Advances in Botanical Research, Vol. 10
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G A part of transverse wall between stalk cell and head cell is penetrated by numerous plasmodesmata arrows. H—J The ultrastructural aspects of internal glands at late-secretory stage are observed as follows. I Plastids P contain numerous oil droplets arrows. J Lipid droplets L in sub-cuticular space are surrounded by silk-like structure arrows. The internal glands in leaves originated from a single undifferentiated palisade cell-like which had a larger nucleus and nucleolus Figure 1C , arrow.
The initial cell of internal glands formed one big vacuolated basal cell and one small, cytoplasmically dense apical cell through the unequal periclinal division Figure 1D , arrows. As the development processed, the apical cell formed one narrow stalk cell and one big head cell with nucleus and nucleolus Figure 1E , arrows.
Volume 94. The Nitrogen-Fixing Legume-Rhizobium Symbiosis
Afterward, the head cell enlarged to form the secretory cell which had a dense cytoplasm and large nuclei with prominent nucleoli Figure 1F. When the internal glands came into secretory stage, the composition and the localization of the secretory compounds in SCS could be detected. The histochemical tests for detecting lipids compounds have given the positive results in this internal gland.
These results were also confirmed using OsO 4 for unsaturated lipids Figure 1J. The Nadi reaction showed up an intense violet or blue-violet staining of the oil droplet contained in the SCS Figure 1K. The head cell of mature internal gland became stained fluorescent yellow-orange with the Naturstoffreagent A which indicated flavones Figure 1L. The histochemical tests carried out to detect polysaccharides compound, using ruthenium Red and PAS, showed up very weak reactions not shown. The internal glands, differing from external glandular trichomes or internal glands in leaves, originated from a signal meristematic cell close to phloem with nucleus and nucleolus Figure 2C.
Through a series of anticlinal division, a uniseriate row of three cells was formed Figure 2D and E. The lower cell of the row corresponded to the basal cell of glands, the upper to the glands head and the intermediate to the stalk. In the young internal gland of stems, the head cell did not have cuticle outer cell wall and was much smaller than that of mature internal glands in size Figure 2E.
With a further thickening of stem, the head cell lengthened and was covered with a thick cuticle. Fully-developed internal glands consisted of one long, cytoplasmically dense and cuticle-covered head cell, one narrow stalk cell and one vacuolated basal cell Figure 2G. When subjected to UV light, the secretory material staining with Neutral red contained in the SCS revealed an intense gold-yellow secondary fluorescence, whereas slight chloroplasts fluorescing red chlorophyll autofluorescence were seen in stalk region Figure 2H.
The Nadi reaction resulting in an intense violet or blue-violet staining of the secretion contained in the SCS indicated the presence of terpenoids Figure 2L. The fluorochrome for flavonoid detection, Naturstoffreagenz A induced a yellow-green secondary fluorescence in head cell and secreted exudate Figure 2M. Similar to internal glands of leaves, the glands in stems gave negative or weak reactions with the tests used for polysaccharides compound.
The release of secreted exudate in SCS of the two internal gland types to the environment through cuticle was not observed. However, each of the three external trichome types of Pogostemon cablin showed intense secretion release in different ways under cryo-SEM Figure S2.
The secreted material was possibly released via the random fibrillar network on the reticulate cuticle of short-stalked capitate glandular trichomes or the gaps between the spherical accumulations of cutin at the apex of peltate glandular trichomes Figure S5. The cuticle of external and internal glands showed different thicknesses, whereas the cuticle of internal glands of leaves had similar morphology and thicknesses with that of internal glands of stems Figure S5.
In the secretory stage, the head cells of three external trichome types of Pogostemon cablin showed different ultrastructural features, although they all had dense cytoplasm with nucleus and nucleolus, numerous plastids and small vacuole. In the two secretory cells of short-stalked capitate glandular trichomes, long and narrow cisternae of rough endoplasmic reticulum, forming stacks, were found in the parietal cytoplasm, lying parallel to each other and to the plasma membrane Figure 3A and B.
