Elsevier

Plant Science

Volume 225, August 2014, Pages 147-160
Plant Science

Programmed cell death: A mechanism for the lysigenous formation of secretory cavities in leaves of Dictamnus dasycarpus

https://doi.org/10.1016/j.plantsci.2014.06.007Get rights and content

Highlights

  • One cell initiation and lysigenous oil cavities may be common in Dictamnus.

  • Lysigenous formation of the secretory cavities in D. dasycarpus is a PCD process.

  • Clusters of cells from a protoepidermal cell undergo different cell death fates.

  • Degradation products in the oil cavities may be used for the synthesis of essential oils.

  • A new description for different types of secretory cavities is determined.

Abstract

The formation of secretory cavities in Rutaceae has been the subject of great interest. In this study, cytological events that are involved in the lysigenous formation of the secretory cavities in the leaves of Dictamnus dasycarpus are characterized by an interesting pattern of programmed cell death (PCD). During the developmental process, clusters of cells from a single protoepidermal cell embark on different trajectories and undergo different cell death fates: the cell walls of the secretory cells have characteristics of thinning or complete breakdown, while the sheath cells present a predominantly thick-walled feature. A DAPI assay shows deformed nuclei that are further confirmed to be TUNEL-positive. Gel electrophoresis indicates that DNA cleavage is random and does not result in ladder-like DNA fragmentation. Ultrastructurally, several remarkable features of PCD have been determined, such as misshapen nuclei with condensed chromatin and a significantly diffused membrane, degenerated mitochondria and plastids with disturbed membrane systems, multivesicular bodies, plastolysomes, vacuole disruption and lysis of the center secretory cell. Cytological evidence and Nile red stains exhibit abundant essential oils accumulated in degenerated outer secretory cells after the dissolution of the center secretory cell. In addition, explanations of taxonomic importance and the relationship between PCD and oil droplet accumulation in the secretory cavities are also discussed.

Introduction

Much research on plant glands has been based on their secretions and structural importance. In Rutaceae, the secretory cavity or oil cavity formation has drawn great interest for more than a century, and these cavities have generally been known to form via one or more of three methods: lysigenous, schizogenous or schizolysigenous processes of the glandular cells [1]. The description of the lysigenous formation of secretory cavities in Rutaceae is now discussed and widely accepted in most of the literature [2], [3], [4], [5], [6] despite the fact that the concept of the lysigenous developmental process has always been disputed in this field [1], and studies supporting lysigenous formation have been objected to by schizogenous [7], [8], [9] or schizolysigenous processes in Citrus sinensis and Citrus limon or related species [1], [10], [11].

Despite extensive study, it is not difficult to determine that this controversy stems from the focus on whether the glandular cell walls undergo lysis or resorption, which has been considered a process of programmed cell death (PCD) in the lysigenous formation of trichome cavities in Dictamnus dasycarpus Turcz. [6], in the schizolysigenous formation of secretory cavities in C. sinensis [11], or in the formation of related glands in other genera, including the lysis of the pigment gland in Gossypium hirsutum [12] and lysigenous formation of laticiferous canals in Decaisnea fargesii [13], and detailed evidence in cytology is also provided.

Although degeneration features in the glandular structures of plants have been reported in previous studies [1], [14], studies on PCD of secretory structures at the cytological and molecular levels have been initiated with greater vigor only in very recent years [11], [12], [13], [15], [16], [17].

In Dictamnus, the formation of secretory cavities in D. albus and D. fraxinella was reported by Rauter [18] and Martinet [19], indicating a process coupled with the lysis of glandular cells. D. dasycarpus is characterized by the presence of a trichome cavity, a secretory cavity, capitate glandular hair, and non-glandular hair. Interestingly, previous studies have investigated intermediate secretory structures, termed trichome cavities, which are characterized by a combination of lysigenous secretory cavities, capitate glandular hairs, and non-glandular hairs [6]. A series of degeneration characters were detected during the formation of trichome cavities in D. dasycarpus, suggesting a typical PCD phenomenon coupled with patterns of autophagy and autolysis [6], [12], [15], [20]. For the homologous structures, the formation of secretory cavities in D. dasycarpus may also be PCD. To date, little research has been conducted on the formation of secretory cavities in D. dasycarpus, and no research has been conducted on the degeneration characters specifically within this developmentally regulated PCD from cyto-morphological points of view.

This study elucidates new elements of the lysigenous formation of secretory cavities in D. dasycarpus. The primary objective of this research was to clarify the sequence of changes during the development of secretory cavities and to provide new evidence for identifying the type of cell death that is involved in the lysigenous formation of the plant gland.

Section snippets

Plant materials

All of the Dictamnus dasycarpus plants that were used for experimental purposes were collected from the Qinling Mountains, Shannxi, China (33°59′31″ N, 108°58′13.6″ E). Four different developmental stages of leaves were collected from May to July 2013 for this research.

Light microscopy

Tissue samples approximately 1–2 mm2 were excised from the four developmental stages and fixed in 2% glutaraldehyde in 0.1 mol L−1 phosphate buffer at 4 °C, pH 7.0. After 4 h of incubation, the samples were rinsed three times in 0.1 mol

Ontogenesis of the secretory cavities

The development of the secretory cavities was traced through four developmental stages: stage 1, initial stage; stage 2, secretory and sheath cell differentiation stage; stage 3, degeneration of secretory cell stage; and stage 4, maturation stage.

Origin and differentiation

Historically, in Rutaceae, the development of secretory cavities has been thought to originate from subprotodermal cells as in Citrus [25], epidermal and subepidermal cells as in C. deliciosa and C. aurantifolia [4], [5], meristematic cells under or including the epidermal cells as in C. limon [10], and a single protoepidermal cell in Ruta [26]. In Dictamnus, the description by Rauter [18] supports the view of a single protoepidermal cell origin. However, Frank [27] argues that the secretory

Acknowledgments

This work was supported by National Natural Science Foundation of China [31200152; 31270428], West Light Foundation of The Chinese Academy of Sciences [2011DF06], Science and Technology Program of The Shaanxi Academy of Sciences [2014K-23], and Opening Foundation of Key Laboratory of Resource Biology and Biotechnology in Western China (Northwest University), Ministry of Education [ZS12010].

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