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Annulus–pore relationship in Gramineae (Poaceae) pollen: the pore margin of Pariana¹

²Department of Botany and Microbiology and Oklahoma Biological Survey, University of Oklahoma, Norman, Oklahoma 73019-6131 USA; ³Botany Department, Stockholm University, SE-106 91 Stockholm, Sweden; ⁴Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299 USA; ⁵University of Oklahoma, Noble Microscopy Laboratory, Norman, Oklahoma 73019 USA

Received for publication May 9, 2002. Accepted for publication January 10, 2003.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION LITERATURE CITED

 
Pariana, a primitive bamboo, is the only genus in the Gramineae (Poaceae) to have pollen grains without an annulus as part of its single aperture (porate) system. In contrast, the markedly thickened exine layer underlying the pore margin is similar to counterparts in all grass genera. Components of the future annulus in Gramineae pollen develop toward the cytoplasm (proximally) and begin to be pressed outward by an increase in the cytoplasm during the microspore vacuolate stage, culminating in an annulus by maturity. However, in some species of Pariana these components are either not sufficiently developed or the cytoplasmic expansion is not sufficient to press the components into an annular ring around the pore. The structural relationship of exine layering in this type of pollen grain in Gramineae and other families with similar apertures has not hitherto been extensively studied. A critical examination of the apertures in bambusoid grasses may clarify their systematic position within the Gramineae.

Key Words: annulus • costa pori • ectexine • endexine • exine • Gramineae • Pariana • Poaceae • pore

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION LITERATURE CITED

 
The archetypal aperture system in grass pollen is a single pore consisting of an "island" of ectoaperture exine, the operculum (Wodehouse, 1935 ), circumscribed by a raised and thickened border of ectexine, the annulus (Jackson, 1928 ; Potonie, 1934 ; Cranwell, 1953 ; Kremp, 1965 ; Punt et al., 1994 ). Proximally (i.e., facing the cytoplasm), a thickened ring-like layer, more-or-less equal in dimensions to the annulus, surrounds the pore margin. This thickening of the endoexine bordering the endopore has been termed "costa pori" by Iversen and Troels-Smith (1950) . This aperture system is characteristic of nearly all of the approximately 10 000 species in the Gramineae and has been extensively documented (e.g., Andersen and Bertelsen, 1972 ; Grant, 1972 ; Watson and Bell, 1975 ; Page, 1978 ; Kohler and Lange, 1979 ; Longhi and Kozuka, 1994 ). However, in rare instances the annulus appears to be absent. This absence was first brought to attention in Pariana vulgaris Tutin (Page, 1978 ) and later, in other species of Pariana (Salgado-Labouriau and Rinaldi, 1990 ; Salgado-Labouriau et al., 1993 ; Chissoe et al., 1994a ).

The present report considers the relationship of the external and internal exine layers of the pore margin in most grasses and in the presumptive non-annulate pollen grains of Pariana (Poaceae: Bambusoideae: Olyreae) after examination by scanning electron microscopy (SEM, whole and freeze-fractured grains) and by transmission electron microscopy (TEM). Comparisons are made with the pore margins in typical representatives of the Gramineae. A sequence of sections of the aperture of Poa annua is included to show examples of the development of the typical annulus of the grass pollen grain aperture as compared with the aperture in some Pariana pollen grains. This character state (i.e., little or no annulus), in conjunction with other taxonomic traits, may be useful in grass phylogeny.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION LITERATURE CITED

 
Collections of Pariana pollen (Table 1) were acetolyzed (Erdtman, 1960 ) and split into fractions for SEM and TEM. The SEM fraction was divided into two additional subfractions. The first, consisting of whole pollen grains, was stained with repeated exposures to osmium and thiocarbohydrazide (Chissoe et al., 1995 ), dried with hexamethyldisizane (Chissoe et al., 1994b ), and mounted on double-stick tape on rectangular specimen stubs. The second SEM fraction was frozen into a pellet with Tissue-Tek O.C.T. 4583 Compound (Miles Scientific Laboratories, Naperville, Illinois, USA), splintered with a steel knife on a cryomicrotome, and collected directly onto specimen stubs (Skvarla et al., 1988 ). Both subfractions were pulse sputter-coated with gold/palladium (Chissoe and Skvarla, 1996 ) and then examined with a JEOL 880 scanning electron microscope (JEOL USA, Peabody, Massachusetts, USA) equipped with a lanthanum hexaboride gun at 15 kV. For comparative purposes, acetolyzed pollen grains of Agropyron repens, Festuca elatior, Poa compressa, and Zea mays (Table 1) were prepared and examined as described.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION LITERATURE CITED