And numerous Golgi vesicles were found in head cell and close to plasma membrane Figure 3C. Unlike short-stalked capitate trichomes, the secretory cell of peltate glandular trichomes contained numerous short segments of SER which surrounded Golgi and plastids Figure 3D and E. And many vesicles between plasma membrane and cell wall were observed Figure 3F , arrows.
In contrast to short-stalked capitate and peltate glandular trichomes, the long-stalked capitate glandular trichomes contained fewer long SER and sparse Golgi Figure 3G and J. And the apical cell was strongly polarized. Numerous small vacuoles occupied the middle and basal parts of the cell and surrounded the nucleus Figure 3G and H.
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The plastidome consisted of amoeboid plastids that often contained moderately large plastoglobuli and lipid-like material and occupied the apical region of the secretory cell Figure 3I and J. Similar to peltate glandular trichomes, one vesicle between cell wall and plasma membrane was present in several specimens Figure 3K. G—K Ultrastructural aspects of the long-stalked capitate trichomes: G the mature glandular trichomes with a cytoplasmically dense apical cell, a narrow stalk cell and an elongated vacuolated stalk cell; H the higher magnification of G showing the secretory cell with the sub-cuticular space SCS , many small vacuoles V , abandent mitochondria M and numerous small plastids P ; I the details of the cytoplasm of the secretory cell showing prevalence of mitochondria M and plastids P with plastoglobuli in the apical region; J the sparse smooth endoplasmic reticulum SER close to a lipid-filled plastid P arrow ; K a bigger vesicle arrow between cell wall CW and plasma membrane PM.
The internal glands located in mesophyll parenchyma ultrastructurally resembled peltate trichomes Figure 4A. In early secretory stage, the head cell of internal glands was characterized by enlarged plastids, numerous small vacuoles, an extensive short rough endoplasmic reticulum RER and the detachment of the thick cuticle from the outer cell walls to form an extensive extracellular SCS Figure 4B and C. In SCS, a smooth-textured, lipid-like material occurred within the fibrillar substance as thin, sheet-like layers Figure 4B.
RER appeared to closely approach or contact plastids and osmiophilic deposits were consistently present along RER segments near the plastids Figure 4C and D. In the late secretory stage, SCS filled with numerous lipid spherosomes surrounded by a lot of fibrillar substance became very big Figure 4J. Plastids often contained large plastoglobuli and oil droplets Figure 4I. Unlike capitate trichomes, the internal glands lacked Golgi bodies and large vesicles but, numerous mitochondria were found. The lateral cell wall of the narrow stalk cell thickened and had become densely staining Figure 4A , arrow.
The narrow stalk cell with dense cytoplasm contained larger nucleus and elliptical chloroplasts with starch grains. Abandent small mitochondria and a few of small vacuoles were also observed in the narrow stalk cell Figure 4F. The basal cell with natural chloroplasts remained vacuolate, and its peripheral cytoplasm appeared to contain fewer organelles than the stalk or secretory cell Figure 4A.
The periclinal cell wall, bordering the stalk cell, usually contained branched plasmodesmata Figure 4G. Compared with internal glands in leaves, the internal glands of stems had one longer, cytoplasmically dense and cuticle-covered head cell, one narrow stalk cell and one vacuolated basal cell Figure 5A.
In secretory stage, the SCS formed by the detachment of the thick cuticle from the outer cell walls was filled with numerous spherosomes Figure 5B , asterisks. The secreted material, stored in the periplasmic space Figure 5C , asterisks , passing through the wall, accumulated temporarily in the SCS. The oil droplets surrounded by membrane-like structure arrow in SCS contained lipid droplets and electron-opaque material outside the oil droplets Figure 5D.
After the head cell reached the characteristic structure of a fully-developed gland, numerous mature plastids with small plastoglobuli, the marked proliferation of the endomembrane system, an increase in the number of mitochondria and a lot of small vacuoles were the remarkable feature of the secretory cell Figure 5E and I. In this stage, the secretory cell contained two nuclei with clear nucleolus Figure 5A.
Plastids were found only in secretory cells, usually in close contact with short cisternae of smooth endoplasmic reticulum SER Figure 5I , arrows. These plastids were variable in form and lacked chloroplasts and starch grains Figure 5F and I. The small vacuoles near plastids and short cisternae of SER often contained larger highly osmiophilic spherosomes Figure 5F. At the apical region of the secretory cell, vacuoles variable in form seemed to be exhausted and in close contact with electron-opaque material Figure 5H and L.
