by morphological characteristics. They are recognized as section- equivalent plant groups, namely Alatoid, Blandoid, Glabelloid, Glaucoid, Japonicoid, Lanceolatoid, and Rotundifolioid. A chromosome analysis of the subgenus yielded nine new counts: 2n = 22 (diploid) for P. alata, P. bicolor, P. diaphanoides, P. flexicaulis, P. hylophila, P. polystachya and P. prosterata, 2n = 44 (tetraploid) for P. okinawensis and 2n = 132 (dodecaploid) for P. reticulata. Japonicoid, which occurs outside the Americas, i.e. in Asia, Africa, and the Pacific islands, is tetraploid, decaploid, and dodeca- ploid (not diploid), while the remaining six plant groups are native to the Americas and diploid (except Glaucoid, which is tetraploid). Further, P. diaphanoides is conspecific with P. glabella. Peperomia boninsimensis from the Ogasawara Islands, Japan, is more closely related to Polynesian species than to other Japanese species. Peperomia okinawensis should be regarded as a variety of P. japonica. Key words: chromosome number, Micropiper, molecular phylogeny, Peperomia blanda, Peperomia boninsimensis, Peperomia diaphanoides, Peperomia japonica var. okinawensis, Piperaceae, plastid DNA, primitive angiosperms Piperales Bercht. & J. Presl have long attract- Piperaceae Giseke, along with Saururaceae ed attention as primitive angiosperms (Cronquist Rich. ex T. Lestib. and Aristolochiaceae Juss., 1957, 1988, Takhtajan 1969, Tamura 1974, En- constitute the Piperales. (APG IV 2016). The dress & Friis 1994). They share apocarpy, mono- family is considered to be one of the more mor- sulcate pollen grains, ethereal oil cells, and rich phologically advanced of the Piperales (Tamura endosperm with other primitive angiosperms, 1974), because it has simple flowers with only one such as Magnoliales Juss. ex Bercht. & J. Presl, orthotropous ovule per ovary and lacks a peri- Canellales Cronq., and Chloranthales Mart., all of anth. Based on Samain et al. (2008), the Pipera- which (including Piperales) are included in the ceae include five genera: Piper L., Peperomia basal clades of angiosperms (APG IV 2016). Ruiz & Pav., Zippelia Blume, Manekia Trel., and Piperales may also be related to monocots. Burg- Verhuellia Miq. er (1977) reported the morphological similarity to The molecular phylogenetics of the Pepero- monocots; e.g. atactostele and 3-merous flowers. mia has been studied by Wanke et al. (2006), Nevertheless, the taxonomy of Piperales has not Smith et al. (2008), Samain et al. (2009), and been adequately studied. Frenzke et al. (2015). They analyzed the DNA se- 2 Acta Phytotax. Geobot. Vol. 70 Fig. 1. Morphology and habit of species of Peperomia subg. Micropiper. A, P. verticillata (Blandoid) [Kobayashi 90 (KYO)] with dimorphic leaves (a, b); B, P. prostrata (Alatoid) [Kobayashi 6 (KYO)] with shoot continuing to grow after flowering (c) and white-lined veins of leaves (d); C, P. bicolor [Kobayashi 96 (KYO)]; D, P. japonica (Japonicoid) [Tamura et al. 44019 (KYO)]; E, P. glabella (Glabelloid) [Kobayashi 34 (KYO)] with grooved veins of leaves (e); F, P. galioides (Glau- coid) [Kobayashi 86 (KYO)] with dimorphic leaves (f, g). quences of trnK (3,204 bp), trnL+trnL- distinguished from other subgenera by densely F+ndhF+g3pd (5,235 bp), trnK+ITS+26S (5,906 the viscid-papillose fruits. Based on Frenzke et bp), and trnK+trnK-psbA (4,870 bp), respectively, al. (2015) and Tropicos (2018), 419 of the 596 spe- and revealed the monophyly of the genus and the cies of P. subg. Micropiper are endemic to the subgeneric relationships. Frenzke et al. (2015) American tropics, while the remaining 177 spe- classified Peperomia (1,520 spp.) into 14 subgen- cies are distributed in Asia, Africa, and the Pa- era primarily based on molecular phylogenetic cific islands. In contrast, the 13 subgenera are en- data: Micropiper (Miq.) Miq. (596 spp.), Pseudo- demic to the Americas, with the exception of P. cupula Frenzke & Scheiris (157 spp.), Leptorhyn- tetraphylla of subg. Pseudocupula. Thus, molec- chum (Dahlst.) Trel. ex Samain (147 spp.), Multi- ular phylogenetic studies of P. subg. Micropiper palmata Scheiris & Frenzke (105 spp.), Tildenia are needed to improve our understanding of (Miq.) Miq. ex Dahlst. (58 spp.), Oxyrhynchum Asian Peperomia. In addition, few data regarding (Dahlst.) Samain (57 spp.), Fenestratae Pino (42 chromosome number and polyploidy are avail- spp.), Peperomia (18 spp.), Erasmia (Miq.) Dahlst. able (Table 1), although these are important char- (13 spp.), Pleurocarpidium Dahlst. (11 spp.), His- acters for tracing evolution along molecular phy- pidulae Frenzke & Scheiris (10 spp.), Perlucida logenetic trees. Scheiris & Frenzke (7 spp.), Phyllobryon (Miq.) In Japan, there are three species of Pepero- Scheiris & Frenzke (7 spp.), and Panicularia mia, P. boninsimensis, P. japonica and P. oki- Miq. (6 spp.). However, the remaining 286 spe- nawensis, all of which have taxonomic issues. cies have not been assigned to any of the subgen- Peperomia boninsimensis is endemic to the Oga- era. sawara Islands, which are ca. 1,000 km distant In this study, we focused on Peperomia subg. from Honshu, and its close relatives are unknown. Micropiper (Fig. 1), which was circumscribed by In Tseng et al. (1999), P. japonica is treated as a Frenzke et al. (2015). It consists of pantropically synonym of P. blanda; however, this synonymy distributed terrestrial or epiphytic herbs that are has not been confirmed by molecular methods. February 2019 kobaYashi & al. –Cp Phylogeny of Peperomia subg. Micropiper 3 Table 1. Present and previous cytological studies of the Peperomia subg. Micropiper species that were investigated here mo- lecular phylogenetically. Taxon Present count Previous count Reference (2n) (n) (2n) P. alata Ruiz & Pav. 22* P. bicolor Sodiro 22* 36 Jose et al. (1994) P. blanda (Jacq.) Kunth 22 22 Samuel & Morawetz (1989) P. boninsimensis Makino 110 Okada (1986) P. boninsimensis c.110 Ono (1977) P. diaphanoides Dahlst. 22* P. dindygulensis Miq. 44 Mathew et al. (1999) P. dindygulensis 44II Mathew et al. (1998) P. fenzlei Regel 44 Samuel & Morawetz (1989) P. fernandeziana Miq. 22+2 Valdebenito et al. (1992) P. fernandeziana 23+2, c.22 Spooner et al. (1987) P. fernandeziana c.22 Sanders et al. (1983) P. flexicaulis Wawra 22* P. galioides Kunth 44 c.22 Valdebenito et al. (1992) P. glabella (Sw.) A. Dietr. 22 22 Samuel & Morawetz (1989) P. glabella ‘Variegata’ 36 Jose et al. (1992) P. heyneana Miq. 22 Mathew et al. (1999) P. heyneana 22II Mathew et al. (1998) P. hylophila C. DC. 22* P. japonica Makino 44 Okada (1986) P. okinawensis T. Yamaz. 44* P. polystachya (Ait.) Hook. 22* P. portulacoides (Lam.) A. Dietr. 22 44 Mathew et al. (1999) P. portulacoides 22II Mathew et al. (1998) P. prostrata B. S. Williams 22* P. reticulata Balf. f. 132* P. rotundifolia (L.) Kunth 22 Jose et al. (1994) P. rubella Hook. 22 22 Bai & Subramanian. (1985), Samuel & Morawetz. (1989) P. skottsbergii C. DC. c.24 Valdebenito et al. (1992) P. skottsbergii c.23 Spooner et al. (1987) P. skottsbergii 22–24 Sanders et al. (1983) P. urvilleana A. Rich. 22 Beuzenberg & Hair (1983) P. urvilleana 44 Murray & Lange (1999) P. verticillata (L.) A. Dietr. 22 22 Samuel & Morawetz (1989) *These numbers are first counted. Although the independence of P. okinawensis has species, second to accumulate information on been questioned (Yonekura 2015), its molecular chromosome number and ploidy level of P. subg. phylogeny has not been evaluated. Micropiper to assess the cytological diversity in The purpose of this study was first to con- the subgenus, and third to revise the previous struct a molecular phylogenetic tree of Pepero- species-level taxonomic treatments and deter- mia subg. Micropiper to show species-level reso- mine the evolutionary units within P. subg. Mi- lution and to reveal the relationships among the cropiper based on all available information. 4 Acta Phytotax. Geobot. Vol. 70 Table 2. Plant materials used in this study. All voucher specimens are preserved in the herbarium of Kyoto University (KYO). Taxon Source / Origin Chro- Voucher mosome Accession number observa- tion atpB-rbcL psbK-I rpL16 rpS16 trnG trnK trnL-L-F trnS-G Peperomia subg. Micropiper a P. alata Cult. KBG , America Kobayashi 92 ○ LC440976 LC440939 LC456943 LC456906 LC440902 LC457017 LC440693 LC456980 Cult. KBG, P. bicolor Kobayashi 96 America ○ LC440962 LC440925 LC456929 LC456892 LC440888 LC457003 LC440679 LC456966 Cult. KBG, P. blanda Kobayashi 75 America ○ LC440973 LC440936 LC456940 LC456903 LC440899 LC457014 LC440690 LC456977
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