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14, 2014 Download T REPRO N DU LA C The International Journal of Plant Reproductive Biology 6(1) pp. 1-14, 2014 P T I F V O E B Y T I O E I L O C G O S I S T E S H T Hybrid Origin of Nephrolepis ×hippocrepicis Miyam. (Nephrolepidaceae) Tzu-Tong Kao1, Wen-Liang Chiou1, Sheng-Yuan Hsu1, Chun-Ming Chen2, Yi-Shan Chao1 & Yao-Moan Huang 1* 1 Taiwan Forestry Research Institute, 53 Nan-Hai Rd., Taipei 10066, Taiwan 2Dr. Cecilia Koo Botanic Conservation Center, 31 Tongsing Rd., Gaoshu Township, Ping-Tung 90646, Taiwan *e-mail: huangym@tfri.gov.tw Received: 10. 05. 2013; Revised & Accepted: 23.06.2013; Published online: 01.10.2013 ABSTRACT Plants of Nephrolepis ×hippocrepicis Miyam. found in the Taipei Botanical Garden, northern Taiwan, were characterized by mostly aborted and a few abnormally large-sized spores, closely- adjoining lanceolate triangulate pinnae, reniform indusia, and bi-colored basal scales with caudate apexes. These characters and C-value of N. ×hippocrepicis are intermediate between those of N. biserrata and N. cordifolia. Its bidirectional interspecific hybrid origins between N. biserrata and N. cordifolia have been identified based on the DNA sequences of a chloroplast region atpB-rbcL spacer and two nuclear regions CAS1 (cycloartenol synthase 1) and gapCp (glyceraldehydes-3-phosphate dehydrogenase) genes. Its spore germination rate was less than 1% and none of the gametophyte produced young sporophyte. Instead of sexual reproduction, the species is likely to propagate through runners and new hybridization events. Keywords: Hybrid, Nephrolepis biserrata, Nephrolepis cordifolia, Nephrolepis ×hippocrepicis INTRODUCTION brownii (Desv.) Hovenkamp & Miyam. (Knapp 2011). All of these are widely distributed in Taiwan. Some plants of Nephrolepis with abnormal spores were Nephrolepis Schott, a monophyletic genus of discovered on two adjacent palms Phoenix hanceana Nephrolepidaceae (Kramer 1990, Hennequin et al. Naudin and Butia capitata (Mart.) Becc. in 2004 at the 2010) is widely distributed in tropical regions. Species Taipei Botanical Garden (TPBG) (Fig. 1B). They are of this genus are characterized by articulate pinnae, both with morphology intermediate between N. biserrata and creeping and erect rhizomes, and reniform to lunulate N. cordifolia and identified as N. ×hippocrepicis indusia. The monophyly of this genus has been Miyam., a hybrid firstly reported at Ryukyu Island of determined by Hennequin et al. (2010). Japan (Hovenkamp & Miyamato 2005). In Taiwan, three Nephrolepis species recorded are N. This study aims to determine the hybrid origin of N. biserrata (Sw.) Schott; N. cordifolia (L.) C. Presl; and N. ×hippocrepicis at the TPBG by comparing their 2 The International Journal of Plant Reproductive Biology 6(1) pp.1-14, 2014 January, 6 (1) 2014 Hybrid origin of Nephrolepis ×hippocrepicis 3 Table 2 — Primers used to amplify and sequence DNA from members of the Nephrolepis in this study. morphology, C-value, and molecular data. Their atpB-1, rbcL-1, CAS1_2620F, CAS1_3523R, reproductive strategy was also studied. ESGAPCP8F1 and ESGAPCP11R1 (Table 2). The DNA region Primer Primer sequence Primer source primers for the region of CAS1 gene were newly atpB-rbcL atpB-1 5'-ACATCKARTACKGGACCAATAA-3' Chiang et al., 1998 MATERIAL & METHODS designed in this study. These three regions were amplified separately with standard polymerase chain atpB-rbcL rbcL-1 5'-AACACCAGCTTTRAATCCAA-3' Chiang et al., 1998 Plant materials were collected at the TPBG around reaction (PCR) using a T3 Thermocycler (Biometra, CAS1 CAS1_2620F 5'-AGGGCGAATGTGGTGTCAT-3' This study the two palms, No. 4420 (Phoenix hanceana Naudin) Göttingen) under the following conditions: (1) CAS1 CAS1_3523R 5'-ATCTTCATGCCATCTTCTGC-3' This study and No. 4428 (Butia capitata Becc.). Samples were denaturing 5 min at 95 °C; (2) denaturing, annealing, and gapCp ESGAPCP8F1 5'-ATYCCAAGYTCAACTGGTGCTGC-3' Schuettpelz et al., 2008 collected from different trees or different sides and extension 35 cycles; denaturing 45 s at 94 °C; annealing different heights of the same palm to avoid sampling the 45 s at 50 °C (atpB-rbcL), 54 °C (gapCp gene), or 56 °C gapCp ESGAPCP11R1 5'-GTATCCCCAYTCRTTGTCRTACC-3' Schuettpelz et al., 2008 same clone. The voucher specimens were deposited in (CAS1 gene); extension 75 s at 72 °C; (3) final extension the herbarium TAIF, Taiwan Forestry Research Institute 8 min at 72 °C. Some PCR products were sequenced hand. The cladistic analyses of sequencing data were Each of the three species, N. biserrata, N. (Table 1). Morphologies of N. ×hippocrepicis, N. directly, while others were cloned into pGEM-T Easy performed by the maximum parsimony (MP) and the ×hippocrepicis, and N. cordifolia, had ca. 64 spores per biserrata and N. cordifolia were examined