Flora - Morphology, Distribution, Functional Ecology of Plants
Ontogenesis of trichome-like cavities in Dictamnus dasycarpus
Introduction
Secretory structures are well known to be critical sites for accumulation of secondary plant substances. In case of secretory cavities of Rutaceae, much attention has been dedicated to their original location, the number of initial cells, and their further differentiation. Fohn (1935) studying secretory cavities in Citrus, concluded they were of subprotodermal origin, but did not identify the number of initial cells. According to Bosabalidis and Tsekos (1982a), secretory cavities of Citrus deliciosa originate from a pair of meristematic cells, including an epidermal cell and a subepidermal cell. Bennici and Tani (2004), however, report that the secretory cavities of Citrus sinensis and Citrus limon are both initiated from clusters of meristematic cells under or including the epidermal cells. Rafiei and Rajaei (2007), studying the oil cavities in Citrus aurantifolia, also conclude that the glands originate from both epidermal and subepidermal cells. Rauter (1871) studying Dictamnus, reported that both secretory cavities and trichome-like cavities originate from a lower daughter cell formed from a single protodermal cell that undergoes periclinal division. A similar interpretation was offered by Sprecher (1956) for Ruta secretory cavities. In contrast, Frank (1883) argued that secretory cavities of Dictamnus originate from clusters of meristematic cells located under the protoderm.
Concerning the manner by which secretory cavities form in Rutaceae, some authors concluded that they occur by an autolytic process of the internal cells within the oil gland, as in Citrus (Bosabalidis and Tsekos, 1982b, Esau, 1977, Rafiei and Rajaei, 2007, Turner, 1999). Other authors disagreed, claiming that these glands typically are the result of a schizogenous process (Fahn, 1979, Knight et al., 2001, Knight et al., 2002, Thomson et al., 1976, Turner, 1999). Still other authors interpreted these secretory cavities to be of schizolysigenous origin (Bennici and Tani, 2004, Buvat, 1989, Tschirch and Stock, 1933). For other genera of Rutaceae Heinrich (1969) reported that the formation of oil glands in Ruta graveolens is a typical schizogenous process, but is a lysigenous phenomenon in Poncirus. Liu and Hu (1997) and Liu et al. (1998) studied the formation of the secretory cavities in Zanthoxylum bungeanum and Evodia rutaecarpa and concluded that they are formed schizogenously. In Dictamnus, Rauter (1871) and Martinet (1872) reported that the formation of secretory cavities in Dictamnus fraxinella and Dictamnus albus is a purely lysigenous process of internal cells.
Early work by Bosabalidis and Tsekos (1982b) detected multivesicular lomasomes and autophagic vacuole-like structures during the lysigenous formation of secretory cavities in Citrus deliciosa, which are considered to be events involved in programmed cell death, PCD (Collazo et al., 2006, Hoh et al., 1995, Robinson et al., 1998). Dangl et al. (2000) suggested that the lysigenous formation of glandular cells may be a PCD phenomenon. This has been confirmed by Liu et al. (2010) studying the lysis of pigment gland formation in Gossypium hirsutum, and the lysigenous formation of laticiferous canals in Decaisnea fargesii (Zhou and Liu, 2010). Chen and Wu (2010), having studied schizolysigenous formation of the secretory cavity in Citrus sinensis, also consider it a PCD process. Evidence for gland PCD was also provided for Digitalis purpurea floral nectaries (Gaffal et al., 2007) and Araucaria angustifolia mucilaginous cells (Mastroberti and de Araujo Mariath, 2008).
Although much work has provided morphological, developmental, and ultrastructural details of secretory cavities in Rutaceae, a detailed study is still lacking on the secretory cavities in Dictamnus dasycarpus Turcz. D. dasycarpus is characterized by a trichome-like oil cavity (Turner, 1999), identified by the combination of a non-glandular hair, an oil cavity and a trichome, named trichome-like cavity in our paper. Formation of this special type of secretory structure may occur by PCD. In the present work, light and scanning electron microscopy were used to analyze the ontogeny of this special type of glandular hair, the trichome-like cavity in D. dasycarpus. Transmission electron microscopy was applied to determine the ultrastructural characters during the development of this structure. In conclusion, the aim of this investigation was to clarify not only the origin and the development of these trichome-like cavities but also to ascertain whether or not PCD was involved in their formation.
Section snippets
Materials
Dictamnus dasycarpus was collected from the Qinling Mountains, Shannxi, China (N: 33°59′31″, E: 108°58′13.6″). Different developmental stages of inflorescences were collected from May to June 2010 for this research.
Light microscopy
Samples of ovary, filament and floral axis of Dictamnus dasycarpus were cut into 1 mm3 pieces. Samples were fixed in 0.1 mol L−1 phosphate buffer (pH 7.0) containing 2.5% glutaraldehyde at 4 °C for 4 h. After three 30 min rinses in 0.1 mol L−1 phosphate buffer, pH 7.0, samples were postfixed
Localization and morphology of the trichome-like cavities
Dictamnus dasycarpus is characterized by the presence of one type of trichome-like secretory cavities. In vivo, the trichome-like cavities exhibit features of a spherical- or oblong-shaped head (Fig. 1). They are located on the surfaces of ovary, filaments (Fig. 2A), petals, sepals, the floral axis, laminas and stem (Table 1). The trichome-like cavity share a similar shape with glandular hairs by an obvious multicellular head and a short stalk (Fig. 1, Fig. 2), non-glandular hairs with a single
Origin of the trichome cavity
The trichome-like cavities are derived from a single protodermal cell (Fig. 9A), which is in accordance with development of other types of glandular hairs (Glover, 2000, Liakopoulos et al., 2006, Marks, 1997, Wagner, 1991). Sequentially, the protodermal cell (Fig. 9A) undergoes a periclinal division resulting in two sister cells (Fig. 9B) that ultimately develop into a mature trichome-like cavity (Fig. 9), which is in agreement with Rauter's (1871) description.
Formation of the trichome cavity
Rutaceae are characterized by
Acknowledgments
This study was supported by the National Natural Science Foundation of China (30970170), Shannxi Provincial Department of Education Scientific Research Projects for the Key Disciplines of a Key Laboratory of China (09JS087) and NWU Graduate Innovation and Creativity Funds (10YZZ35).
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Programmed cell death: A mechanism for the lysigenous formation of secretory cavities in leaves of Dictamnus dasycarpus
2014, Plant ScienceCitation Excerpt :However, the degeneration of mitochondria and plastids seems to be an early event, as described in the degradation of the pigment gland in G. hirsutum leaves [12]. The occurrence of multivesicular bodies in the secretory cells of the secretory cavities in D. dasycarpus has been considered typical evidence of autophagy in plant PCD [20,43,44], and a similar phenomenon has also been reported in the lysigenous formation of trichome cavities in D. dasycarpus [6] and in the schizolysigenous formation of secretory cavities in C. sinensis [10]. The formation of secretory cavities and trichome cavities in C. sinensis [11] and D. dasycarpus [6] is now considered a PCD process.
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