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Lilium spp. pollen in China (Liliaceae): Taxonomic and Phylogenetic Implications and Pollen Evolution Related to Environmental Conditions

  • Yun-peng Du,

    Affiliation College of Landscape Architecture, National Engineering Research Center for Flowers, Beijing Forestry University, Beijing, China

  • Chi Wei,

    Affiliation College of Landscape Architecture, National Engineering Research Center for Flowers, Beijing Forestry University, Beijing, China

  • Zhong-xuan Wang,

    Affiliation College of Landscape Architecture, National Engineering Research Center for Flowers, Beijing Forestry University, Beijing, China

  • Shuang Li,

    Affiliation College of Landscape Architecture, National Engineering Research Center for Flowers, Beijing Forestry University, Beijing, China

  • Heng-bin He,

    Affiliation College of Landscape Architecture, National Engineering Research Center for Flowers, Beijing Forestry University, Beijing, China

  • Gui-xia Jia

    gxjia@bjfu.edu.cn

    Affiliation College of Landscape Architecture, National Engineering Research Center for Flowers, Beijing Forestry University, Beijing, China

Lilium spp. pollen in China (Liliaceae): Taxonomic and Phylogenetic Implications and Pollen Evolution Related to Environmental Conditions

  • Yun-peng Du, 
  • Chi Wei, 
  • Zhong-xuan Wang, 
  • Shuang Li, 
  • Heng-bin He, 
  • Gui-xia Jia
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Correction

7 Mar 2014: The PLOS ONE Staff (2014) Correction: Lilium spp. pollen in China (Liliaceae): Taxonomic and Phylogenetic Implications and Pollen Evolution Related to Environmental Conditions. PLOS ONE 9(3): e91543. https://doi.org/10.1371/journal.pone.0091543 View correction

Abstract

Recent molecular and karyologic studies have significantly modified delimitation of Lilium. However, despite the importance of pollen evolution in the genus comprehensive studies with electron microscopy and evaluation of pollen evolution are lacking. Therefore, we studied pollen morphology in a sample of 65 individuals from 37 taxa covering all the sections distributed in the world, using scanning electron microscopy. Our collection of 49 individuals from 21 taxa covering all five sections in China was also included in the database. We found pollen tetrads in L. bakerianum. Based on present and previous studies, our results suggest that pollen from L. formosanum should be classified as a new type, Formosanum. Combined with morphological and molecular evidence, pollen sculpture patterns appear to reflect phylogenetic relationships and are useful for species or subsection delimitation. Based on a comprehensive survey and correlation with potential functional implications, we propose the following hypothesis: evolution of an exine sculpture shows pollen type trends from Martagon → Callose → Concolor → Formosanum. The evolutionary trend regarding pollen sculpture and size could be related to selective pressure to adapt to environmental conditions. Pollen size and shape showed a significantly positive correlation with annual precipitation, and smaller pollen grains appear to adapt better in habitats with extreme conditions. Evolution trends in exine sculpture do not appear to be definitively correlated with pollen size and shape.

Introduction

Approximately 110 to 115 Lilium species are distributed in the cold and temperate regions of the Northern Hemisphere [1], [2], particularly in East Asia, the Himalayas and Hengduan Mountains, North America and Europe. A total of 55 species occur in China [2]. De Jong [3] and Patterson and Givnish [4] consider southwest China and the Himalayas to be the center of origin of this genus.

Classification of this genus has been historically complicated. Several classifications for Lilium have been proposed based on morphological characters. Detailed studies have been performed for East Asia, European and North American Lilium species [5][7]. Based on 13 morphological characters and two germination types, Comber divided this genus into the following seven sections: Martagon Rchb., Pseudolirium Endl. which is limited to North America, Liriotypus Asch. and Graeb. which is distributed across Europe and the Caucasus, Archelirion Baker, Sinomartagon Comber, Leucolirion Wilson, and Daurolirion Comber, representing the most widely accepted taxonomical divisions [8]. Wang and Tang recognized sect. Lophophorum (Bur. et Franch.) Wang et Tang out of sect. Sinomartagon Comber and included campaniform-flowered species [9]. Liang [10] and Haw [11] modified sect. Lophophorum to accommodate the Nomocharis-like Lilium species in sect. Sinomartagon Comber. Chinese species were divided into five sections: Martagon, Archelirion, Sinomartagon, Leucolirion and Lophophorum.

Recently, molecular phylogenetic analyses and chromosome techniques have improved the understanding of several groups within the genus and modified the phylogenetic position of Comber’s classification, such as placement of sect. Daurolirion Comber in sect. Sinomartagon, L. henryi in subsect. Leucolirion 6b, modification of sect. Lophophorum and relationship confirmation in sect. Liriotypus [12][13], [16][21]. Preliminary research found that sect. Sinomartagon, which mainly occurred in China, was complicated and polyphyletic. As indicated by Patterson and Givnish [4], intercontinental dispersal details of the genus Lilium are not yet clear. The division of subsect. Sinomartagon 5c and sect. Lophophorum are controversial and will require further research. Nishikawa et al. [18], [19] suggested that L. henryi be classified into subsect. Leucolirion 6a and that it showed similar morphological features with L. rosthornii, thereby demonstrating that the phylogenetic position of L. rosthornii needs further study.

There are few relevant studies regarding pollen morphology which defines the taxonomic and reflect the evolution of the genus. According to the description within Lilium by Baranova [22] based on the number, shape and arrangement of columellae that form the muri, there are three morphological types of pollen: (1) Martagon (muri formed by rectangular columellae); (2) Callose (muri formed by rounded columellae); and (3) Concolor (muri formed by separated rounded and polygonal columellae). Previous studies found that most Lilium species have single pollen grains. However, pollen tetrads were found in L. sempervivoideum H. Lév. and L. amoenum E. H. Wilson ex Sealy, and the size and sculptural elements confirmed the taxa as two subspecies in L. sempervivoideum [23]. The pollen morphology of L. lophophorum (Bur. et Franch.) Franch., L. henrici Franch., L. souliei (Franch.) Sealy and L. nanum Klotz. et Garcke supported placement in Lilium, which differs from Nomocharis in apture and sculptural elements, and showed an evolutionary aperture trend from monocolpate to porate [24]. Muratović et al. [25] showed that two related European species, L. bosniacum and L. carniolicum, share similar pollen morphology. In addition, pollen morphology of some Chinese species under scanning electron microscopy (SEM), including 9 species described by Li and Qin [26], 10 species and 3 cultivars by Zhang et al. [27], and 12 species and 6 cultivars by Wu et al. [28], could provide taxonomic implications within Lilium:pollen has not only the commonness of genus, but also the specificity of single species. Interspecific pollen size and morphological characteristics has some difference, which has a certain reference value for the classification of Lilium. For example, there are differences in pollen size among L. cernnum, L. lanciflium and L. pumilum. Also there are significant differences in pollen ornamentation and morphology between L. leucanthum and its variety L. leucanthum var. centifolium from Qinling Mountains. Results obtained by Wang et al. [29] and Liu [30] indicate that pollen size parameters of L. pumilum and L. concolor from different provenances showed different degrees of variation. Determining whether this is a universal phenomenon in other species or if