and vectors (Promega, Madison). Ligation, transformation, neighbor-joining (NJ) method using PAUP* v. 4.0b10 sporangium (the abortive spores in N. ×hippocrepicis compared. Spore number per sporangium, spore plating and selection of clones followed the instructions (Swofford 2002). All characters were weighted equally were also counted). Germination percentages of their morphology, spore germination percentage, and C-value included with the kit. 30 clones in each sample were and gaps were treated as fifth base (MP) or pair-wise fresh mature spores were 96%, < 1%, and 97%, were determined following Huang et al. (2009) and screened using T7 and SP6 vector primers (Lunt et al. deletion (NJ). The most parsimonious trees were respectively. Only N. biserrata and N. cordifolia Chao et al. (2012). 1999). The plasmid DNAs from the 10 positive clones obtained with heuristic searches of 1000 replicates with Total genomic DNA was extracted using Plant produced sporophytes through their spore cultures. C- were purified using the High-Speed Plasmid Mini Kit random stepwise sequence addition, tree Genomic DNA Mini Kit (Geneaid Biotech Ltd.). A value of N. ×hippocrepicis fell between N. biserrata and (Geneaid, Taipei, Taiwan), and sequenced in an Applied bisection–reconnection (TBR) branch swapping, and chloroplast region atpB-rbcL spacer and two nuclear N. cordifolia (Fig. 6). Biosystems Model 3730 automated sequencer (Applied saving the best tree from each random sequence regions, cycloartenol synthase 1 (CAS1) gene and The two N. ×hippocrepicis populations in the Taipei Biosystems, Carlsbad, CA, USA). All sequences were addition. Bootstrap support values (BS) were calculated glyceraldehydes-3-phosphate dehydrogenase (gapCp) Botanical Garden had different chloroplast atpB-rbcL submitted to GenBank (Table 1) and aligned by BioEdit with 500 replicates. Neighbor-joining analyses were gene, were amplified and sequenced, using primers spacer sequences. The sequences of N. ×hippocrepicis v.7.1.3.0 (Hall, 1999), and the alignment was checked by conducted by calculating Kimura's (1980) 2-parameter plants on P. hanceana were identical with those of N. distance and BS were calculated with 1000 replicates. Table 1 — Information of vouchers in this study. biserrata while the sequences of those on B. capitata Nephrolepis brownii was used as the out group for were identical with N. cordifolia (Fig. 7A). The alleles of Voucher Host tree Host tree GenBank Acession Number phylogenetic analysis. nuclear CAS1 and gapCp genes belong to two different Name Specimen in TAIF* of TPBG** Number atpB.rbcL CAS1 gapCp groups in all sampling N. ×hippocrepicis while the other N. biserrata Y M Huang 1166 Elaeis guineensis Jacq. No. 5167 KF277238 KF277212 RESULTS three species, N. biserrata, N. cordifolia, and N. N. biserrata Y M Huang 1167 Elaeis guineensis Jacq. No. 4455 KF277239 KF277213 brownie, only had one. One group of the N. N. biserrata Y M Huang 1168 Elaeis guineensis Jacq. No. 4454 KF277240 KF277214 KF277227 Morphological comparisons among N. biserrata, N. ×hippocrepicis alleles was clustered with N. biserrata N. biserrata Y M Huang 1174 Phoenix hanceana Naudin No. 4420 KF277241 ×hippocrepicis, and N. cordifolia are summarized in and the other with N. cordifolia (Fig. 7B & C). N. brownii Y M Huang 1172 Phoenix dactylifera L. No. 5201 KF277250 KF277226 KF277237 Table 3 and illustrated in Figs. 2-5. Most characters of N. N. cordifolia Y M Huang 1169 Arenga pinnata (Wurmb) Merr. No. 5117 KF277247 KF277223 KF277236 ×hippocrepicis were intermediate between N. biserrata N. cordifolia Y M Huang 1170 Phoenix dactylifera L. No. 4425 KF277248 KF277224 DISCUSSION N. cordifolia Y M Huang 1171 Phoenix dactylifera L. No. 4425 KF277249 KF277225 and N. cordifolia, except its spores were the largest (if N. ×hippocrepicis Y M Huang 1173 Butia capitata (Mart.)Becc. No. 4428 KF277245 KF277215 KF277228 not aborted). Nephrolepis ×hippocrepicis could be Hybrid Origins of Nephrolepis ×hippocrepicis— KF277219 KF277232 distinguished from N. biserrata and N. cordifolia by According to the NJ trees of chloroplast atpB-rbcL N. ×hippocrepicis Y M Huang 1175 Phoenix hanceana Naudin No. 4420 KF277242 KF277216 KF277229 lanceolate triangulate pinnae (Fig. 2B & 3), reniform spacer sequences and nuclear genes of CAS1 and gapCp KF277220 KF277233 indusia (Fig. 1H), aborted spores (Fig. 4B), and bi- (Fig. 7B & C), Nephrolepis ×hippocrepicis was N. ×hippocrepicis Y M Huang 1176 Phoenix hanceana Naudin No. 4420 KF277243 KF277217 KF277230 colored basal scales with caudate apex (Fig. 5L & P). In originated from the bidirectional hybridization between KF277221 KF277234 addition, the pinnae of N. ×hippocrepicis are closely N. biserrata and N. cordifolia. The chloroplast atpB- N. ×hippocrepicis Y M Huang
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