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Pollen Morphology of the Platycodonoid Group (Campanulaceae S

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Pollen Morphology of the Platycodonoid Group (Campanulaceae S Journal of Integrative Plant Biology 2012, 54 (10): 773–789 Research Article Pollen Morphology of the Platycodonoid Group (Campanulaceae s. str.) and Its Systematic Implications F HONG De-Yuan∗ and PAN Kai-Yu State Key Laboratory of Systematic & Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, China ∗ Corresponding author Tel: +86 10 6283 6096; Fax: +86 10 6259 0843; E-mail: [email protected] F Articles can be viewed online without a subscription. Available online on 11 September 2012 at www.jipb.net and www.wileyonlinelibrary.com/journal/jipb doi: 10.1111/j.1744-7909.2012.01164.x Abstract In this study, we examined the pollen morphology of the platycodonoid group in Campanulaceae s. str. using a scanning electronic microscope. We used pollen grains of 25 accessions representing 24 species of the Codonopsis complex (including Campanumoea, Cyclocodon, Leptocodon, and all three subgenera of Codonopsis), which is extremely controversial among authors for taxonomic treatment. Pollen morphology of all the other genera in the group observed by previous authors is taken into account in our discussion. A total of nine pollen types with two subtypes in the group were recognized and named for the first time. Molecular and morphological data imply that each pollen type corresponds to a natural group at generic level, and thus the mergence of Leptocodon with Codonopsis and the restoration of Cyclocodon as a separate genus are justifiable, and Codonopsis subg. Pseudocodonopsis, subg. Obconicicapsula, and two species of Codonopsis subg. Codonopsis (C. purpurea and C. chimiliensis) may be better classified as three independent genera separate from the core Codonopsis. Keywords: Campanulaceae s. str.; platycodonoid group; Codonopsis complex; pollen morphology; pollen type; taxonomy; systematics. Hong DY, Pan KY (2012) Pollen morphology of the platycodonoid group (campanulaceae s. str.) and its systematic implications. J. Integr. Plant Biol. 54(10), 773–789. Introduction tell us that the Campanulaceae s. str. consists of three ma- jor monophyletic groups: campanuloids, platycodonoids and The Campanulaceae s. str. is a well-established family (Cosner wahlenbergioids. et al. 1994; Gustafsson and Bremer 1995; Gustafsson et al. On the other hand, the three studies mentioned above also 1996; Lundberg and Bremer 2003). However, the subdivisions indicate that the phylogenetic relationships within each of the of the family and the relationships of genera were unclear three major groups are far from well established. They all clearly before this century. Recent studies on molecular systematics show that Campanula and Wahlenbergia each is a polyphyletic of the Campanulaceae s. str. have resulted in more insight genus in the traditional sense. Eddie et al. (2003) and Haberle into infrafamilial phylogenetic relationships. Eddie et al. (2003) et al. (2009) have convinced us that the genus Codonopsis analyzed the phylogenetic relationships of the family using ITS Wall. in the platycodonoid group is also polyphyletic. sequences of nuclear ribosomal DNA. Borsch et al. (2009) Pollen morphology has been used as a very powerful conducted analyses of phylogenetic relationships using DNA tool to consider systematics of the Campanulaceae. Erdtman sequences of the chloroplast gene petD. In the same year, (1952) conducted a rather extensive survey on pollen of the Haberle et al. (2009) used DNA sequences of three chloroplast Campanulaceae s. lat. and pointed out that Schonland’s¨ “sub- genes, atpB, matK, and rbcL, to analyze the phylogenetic tribes of Campanulaceae – Campanuloideae do not seem to relationships of the Campanulaceae s. str. These three studies be homogeneous.” For example, Schonland’s¨ Platycodinae is C 2012 Institute of Botany, Chinese Academy of Sciences 774 Journal of Integrative Plant Biology Vol. 54 No. 10 2012 amixtureofPlatycodon with pollen having elongate apertures, Pseudocodonopsis have pollen morphology distinctly different and Microcodon and Musschia with porate pollen. Thulin (1975) from that of most species of subg. Codonopsis. If the other further emphasized the significance of pollen morphology in species of subg. Pseudocodonopsis are the same as these taxonomy, stating that for the arrangement of genera in the three species in terms of pollen morphology, one could question Campanulaceae s. str., the first consideration should be pollen the justification for keeping them in Codonopsis, considering morphology. Morris and Lammers’ (1997) work is the most the sharp differences in external morphology between two extensive on the Codonopsis complex. They observed pollen subgenera. morphology of 23 accessions representing 17 