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A New Classification of Marginal Resin Ducts Improves Understanding of Hard Pine (Pinaceae) Diversity in Taiwan

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A New Classification of Marginal Resin Ducts Improves Understanding of Hard Pine (Pinaceae) Diversity in Taiwan Flora 209 (2014) 414–425 Contents lists available at ScienceDirect Flora journal homepage: www.elsevier.com/locate/flora A new classification of marginal resin ducts improves understanding of hard pine (Pinaceae) diversity in Taiwan a,b, a,c d d Chiou-Rong Sheue *, Hsiu-Chin Chang , Yuen-Po Yang , Ho-Yih Liu , a,b,e c Peter Chesson , Fu-Hsiung Hsu a Department of Life Sciences, National Chung Hsing University, 250 Kuo Kuang Road., Taichung 402, Taiwan b Center of Global Change Biology, National Chung Hsing University, 250, Kuo Kuang Road, Taichung 402, Taiwan c Department of Biological Resources, National Chiayi University, 300 Syuefu Road., Chiayi City 600, Taiwan d Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung 804, Taiwan e Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA A R T I C L E I N F O A B S T R A C T Article history: Resin ducts provide important characters for classifying the Pinaceae. Here we study Pinus massoniana Received 18 November 2013 and P. taiwanensis and show that the generally-used term marginal (=external) resin duct, applied to Accepted 5 June 2014 ducts in needle leaves, needs to be further differentiated into marginal (strongly attaching to the dermal Edited by R. Lösch tissue, and lacking the complete ring structure formed by the sheath cells) and submarginal ducts Available online 28 June 2014 (adjacent to hypodermal cells, with a complete ring structure formed by the sheath cells). On this basis P. massoniana and P. taiwanensis, which are nearly indistinguishable based on external morphology, are Keywords: clearly differentiated. Their similar morphology has led to a long standing debate on where P. massoniana Hard pines occurs in Taiwan. Based on this new classification of resin ducts, we examined old herbarium specimens Pinus massoniana previously identified as P. massoniana, surveyed current hard pines in Taiwan, and checked historical Pinus taiwanensis Submarginal resin duct documents. Needle leaves of these two taxa were studied and compared with the material of P. Huoyansan massoniana from mainland China as a reference. Pinus massoniana shows almost exclusively marginal Junjianyan resin ducts, with extremely rare changes along the length of the duct to submarginal positions. In contrast, P. taiwanensis shows a mixture of medial, submarginal, septal, and rarely endonal ducts, with occasional changes of the duct between various types. Re-identification of specimens showed that only 5 specimens are possible native P. massoniana collected from northern Taiwan and the others are all P. taiwanensis. The hard pine of Junjianyan is unexpectedly found to be the only currently known P. massoniana in Taiwan, which is likely a relic of historical afforestation. The hard pine from Huoyansan and the Coastal Range, which is widely accepted as P. massoniana, is not this species. In addition to the taxonomic value of the new definition applied to these two studied taxa, we expect that this approach can generally be applied distinguishing the respective characters in the genus Pinus and in other conifers. ã 2014 Elsevier GmbH. All rights reserved. Introduction species, Harlow (1931) stated that the relative position of the ducts in the needle may be used as an aid, but that the number of resin In conifers, resin ducts provide important characters for ducts in the needles is of no particular importance except for a few classification, especially for distinguishing Pinus L. species species that normally only have two or three ducts. Napp-Zinn (Boratynska and Bobowicz, 2001; Fu et al., 1999; Knopf et al., (1966) classified four types of resin ducts of the genus Pinus 2012; Li and Keng, 