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(American Journal of Botany. 1999;86:841-854.)
© 1999 Botanical Society of America, Inc.

Further studies of the glandular tissue of the Sauromatum guttatum (Araceae) appendix1

Hanna Skubatz 2, 4 and Dennis D. Kunkel 3

2Deptartment of Botany, Box 355325, University of Washington, Seattle, Washington 98195; and 3Bekesy Laboratory, PBRC, University of Hawaii, Honolulu, Hawaii 96822

Received for publication March 23, 1998. Accepted for publication October 19, 1998.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Electron microscopic studies showed that the trans-Golgi network (trans indicates the polarity of cisternae within the Golgi apparatus; it is opposite to the cis-face that is adjacent to the rough endoplasmic reticulum) was involved in the processing of the osmiophilic material present in the appendix of the inflorescence of Sauromatum guttatum. This material accumulated in the rough endoplasmic reticulum and in special pockets of the plasma membrane prior to heat production. Associations between the endoplasmic reticulum and trans-Golgi network were observed. The Golgi apparatus was composed of 5–6 dictyosomes on one side and one or two somewhat detached cisternae on the other side. Various nonosmiophilic Golgi-derived vesicles were observed: small ones covered with spike-like material, large ones with a smooth surface, and irregularly shaped ones. These electron-translucent vesicles seemed to accumulate in specific localities at the plasma membrane surface in the vicinity of the osmiophilic material; they were not found when the aroma was released. During heat production, the Golgi structures shrank and the activity of the trans-Golgi network seemed to be reduced. At the same time, coated pits were seen at the plasma membrane surface. In some cells, hypertrophic Golgi apparatuses were seen with only 2–3 dictyosomes that contained granulated material in their lumens. Finally, the osmiophilic material was also found in the plasmodesmata.

Key Words: appendix • Araceae • electron microscopy • Golgi • osmiophilic material • secretion • voodoo lily


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The production of heat and aroma by the appendix of the inflorescence of Sauromatum guttatum (voodoo lily) is a result of a series of coordinated events involving organelle–organelle interactions, including the endoplasmic reticulum (ER) and plasma membrane (PM). Two to one days before D-day, the day of heat production and release of odor, the appendix accumulates osmiophilic material in special structures of the plasma and ER membranes (Skubatz et al., 1995 ), and that material becomes undetectable in the tissue during heat production. This fact suggests that the osmiophilic material is synthesized and accumulates within the cell until it is discharged on D-day. Additional electron microscopic studies showed that the ER interacts with the PM, creating novel routes of movement, most conceivably for the osmiophilic material (Skubatz et al., 1996 ). It seems that fusion events create channels from the interior to the exterior of the cell. Furthermore, a multitubular body, most likely originating in the ER, seems to fuse with the plasma membrane and to appear only on D-day (Skubatz et al., 1996 ). During the thermogenic activity, more than 100 compounds from at least eight different chemical classes [monoterpenes, sesquiterpenes, fatty acids, ketones, alcohols, aldehydes, indole, phenolic and sulfur compounds (Skubatz et al., 1996 ), and amines (Smith and Meeuse, 1966 )] are liberated.

In plant glands, the Golgi apparatus is active and involved in the export of various molecules to different localities of the cell, especially to the plasma membrane (Schnepf, 1974 ; Fahn, 1979 ; Vogel, 1989; Krontestedt-Robards and Robards, 1993 ). In oil-secreting cells, for example, numerous Golgi-derived vesicles are present near the plasma membrane (Fahn, 1979 ). The morphology and activity of the Golgi apparatus have never been studied in the thermogenic appendix of S. guttatum or in any other thermogenic plants. Our present electron microscopic study shows that the Golgi apparatus is indeed active prior to the production of heat and odor and that the trans-Golgi network is involved in the processing of the osmiophilic material.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant material and growth condition
Inflorescences of Sauromatum guttatum were allowed to develop under the conditions described previously (Skubatz, Kunkel, and Meeuse, 1993 ). The developmental stage of the appendix was determined retrospectively with respect to the day of inflorescence opening and heat production (D-day).

