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Histological and Cytological Characterization of Anther and Appendage Development in Asian Lotus (Nelumbo Nucifera Gaertn.)

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Histological and Cytological Characterization of Anther and Appendage Development in Asian Lotus (Nelumbo Nucifera Gaertn.) International Journal of Molecular Sciences Article Histological and Cytological Characterization of Anther and Appendage Development in Asian Lotus (Nelumbo nucifera Gaertn.) Dasheng Zhang 1,2 , Qing Chen 3, Qingqing Liu 1,2, Fengluan Liu 1,2, Lijie Cui 4, Wen Shao 1,2, Shaohua Wu 3, Jie Xu 5,* and Daike Tian 1,2,* 1 Shanghai Chenshan Plant Science Research Center of Chinese Academy of Sciences, Shanghai Chenshan Botanical Garden, Shanghai 201602, China; [email protected] (D.Z.); [email protected] (Q.L.); [email protected] (F.L.); [email protected] (W.S.) 2 Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai 201602, China 3 College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, China; [email protected] (Q.C.); [email protected] (S.W.) 4 Development Center of Plant Germplasm Resources, College of Life Science, Shanghai Normal University, Shanghai 200234, China; [email protected] 5 School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China * Correspondence: [email protected] (J.X.); [email protected] (D.T.); Tel./Fax: +86-21-5776-2652 (D.T.) Received: 10 January 2019; Accepted: 22 February 2019; Published: 26 February 2019 Abstract: The lotus (Nelumbo Adans.) is a perennial aquatic plant with important value in horticulture, medicine, food, religion, and culture. It is rich in germplasm and more than 2000 cultivars have been cultivated through hybridization and natural selection. Microsporogenesis and male gametogenesis in the anther are important for hybridization in flowering plants. However, little is known about the cytological events, especially related to the stamen, during the reproduction of the lotus. To better understand the mechanism controlling the male reproductive development of the lotus, we investigated the flower structure of the Asian lotus (N. nucifera). The cytological analysis of anther morphogenesis showed both the common and specialized cytological events as well as the formation of mature pollen grains via meiosis and mitosis during lotus anther development. Intriguingly, an anatomical difference in anther appendage structures was observed between the Asian lotus and the American lotus (N. lutea). To facilitate future study on lotus male reproduction, we categorized pollen development into 11 stages according to the characterized cytological events. This discovery expands our knowledge on the pollen and appendage development of the lotus as well as improving the understanding of the species differentiation of N. nucifera and N. lutea. Keywords: Asian lotus; anther; pollen; microspore; anther appendage 1. Introduction The Lotus (Nelumbo) is a perennial aquatic plant with ornamental, medicinal, edible and cultural importance [1–3]. It has only two living species: the American lotus (N. lutea Willd.) and the Asian lotus (N. nucifera Gaertn.) [4]. The American lotus has light-yellow colored flowers only and is distributed in North America and the northern regions of South America, while the Asian lotus has a richer diversity in morphology at the population level with wider distribution ranges (Asia, north Oceania and south Russia). The Asian lotus, also called the sacred lotus, has been domesticated in Asia for about 7000 years and is cultivated as a major crop where its rhizomes and seeds are used as vegetables particularly in China and Southeast Asian countries [5]. It is the national flower of India and one of the traditional flowers of China and Vietnam. Furthermore, the Asian lotus plays a significant role in Int. J. Mol. Sci. 2019, 20, 1015; doi:10.3390/ijms20051015 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 1015 2 of 15 religious and cultural activities in many Asian countries [6]. A long history of artificial hybridization and selection has generated more than 2000 lotus cultivars that differ in plant size, flower color, flower form, flower shape and tepal number [7]. As a famous ornamental plant, lotus is widely planted in water gardens, ponds, lakes and rivers to beautify and purify the environment. It also produces a series of secondary metabolites with important medicinal functions, including flavonoids, alkaloids, triterpenoids, steroids, glycosides and polyphenols from the leaves, flowers, seedpods and seeds [8]. The lotus is a long-day plant. Its flowers open in the early morning and the life span of one single flower usually does not exceed four days. The lotus flower is solitary and hermaphrodite, and is composed of the perianth, androecium, gyneceum, receptacle, and peduncle (Figure1a). The calyx is the outermost whorl of the perianth, usually consisting of four sepals