1994; Law et al., 1978; Richardson, 1998; Wu according to their location in the leaf: (1) ducts in contact with the and Hu, 1997). Resin ducts have also been used to differentiate hypodermis, viz. marginal (=external); (2) ducts surrounded by Pinus hybrids (Kormutak et al., 1993). For the identification of pine chlorenchyma, viz. medial; (3) ducts in contact with the bundle sheath (endodermis) in the chlorenchyma, viz. endonal; and (4) ducts inside the bundle sheath. Biswas and Johri (1997) added another type of resin duct in the mesophyll, viz. septal, referring to * Corresponding author at: National Chung Hsing University, Department of Life the duct connected to both endodermis and hypodermis. In this Sciences, 250, Kuo Kuang Road, Taichung 402, Taiwan. Tel.: +886 4 22857395; fax: study, we reexamine the marginal resin duct type and show that it +886 4 22857395. E-mail addresses: [email protected], [email protected] (C.-R. Sheue). can be divided usefully into two types, which we then use to solve a http://dx.doi.org/10.1016/j.flora.2014.06.007 0367-2530/ã 2014 Elsevier GmbH. All rights reserved. C.-R. Sheue et al. / Flora 209 (2014) 414–425 415 long standing mystery on the taxonomy and distribution of hard Pinus massoniana was first described by Lambert (1803). He pines in Taiwan. stated “the specimen represented in this plate (t. 12) is in the According to the Flora of Taiwan (Li and Keng, 1994), four Banksian Herbarium, having been brought by Mr. Francis Masson species of pines are native to Taiwan, P. armandii Franch. var. from the Cape of Good Hope, where it was raised by seeds which mastersiana Hayata, P. morrisonicola Hayata, P. massoniana Lamb. had been sent from China....I have not been able to obtain any fruit and P. taiwanensis Hayata. The former two species are soft pines of P. masoniana, nor any further information”. Thus, the plate only (subgenus Strobus) with one vascular trace inside a vascular showed young shoots, needle leaves and male catkins (Lambert, bundle, and the latter two species are hard pines (subgenus Pinus) 1803). However, it seems strange that it was given the common with two vascular traces inside a vascular bundle. Of these native name ‘Indian pine' (Lambert, 1803). Since the type specimen of this pines, P. taiwanensis has the widest distribution in Taiwan (Li and taxon can no longer be found in the BM herbarium, t. 12 (in Keng, 1975), ranging from altitudes of 680 m to 3100 m in the Lambert 1803) was selected as an iconotype (Farjon, 2010). Central Range (Sheue et al., 2003). Since P. hwangshanensis Hsia in Pinus massoniana, with three varieties reported in mainland China was proved to be a synonym of P. taiwanensis (Fu et al.,1999), China (Fu et al.,1999), is regarded a species widely distributed from its distribution extends to central and eastern China. southwestern and eastern China and Taiwan. According to Li and Recently, a third hard pine, P. fragilissima Businský, was Keng (1994) it was mostly found in Taiwan in northern parts and described from southern Taiwan (Businský, 2003). This new hard eastern coastal hills. The so-called P. massoniana, growing in pine was distinguished by a sparse crown and long cones with lowland central Taiwan (Huoyansan) and the Coastal Range is in often flat apophyses, but otherwise has very similar morphology to morphology extremely similar to the other Taiwan’s native hard P. taiwanensis. Thus, we follow Farjon (2010) in treating P. pine P. taiwanensis. These two hard pines are often identified by fragilissima as a variety of P. taiwanensis. their collection localities rather than by recognizable and reliable Table 1 Results of re-identification using resin duct traits of 34 herbarium specimens previously identified as P. massoniana. Only nine specimens (no. 1–7, 9–10) are confirmed as P. massoniana with only marginal resin ducts. No. Location (current place) Herb. code/ Collector, notes on specimen Year Resin duct no Reidentification no. (type) f 1 Sanjiaoyong (Sanxia, Taipei) TAIF2775 Mori, cultivated 1910 6 (6Mar) P. massoniana a 2 Taihoku (Taipei) K Price 341 , open hillside, Siuleny (Sintian) 1912 5 (5Mar) P. massoniana a f 3 Taihoku (Taipei) K Wilson 10,136 , cultivated and also wild around 1918 5 (5Mar) P. massoniana Herinbi a 4 Taihoku (Taipei) K Wilson 10,299 , in all probability wild and 1918 9 (9Mar) P. massoniana indigenous f 5 Casan (Taipei) TAIF2782 Sasaki, cultivated 1923 6 (6Mar) P. massoniana 6 Taihoku (Taipei) TAI183485 Suzuki 1935 4 (4Mar) P. massoniana 7 Wantan, Sintian (Taipei) TAI013104 Shimizu 3328 1936 4 (4Mar) P. massoniana b 8 Taitung (Coastal Range) TAI013112 Yamamoto & Mori YM161 1937 1 (1Mar)? – f 9 Nanfengsan (Kaoshiung) PPI00616 RC Zhang 05, cultivated 1968 7 (7Mar) P. massoniana f 10 Taichung Park PPI00611 RC Zhang 51, cultivated 1969 8 (8Mar) P. massoniana c 11 Yangmingshan (Taipei) PPI31419 MY Ji [–] 2 (2Med) P. luchuensis 12 Nanris, Taito (Nanliao, Taitung, Coastal Range) TAIF2777 Kawakami & Nakahara, not cultivated 1906 4 (2Med 2Mar) P. taiwanensis a d 13 N. Horisha (Buli, Nantou) K Price 714 , river bank, Niaibam valley 1912 2 (2Med) P. taiwanensis f e 14 Casan (Taipei) TAIF2780 S. Sasaki, cultivated 1918 6 (6Med) P. thunbergii 15 Peinanda Xi, Taitung (Coastal Range) TAIF2778 S. Sasaki, not cultivated 1920 3 (2Med 1Mar) P. taiwanensis 16 Casan (Taipei) TAI013102 S. Suzuki 1929 3 (3Med) P. taiwanensis 17 Taitung (Coastal Range) TAI114770 Yamamoto & Mori 1937 6 (4Med 2SM) P. taiwanensis 18 Taipei Botanic Garden TAIF166314 LM Zang 1949 3 (2Med 1SM) P. taiwanensis 19 Anmashan TAI196536 TY Yang 1984 3 (2Med 1SM) P. taiwanensis 20 Dabajianshan TNM G0857 CS Yarng 1986 4 (3Med 1SM) P. taiwanensis f c 21 National Chung Hsing University, Taichung PPI027272 NC Bai cultivated 1987 3 (3Med) P. luchuensis 22 Huoyansan TAI217224 KC Yang 1988 4 (1Med 2Mar P. taiwanensis 1SM) 23 Guangao, Nantou TNM G065 WB Lu 1989 7 (7Med) P. taiwanensis 24 Xinkangshan, Hualian (Coastal Range) TNM G0854 TY Yang et al. 1989 4 (3Med 1Sep) P.
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  • Molecular Mechanism of Lateral Bud Differentiation of Pinus Massoniana
    www.nature.com/scientificreports OPEN Molecular mechanism of lateral bud diferentiation of Pinus massoniana based on high‑throughput sequencing Hu Chen1,2,3,4, Jianhui Tan1,3, Xingxing Liang1, Shengsen Tang1,2, Jie Jia1,3,4 & Zhangqi Yang1,2,3,4* Knot‑free timber cultivation is an important goal of forest breeding, and lateral shoots afect yield and stem shape of tree. The purpose of this study was to analyze the molecular mechanism of lateral bud development by removing the apical dominance of Pinus massoniana young seedlings through transcriptome sequencing and identify key genes involved in lateral bud development. We analyzed hormone contents and transcriptome data for removal of apical dominant of lateral buds as well as apical and lateral buds of normal development ones. Data were analyzed using an comprehensive approach of pathway‑ and gene‑set enrichment analysis, Mapman visualization tool, and gene expression analysis. Our results showed that the contents of auxin (IAA), Zea and strigolactone (SL) in lateral buds signifcantly increased after removal of apical dominance, while abscisic acid (ABA) decreased. Gibberellin (GA) metabolism, cytokinin (CK), jasmonic acid, zeatin pathway‑related genes positively regulated lateral bud development, ABA metabolism‑related genes basically negatively regulated lateral bud diferentiation, auxin, ethylene, SLs were positive and negative regulation, while only A small number of genes of SA and BRASSINOSTEROID, such as TGA and TCH4, were involved in lateral bud development. In addition, it was speculated that transcription factors such as WRKY, TCP, MYB, HSP, AuxIAA, and AP2 played important roles in the development of lateral buds. In summary, our results provided a better understanding of lateral bud diferentiation and lateral shoot formation of P.
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