Electron microscopy
Tissue blocks were fixed in glutaraldehyde followed by osmium tetroxide as described previously (Skubatz, Kunkel and Meeuse, 1993 ). Ultrathin sections (silver to light-yellow interference color) from the subepidermal tissue (1–20 cell layers beneath the epidermis) were examined with a Philips-410 electron microscope.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Prior to D-day, many active Golgi complexes were observed in the Sauromatum appendix. Each Golgi apparatus consisted of 5–6 tightly-stacked cisternae (Fig. 1A) and one somewhat detached cisterna (Fig. 1B). The polarity of the Golgi dictyosomes was determined by the presence of vesicles at the trans-side and the presence of rough endoplasmic reticulum (rER) parallel to the Golgi dictyosomes at the cis-side. There were numerous vesicles with irregular shapes at the trans-face of the Golgi dictyosomes and also smooth vesicles (V) that budded off the Golgi cisternae and migrated towards the plasma membrane. The smooth vesicles were homogeneous in shape and size, and had a low electron-density; some of the vesicles seemed to be connected (asterisks in Fig. 1A insert). Interactions between Golgi dictyosomes and a somewhat detached but active flat cisterna, designated as the trans-most cisterna, were observed in some cells (Fig. 1B and insert). Numerous vesicles were released from that cisterna. Another inactive reticulum (R) near the Golgi dictyosomes was often found. It may be that this is a Golgi cisterna that is quiescent in some cells and active in others.



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  		Fig. 1. Golgi apparatus in cells producing osmiophilic material in the Sauromatum appendix 2 d before heat production and the release of odor. (A) A typical arrangement of Golgi dictyosomes (D) in which the cis-face is adjacent to the rough endoplasmic reticulum (rER). The trans-face of the Golgi area is characterized by an extended accumulation of vesicles. Smooth-surfaced vesicles (V) are migrating towards the plasma membrane (PM). Numerous osmiophilic particles (P) are decorating the PM. A curved reticulum (R) next to the dictyosomes is frequently seen. The insert shows another Golgi apparatus with many smooth-surfaced vesicles restricted to the trans-face of the dictyosomes; some vesicles are connected (asterisks). (B) Smooth-surfaced vesicles (V) released from dictyosomes connecting with a distant cisterna. The trans-Golgi network is composed of a trans-most cisterna and a curved reticulum (R) seen near the trans-most cisterna. Note the presence of ribosomes in the close vicinity of the trans-most cisterna (arrows). The insert shows another cell with the same arrangement of Golgi dictyosomes with a detached flat trans-most cisterna (an arrow) and a curved reticulum (R). CW, cell wall; L, lipid body; M, mitochondrion; Va, vacuole. Bars = 0.2 µm.

 
The tubulovesicular structure and versatility of the trans-most cisterna were clearly demonstrated in Fig. 2. The existence of a vesiculated structure is seen in Fig. 2A. In some cases a single cisterna formed a kind of interstack bridge between two Golgi dictyosomes (Fig. 2B). This cisterna was associated with small vesicles covered with a spike-like material (arrowheads; 2B-C) and also large smooth vesicles; it elongated and formed knoblike protuberances (2C, arrows) that probably mirror the budding-off of vesicles. A long filamentous structure was seen in many cells alongside the plasma membrane (Fig. 2B). This structure is part of the ER network.



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  		Fig. 2. Tubular-reticular trans-Golgi network 2 d before heat production. (A) A tubular-reticular cisterna (arrows) at the trans-face of dictyosomes (D). (B) A cisterna (arrows) forms an interstack bridge between two adjacent Golgi dictyosomes (D); arrowheads point to small decorated vesicles. An open arrow points to a tubular filament alongside the plasma membrane (PM). (C) The trans-most cisterna forms an extended, tubular reticular structure (arrows) with knob-like structures. Arrowheads point to decorated vesicles with spike-like structures. Bars = 0.1 µm.

 
Figure 3A-C shows the filamentous structures, most likely microtubules, connected to the sER and rER. At the regions where these ultrastructures were present near the plasma membrane, Golgi vesicles as well as osmiophilic material were undetectable. One likely explanation for this observation is that the cortical ER creates a physical barrier for the vesicles to reach certain areas of the plasma membrane in the Sauromatum appendix.



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  		Fig. 3. Filamentous structures near the plasma membrane in the appendix cells 2 d before heat production. (A) Close association between the tubular structures and the plasma membrane (PM), the smooth ER (sER), and rough ER (rER). (B–C) Tubular structures in close contact with the PM. Bars = 0.1 µm.

 
Often, certain elements of rER had a vesicular appearance with a smooth surface. Figure 4 shows that the rims of the rER cisternae formed a vesiculated reticulum in the proximity of numerous vesicles; some of the vesicles were large and were derived by budding of the ER (asterisks), some were smaller and supposedly derived from the Golgi dictyosomes. The reticular element (R) that is found near dictyosomes was detected in the vicinity of these regions (see Fig. 1).