species, and Consequently, we think that it is worthwhile to conduct took into account the results of previous investigators. As a more extensive observations on pollen morphology of the result, they recognized four pollen types, and revealed their platycodonoid group, and to conduct a comprehensive analysis close relationships with taxonomy. because of the diverse pollen morphology of the group and the Molecular phylogenetic results clearly show that there is controversial views on taxonomy among authors as mentioned a major dichotomy between the colpate/colporate pollen al- above. liance (platycodonoid taxa) and the porate pollen alliance Since previous authors have already conducted extensive (wahlenbergioid and campanuloid taxa). The wahlenbergioid observations on the pollen morphology of Canarina (Erdtman and campanulioid groups both have porate pollen, but the 1952; Dunbar 1975a; Avetisjan 1986), Cyananthus (Erdtman former possesses capsules dehiscent by apical valves (loculi- 1952; Dunbar 1975a; Shrestha and Tarasevich 1992), Os- cidal), while capsules of the latter are dehiscent by lateral pores trowskia (Erdtman 1952; Dunbar 1975a; Avetisjan 1986), Platy- (poricidal). codon (Dunbar 1975a; Avetisjan 1986;), and Echinocodon In the platycodonoid group, the circumscription of Codonop- (Hong 1984), we intend to pay special attention to Campanu- sis has been controversial among authors. Moeliono and Tuyn moea, Codonopsis, Cyclocodon and Leptocodon. Morris and (1960) merged Campanumoea s. lat. (including the genus Cy- Lammers’ (1997) observation strongly implies that pollen in clocodon)withCodonopsis. This circumscription of Codonopsis Codonopsis s. lat. (Shen and Hong 1983) is polytypical, and was accepted by Grey-Wilson (1990) and Lammers (1992). Eddie et al. (2003) and Haberle et al. (2009) use molecular data Grey-Wilson (1990) merged Leptocodon into Codonopsis, and to show that the taxon is polyphyletic. Therefore, we greatly this action was followed by Lammers (1999). Thus, Lammers expanded sampling in Codonopsis, including the type species adopted the broadest concept of Codonopsis, accommodating C. viridis. all four genera mentioned above. However, Hong (1983) recog- nized Campanumoea s. lat. (including sect. Cyclocodon) and Leptocodon each as an independent genus. Hong and Pan Results and Discussion (1998) restored Cyclocodon at generic rank based on data from the pollen and seed-coat, which are distinct from those The results of our observations are presented in Figures 1–6 in Codonopsis and Campanumoea sect. Campanumoea.In and Table 1, where previous observations are also provided “Flora of China” (Hong et al. 2011: p. 505), readers can find to give adequate information for discussion purposes. From controversial views on how to treat the group under discus- Table 1, the pollen of Platycodon is 5–6-colporate with medium- sion. Hong recognized four genera, but the two co-authors, high sexine spinules (1.5 µm), and is thus a distinct type Lammers and Klein, stated their belief that Campanumoea and of pollen called the Platycodon Type. The pollen of genus Leptocodon should be merged into Codonopsis. Another issue Ostrowskia is very special, and is 6–7-colpate with large- involved in the taxonomic treatment of the group under study verrucose sexine. It is deserving of being named an indepen- is whether Codonopsis s. str. is monophyletic or polyphyletic. dent pollen type, the Ostrowskia Type. The genus Echinocodon According to the current designation (Shen and Hong 1983; D. Y. Hong possesses 4–5-colpate pollen with short colpi Hong in Hong et al. 2011), Codonopsis consists of three (colpus length/polar axis length =∼ 0.36) and basally divided subgenera, subg. Codonopsis, subg. Obconicicapsula D. Y. sexine spinules. Such pollen cannot be assigned to any Hong (1980) and subg. Pseudocodonopsis Kom. (1908). Two of the above-mentioned types, and thus is here designated molecular trees, one based on the ITS sequence of nuclear as the Echinocodon Type. According to Dunbar (1975a) ribosomal DNA (Eddie et al. 2003), and the other based on and Shrestha & Tarasevich (1992), the pollen of the genus three cpDNA genes, atpB, matK and rbcL(Haberle et al. Cyananthus is 6–9-colpate with long colpi, verrucose colpus 2009), indicate that the only species of subg. Obconicicapsula, membrane, and verrucose sexine (Table 1). It should also Codonopsis dicentrifolia (C. B. Clarke) W. W. Smith, does be designated an independent pollen type, the Cyananthus not join the Codonopsis clade, but instead forms a clade Type. with Cyananthus lobatus. Based on their observations, Morris Based on previous observations (Erdtman 1952; Dunbar and Lammers (1997) revealed that three species in subg. 1975a; Avetisjan 1967, 1986; Hong 1984; Morris and Lammers Pollen Morphology of the Platycodonoid Group 775 Figure 1. SEM photographs
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