that are green, thick, tenacious, and similar to tetals in structure, except that they fall earlier. One flower contains twenty or more tepals that vary widely in size, shape, number and color from population to population and from cultivar to cultivar, which results in a diverse floral morphology. Usually, a lotus flower is self- incompatible because the multiple stigmas of a receptacle mature ahead of the stamens in the same flower [6]. Up to now, the majority ofInt. lotuses J. Mol. Sci. 2019 have, 19, x stamens with a few exceptions such as ‘Guangyue3 of 16 Lou’, ‘Miracle’, etc. and the three thousand-petalled-typelotus cultivars, while the appendage Asian of lotusthe American cultivars lotus is bright ‘Qian yellow Ban’, with a ‘Yiliangsickle-like shape. Qianban’, and ‘Zhizun The appendage only had two layers: the epidermis and hypodermis parenchyma (Figure 1h). The Qianban’ where thesubepidermal stamens parenchyma are fully also transformed contained a high density into of tepals. granules that could be deeply stained with toluidine blue (Figure 1h). Figure 1. Development and transverse sections of the anther and appendage of N. nucifera ‘Honghu Figure 1. DevelopmentHong’. and(a) Scheme transverse of the flower sections morphology ofand theits generative anther structures and appendageof ‘Honghu Hong’. of (b) N. nucifera ‘Honghu a Longitudinal section at the stamen primordium differentiation stage, the arrows indicate the stamen Hong’. ( ) Schemeprimordium. of the ( flowerc) Longitudinal morphology section at the pistil and primordium its generative differentiation stage, structures the arrows of ‘Honghu Hong’. (b) Longitudinal sectionindicate the at carpel. the stamen(d–f) Anther primordiumand anther appendagesat differentiation different developmental stage, stages, the the arrows indicate the arrows indicate the anthers and the appendages respectivly. (g) Transverse section of the anther at stamen primordium.the (c mature) Longitudinal pollen stage. (h) sectionTransverse section at the of pistilthe anther primordium appendage at the young differentiation microspore stage, the arrows indicate the carpel. (stage.d–f )An, Anther anther; Ap, and appendage; anther Ca, carpel; appendagesat E, epidermis; En, endothecium; different F, developmental filament; M, middle stages, the arrows layer; MP, mature pollen; OB, osmiophilic body; P, parenchyma; Re, receptacle; St, stamen; T, indicate the antherstapetum; and the Te, Tepal; appendages V, vascular elements. respectivly. (b,c) Bar = 100 (g μm;) Transverse (d,e) Bar = 0.3 mm; section (f) Bar = 10 ofmm; the (g,h) anther at the mature Bar = 10 μm. pollen stage. (h) Transverse section of the anther appendage at the young microspore stage. An, anther; Ap, appendage; Ca, carpel; E, epidermis; En, endothecium; F, filament; M, middle layer; MP, mature pollen; OB, osmiophilic body; P, parenchyma; Re, receptacle; St, stamen; T, tapetum; Te, Tepal; V, vascular elements. (b,c) Bar = 100 µm; (d,e) Bar = 0.3 mm; (f) Bar = 10 mm; (g,h) Bar = 10 µm. Int. J. Mol. Sci. 2019, 20, 1015 3 of 15 The pollen development of the American lotus has been described and can be divided into five different stages [9]. However, the development of the pollen and anther of Asian lotus, a more economically important species, still remains unknown. Due to a long history of geographical isolation and evolution, large differences exist in the morphology between these two species, especially in the stamen, anther pigment and appendage shape. Although both the American lotus and Asian lotus can easily hybridize with each other to produce fertile seeds, the reproductive ability of their hybrid offspring has largely declined [4,10]. To better understand the process and characteristics of the male reproductive development of the Asian lotus in comparison with previous reports on the American lotus, we investigated the flower and anther structure, anther morphogenesis, and pollen formation of a wild type Asian lotus. Exploring the developmental events in the lotus plant, particularly into its reproductive mechanism, will improve our knowledge on species identity and differentiation. 2. Results 2.1. The Morphologic Characteristics of the Anther and Its Appendage in N. nucifera In the underwater flower bud, the stamens originated from the stamen primordium, which came from the lateral edges of the growth cone inside the tepal primordium (Figure1b) and appeared around the base of the receptacle. Shortly after the formation of the stamen primordium, the pistil primordium formed at the top central domain of the growth cone. Meanwhile, the receptacle gradually developed and elevated incrementally (Figure1c). Before the anther sac was initiated, the appendage could obviously be observed at the top of the stamen (Figure1d). Along with stamen development, the anther and appendage gradually elongated and reached 2.5–4.5 cm at full
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