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  		Fig. 4. Serial sections through an association of rough endoplasmic reticulum with vesiculated regions characteristic of Golgi apparatus. (A–B) The rims of rough endoplasmic reticulum (rER; arrows) cisternae encompass vesiculated regions. Asterisks indicate vesicles that may have originated in the rER. The origin of the rest of the vesicle-like structures is probably from the curved reticulum that is part of the Golgi apparatus. The insert in B shows vesiculation of the rER in another cell. Bars = 0.2 µm.

 
Evidence for the association of the rER and the Golgi dictyosomes was further provided in the serial sections through a portion of a cell containing Golgi dictyosomes on D-day (Fig. 5A-D). During the thermogenic activity, when the aroma is released, the morphology of the Golgi complex changed. The dictyosomes tended to be smaller and the outermost trans-cisternae still created an extended reticulum. The numerous vesicles seen prior to D-day at the trans-face of the Golgi stacks were absent; instead, a clump of vesicle-like structures that may have originated from the Golgi (asterisks) were seen in the vicinity of the dictyosomes. Some vesicles were decorated with ribosomes (arrowheads), suggesting that they had originated from the ER. The boundary between the ER and the Golgi was difficult to distinguish. The images in Fig. 5A-B also suggest that the trans-most cisterna can sometimes be associated with the rER. Figure 5E shows another thermogenic cell with Golgi dictyosomes that exhibited a long trans-most cisterna facing the plasma membrane. Another characteristic ultrustructural feature of a cell during the thermogenic activity was the presence of what seemed to be coated pits in the plasma membrane (Fig. 5F). Prior to D-day, coated pits were not as easily detected as on D-day.



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  		Fig. 5. Golgi apparatus during the thermogenic activity and secretion of volatiles. (A–D) Serial sections through a Golgi complex. The Golgi dictyosomes (D) are reduced in size and an extension of the trans-most cisterna (solid arrows) is clearly seen. The large clump of vesiculated structures with smooth (asterisks) and rough surfaces (arrowheads) seems to be connected to the trans-cisternae. (C–D) The vesiculated structures move away from the dictyosomes; an open arrow points to the reminiscence of the clump of vesicles (D). Association between the endoplasmic reticulum and a mitochondrion (M, curved arrows) is observed. (E) Another Golgi complex with an extended trans-cisterna in the vicinity of the plasma membrane (PM). (F) Coated pits (arrows) in the PM during heat production. CW, cell wall. Bars = 0.2 µm.

 
Some cells at the pre D-day stage had very enlarged Golgi structures with only 2–3 cisternae (Fig. 6); the trans-most cisterna was bent and formed an entirely closed circle that seemed to engulf some ribosomes. Reticular elements were seen around the cisternae and some were studded with ribosomes.



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  		Fig. 6. Hypertrophic dictyosomes 2 d before heat production. (A) Hypertrophic dictyosomes (D) near the plasma membrane (PM). The cisternae form a ring shape at the trans-face. Reticular membranes (arrows) and membranous structures that resemble vesicles (arrowheads) are present near the cisternae. The enlarged Golgi apparati were found in cells 7–10 cell layers underneath the epidermis. CW, cell wall. Bars = 0.1 µm.

 
At the pre D-day stage, the trans-Golgi network seems to be involved in the processing of the osmiophilic material (Fig. 7). The osmiophilic material was seen in the swollen terminals of some cisternae and in the trans-most cisterna with its vesiculated branches (Fig. 7B-C, F). The osmiophilic material was invisible in the cisternae in the cis-region. Osmiophilic, small, dark vesicles were not detected near the plasma membrane, suggesting that the disappearance in Fig. E-F of the osmiophilic aggregate may be attributed to either its processing and packaging into electron-translucent vesicles seen in Fig. 7A, or to its dissolution and recycling by the trans-cisternae. On D-day the osmiophilic material was not found in the Golgi complex.



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  		Fig. 7. Serial sections through a Golgi apparatus involved in the processing of osmiophilic material two days before heat-production. (A) Osmiophilic material is visualized in the terminal edges of the trans- cisternae and is not evident in the cis-cisternae. Many vesicles (V) are released from the trans-most cisterna (arrows). (B–D) Osmiophilic material (O) accumulates in the trans-cisterna and the surrounding area. Electron-translucent and smooth vesicles (V) are released from cisternae close to the trans-cisterna and seem to migrate towards the plasma membrane (PM). (F) Osmiophilic material in the knob-like structures of the trans-cisterna (arrows). M, mitochondrion. Bars = 0.2 µm.