In addition, vacuoles with electron-opaque material were often observed near the plasma membrane Figure 5L. Short segments of SER filled with osmiophilic droplets appeared closely approach or contacted the plasma membrane and plastids Figure 5G and I. Numerous mitochondria were extensively distributed within the cytoplasm near other organelles Figure 5E. The Golgi was sparse and not well-developed.
The stalk cell had two big vacuoles and cellulosic cell walls that were stained black. The cytoplasm was dense and had several mitochondria. The stalk cell contained one triangular nucleus with clear nucleolus and many plastids with big stanch grains Figure 5J. The basal cell was highly vacuolated and its peripheral cytoplasm appeared to contain fewer organelles than the stalk or secretory cells. Plasmodesmata occurred frequently between the head cell and the stalk cell, and also occurred between the basal cell and the stalk cell, but were less numerous Figure 5K.
There was not obvious connection between the internal gland and parenchymal cells around. A Longitudinal section of internal glands showing that the internal gland has a long head cell HC , a stalk cell SC and a basal cell BC. D Oil droplets in SCS contain lipid droplets L and membrane-like structure arrow outside the oil droplet.
E Portion of head cell showing numerous mitochondria M , small vacuoles V and plastids P. F Vacuoles with electron-opaque material arrows are in close to plastid P and mitochondria M. G The smooth endoplasmic reticulum arrows is observed to be in close to plasma membrane PM.
H Portion of mature internal glands showing electron-opaque material arrows in close contact with vacuoles. I The smooth endoplasmic reticulum arrows in close to plastids P. J The stalk cell with thickened lateral wall arrow contains big vacuoles V , the nucleus N and numerous plastids P.
K The details of cell wall showing plasmodesmata arrows that connect the narrow stalk cell and head cell. L The details of head cell showing that vesicles V near plasma membrane PM are in close connect with electron-opaque material arrows. Observations on transverse section of leaves showed internal glands of Pogostemon cablin distributed among palisade cells, which was similar to the intact sub-dermal secretory cavities of Eucalyptus  and elaiophores of Oncidium trulliferum .
In contrast to the elaiophores of Oncidium trulliferum which secreted and stored oils under a distinct subepithelial layer, the oils of the internal glands were secreted and stored in the SCS like the external glandular trichomes. Compared to the internal glands in leaves, numerous internal glands with long head cell among cortex cells of stems had bigger SCS filled with oil droplets.
Observations on the development of the two internal glands types showed that the glands of stems originated from a single meristematic cell close to phloem and the internal glands in leaves originated from one undifferentiated palisade cell. These results indicated that the two internal gland types both originated from similar ground meristem.
The absence of the two internal gland types in primordial leaves and apical dome of the stem apex suggested cellular differentiation at a later stage during the maturation of stems and leaves. However, cell differentiation terminates in early leaf development, which is described by Cutter . These observations may not provide further evidence for this hypothesis.
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An abundance of terpenoids was reported in the leaves and stems of Pogostemon cablin . Monoterpenes dominate the secretory material of Rutaceae species  and the Lamiaceae  ; Sesquiterpenes and other terpenes are the main components of the essential oil of the Asteraceae . Terpenoids have many different functions in plants such as attracting pollinating insects to flowers or protecting the plant from destruction by herbivores and other pathogens  , .
The result of the Nadi reagent test revealed the presence of the terpenoids in the secretory material stored in SCS of all mature gland types of Pogostemon cablin. The abundant terpenoids in the external and internal glands of Pogostemon cablin may protect the plant from destruction by herbivores through influencing their alimentary system.
Histochemical test on the two fully developed internal glands indicated that the secretion contained lipophilic components. These results are similar to the phytochemical data available for other species of the Lamiaceae . The presence of lipid compounds in palisade tissue has also been reported by Maria et al. Only the internal glands and short-stalked capitate glandular trichomes contained flavones. These functions of flavones had been accentuated by the presence of flavonoids in internal glands.