 
Very distinct types of electron-translucent vesicles were detected around the osmiophilic particles of the plasma membrane prior to D-day (Fig. 8A-D and E insert), but were not detectable on D-day. The vesicles seemed to be oriented around the osmiophilic particles (Fig. 8A-D). They were lined up around these sites, forming rows of three or four vesicles in a file perpendicular to the plasma membrane. In many cases, Golgi dictyosomes were found close to the osmiophilic particles at the plasma membrane (Fig. 8E).



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  		Fig. 8. Association between osmiophilic particles and vesicles at the plasma membrane surface 2 d before heat production. (A–D) Serial sections reveal the presence of vesicles in the vicinity of the osmiophilic particles (P) at the plasma membrane (PM). (A) The presence of electron-translucent vesicles near an osmiophilic particle (P). Dictyosomes (D) are at a distance from the PM. (B–C) An association between the vesicles and an osmiophilic particle (P). (D) Vesicles are still detected in the vicinity of the PM but the osmiophilic material is not. Note the presence of ribosomes and rough endoplasmic reticulum (rER) in the vicinity of the vesicles and PM. (E) Dictyosomes in close association with an osmiophilic particle (P). Note the presence of rER and ribosomes near the dictyosomes and particles. Another cell in which vesicles are detected near the PM is shown in the insert. M, mitochondria. Bars = 0.25 µm.

 
The osmiophilic material was also found in the plasmodesmata (Fig. 9). It accumulated in the central cavity of branched plasmodesmata. On D-day, the plasmodesmata as well as the associated ER were electron-translucent.



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  		Fig. 9. Plasmodesmata in the appendix tissue before and during heat production. (A–C) One to 2 d before heat production and (D) during heat production. (A) Cells with osmiophilic material near the plasma membrane (PM) are interconnected by plasmodesmata (Pd). (B) Osmiophilic material (O) in the plasmodesmata (asterisks) of two adjacent cells. (C–D) A channel-like structure of the endoplasmic reticulum (ER) that is in continuity with the Pd. Open arrows point to the plasmodesmal portion connected to the ER channels. Electron-translucent ER is indicated by a big asterisk. rER, rough ER. Bars = 0.1 µm.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Our recent ultrastructural study on the trafficking of the osmiophilic material in the cells of the Sauromatum appendix provided electron microscopic evidence for its movement from the ER to the special pockets of the plasma membrane (Skubatz et al., 1995 ). The present study suggests that the trans-Golgi network may also be involved in the processing of this material. The morphology of the Golgi apparatus in the appendix tissue of the inflorescence of Sauromatum guttatum has been studied at the pre D-day stage and on D-day when heat and odor are released. Prior to D-day, the Golgi dictyosomes consist of 5–6 dictyosomes and an active trans-Golgi network. Some cells had enlarged Golgi dictyosomes. Prominent accumulations of vesicles were observed near the trans-most cisternae and rough ER. This trans-Golgi activity is probably not related to the appendix growth because at the pre D-day stage, 1–2 d before heat production, the appendix does not elongate anymore, suggesting that the role of the trans-Golgi cisterna is in the accumulation of compound(s) needed for the production of heat and odor. On D-day, the Golgi dictyosomes are reduced in size, and the number of secretory vesicles is also reduced. The ultrastructure of the trans-most cisterna also changes during heat production; it becomes shorter and linear without any noticeable branching. The reduction in Golgi size on D-day, when the secretory process is at its peak, suggests that the secretory products accumulate at the pre D-day stage and are released on D-day. In mammalian cells it has been shown that the trans-Golgi can form tubulovesicular structures that interconnect membranes of adjacent Golgi (Cooper et al., 1990 ). It is possible that the bridge formed between two adjacent Golgi dictyosomes seen in Fig. 2 consists of trans-Golgi cisternae and that those structural changes may reflect changes in Golgi functions. In many systems, the ultrastructure of the Golgi dictyosomes is an expression of its function in secretion (Beans and Kessel, 1968 ; Griffiths and Simon, 1986 ; Morré, 1987 ; Pavelka, 1987 ; Griffing, 1991 ).

When the osmiophilic material accumulates in the appendix cells at the pre D-day stage (Skubatz et al., 1995 ), it is detectable in the trans-Golgi. The trans-most cisternae play an important role in the sorting of secretory proteins in many secretory systems and are the main exit site for several newly synthesized molecules passing from the Golgi complex to other cellular locations (Geuze and Morré, 1991 ). In animal cells, for example, the sorting of proteins into the secretory granules of pancreatic ß-cells (Kuliawat and Arvan, 1994 ) and of Aplysia neurons (Sossin, Fisher, and Sceller, 1990 ) occurs in the trans-most cisternae. In plants, the sorting, processing, and packaging of polysaccharides and glycoproteins transported to the cell wall and plasma membrane (Chrispeels, 1976 , 1991a , b ; Staehelin et al., 1990 , 1993 ; Zhang and Staehelin, 1992 ; Schnepf, 1993 ; Staehelin and Moore, 1995 ) and to the vacuoles (Chrispeels, 1991a , b ; Griffiths and Watson, 1993 ) are carried out in the trans-most cisterna. The trans-Golgi network also consists of acidic compartments that permit the dissociation of molecules taken in by endocytosis as well as the recycling of proteins from the plasma membrane (Staehelin and Chapman, 1987 ; Fowke, Tanchak and Galway, 1991 ). It is possible that some of the osmiophilic material may be dissociated in the trans-most cisterna and its constituents may migrate back to the ER via the Golgi-ER connections at the trans-region.

The boundary between the ER and the trans-Golgi network is not well distinguished in the appendix tissue. In active secretory cells of plants and mammals, the boundary of the ER–Golgi is enormously complex and also difficult to distinguish (Griffiths, 1996 ). In Sauromatum cells, it appeared on many occasions that ribosomes were also associated with the trans-cisternae. Whether specific proteins were synthesized at those locations has yet to be determined. On D-day, coated pits were found in the plasma membrane, suggesting that the direction of flow of material from Golgi to plasma membrane may be reversed and recycling of plasma membrane components may occur.

While it is not possible from electron micrographs to determine the direction of the flow of different vesicles, the presence of electron-translucent vesicles near the osmiophilic material at the plasma membrane is clear. These vesicles are most likely transported from the Golgi to the plasma membrane. The osmiophilic particles seen in the cell in Fig. 7 have the same electron density as those previously studied at pre D-day stage (Skubatz et al., 1995 ), which had been shown to originate from the ER.

It appears that the ER in the appendix cells is present also as a tubular element not only near the peroxisomes (Skubatz et al., 1993 ) and the plasma membrane (Skubatz et al., 1996 ), but also near the Golgi dictyosomes. In plant cells, the ER occurs in two basic and continuous forms (Quader and Schnepf, 1986 , 1989 ; Hepler et al., 1990 ). The first type is arranged in flat cisternae of variable sizes, and the second form is thin tubular elements that are interconnected and consist of microtubules. The tubular ER is also involved in the secretion of various metabolites in salt glands, nectar-secreting cells, and oil glands (Fahn, 1979 ). In the cells of the Sauromatum appendix, portions of the rER cisternae were characteristically smooth when they were close to other cellular organelles. These include regions of ER adjacent to the plasma membrane, mitochondria, microbodies, and Golgi dictyosomes.

The ER has been reported to form a continuous structure between adjacent cells via its passage through the plasmodesmata (Robards and Lucas, 1990 ; Oparka, 1993 ), and it has been shown that lipids (Grabski, de Feijter, and Schindler, 1993 ) and other molecules (Beebe and Turgeon, 1991 ; Lucas, Ding, and van der Schoot, 1993 ) can migrate from the ER of one cell to the other through the plasmodesmatal pore. Our electron micrographs reveal the presence of osmiophilic material in the plasmodesmata, and it is likely that this material can also move to the neighboring cells.

At the present time our understanding of the secretory pathways in the Sauromatum appendix is still incomplete. However, we can conclude that the pathways comprise the ER, plasma membrane, and trans-Golgi network. The intimate association between the ER and these other cellular components is quite striking, and it seems that the smooth-surfaced ER is in the immediate region of association with different cellular organelles, whereas at other sites along its surface it has ribosomes. We suggest that the appendix tissue is a perfect example of a functionally continuous system that is involved in the production of volatiles and heat, where the sites of membrane interactions may facilitate exchange of lipids and other material between adjacent membrane components.

Other members of the Araceae family also produce heat and aroma during anthesis, and it is likely that the intense interactions between different cellular organelles are the reason for these highly coordinated events. We suspect that the Golgi dictyosomes are active in plants of other families that have osmophores (Asclepiadaeae, Aristolochiaceae, Orchidaceae, and Burmanniaceae; Vogel, 1989 ).


   FOOTNOTES
 
1 Back

4 Author for correspondence. Back


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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