 
Ectexine sculpturing immediately surrounding the pore in Pariana stenolemma (Fig. 1), P. argentea (Fig. 2), P. pallida (Fig. 3), P. radiciflora (Fig. 4), and P. bicolor (Fig. 10) pollen was identical with ectexine sculpturing on all other areas (i.e., non-apertural ectexine) of the pollen wall surface. Sculpturing consisted of fused and spinulose areolate elements grouped into irregular islands interspersed with globular/granular exine particles approximately 0.25 µm in diameter (Figs. 1–4, 10). However, as pointed out elsewhere (Salgado-Labouriau et al., 1993 ), sculpturing elements tended to become concentrated and slightly uplifted around the pores in some species (Figs. 4, 10). The lack of ectexine differentiation in the pore area (Figs. 1–4, 9–15) clearly indicated the absence of an annulus as originally defined by Jackson (1928) and subsequently enumerated in pollen glossaries (Kremp, 1965 ; Punt et al., 1994 ) and texts (Faegri and Iversen, 1964 ; Moore et al., 1991 ). This absence was especially notable when compared with similar features in SEM micrographs of Poa compressa (Figs. 7, 8), Zea mays (Figs. 16, 17), Agropyron repens (Fig. 18), and Festuca elatior (Fig. 19), as well as with all published light, SEM, and TEM micrographs of Gramineae pollen (e.g., Wodehouse, 1935 ; Erdtman, 1971 ; Nilsson et al., 1977 ; Moore and Webb, 1978 ; Kapp et al., 2000 ). The exterior curvature of the pore area in these taxa was markedly arched, signifying annuli, as compared to the smooth curvature of the pore areas in the aforementioned Pariana pollen grains.

View larger version (149K): [in this window] [in a new window]   Figs. 1–8. Scanning electron micrographs of Pariana (Figs. 1–6) and Poa compressa (Figs. 7, 8) pollen. 1. Pariana stenolemma. View of whole pollen grain showing non-annulate aperture. 2. Pariana argentea. Pore region without an annulus. 3. Pariana pallida. Non-annulate pore region almost indistinguishable from the ectexine. 4. Pariana radiciflora. Although the grain appears non-annulate, a slightly elevated row of exine elements immediately surrounds the pore. 5, 6. Pariana stenolemma. Pollen grain with freeze fracture through non-apertural exine showing thickening of layer beneath the pore (arrow). 6. Enlarged view of internally thickened layer similar to Fig. 5. 7, 8. Poa compressa. 7. Freeze fracture in same area of exine as that of Pariana stenolemma in Fig. 5, showing the lower internal thickening (arrow) surrounding the pore. 8. Pore region on exine surface showing an annulus (a) surrounding the operculum typical of most grass pollen grains. Compare with non-annulate Pariana (Figs. 1–5, 10). Unless indicated, bar = 1 µm.Figs. 9–19. Transmission (Figs. 9, 14, 15) and scanning (Figs. 10–13, 16–19) electron micrographs of Pariana, Zea (Figs. 16, 17), Agropyron (Fig. 18), and Festuca (Fig. 19) pollen. 9–11. Pariana bicolor. 9. The arrows indicate the thickened lower layer, the problematic endexine, surrounding the pore. 10. While an annulus is not apparent, exine elements appear to be slightly concentrated around the pore (see Fig. 4). 11. Freeze fracture through the pore area. Note smooth exterior curvature of exine in pore area (compare with distinct annulate areas in Figs. 16–19) and thickened layer beneath pore (arrow). 12–15. Pariana radiciflora. 12. Freeze fracture through area slightly away from pore (same as Fig. 16) showing smooth exterior curvature of exine and slight thickening of lower exine layer. 13. Freeze fracture through edge of pore. Note smooth exterior curvature of exine as previously noted in Figs. 9–12 and narrow layer (arrows) beneath the pore similar to that in Figs. 9 and 11. 14. Edge of pore area showing prominent development of the lower thickened layer (arrows) surrounding the pore. 15. Section directly through pore suggesting an endexine origin for the lower thickened layer. 16, 17. Zea mays. 16. Freeze fracture through edge of pore showing prominent annulus (a) and lower thickened layer. Note distinct break in curvature of exine surface over the pore area in comparison with Pariana (Figs. 11–14). 17. Freeze fracture directly through pore showing annulus (a) and lower thickened layer. Compare with Fig. 11. 18. Agropyron repens. Freeze fracture similar to Zea (Fig. 16) but with less pronounced annulus and lower thickened layer. 19. Festuca elatior. Freeze fracture on edge of annulus showing elevation of annulus above curvature of exine surface and the lower thickened layer. Unless indicated, bar = 1 µm.>

View larger version (112K): [in this window] [in a new window]   Figs. 9–19. Transmission (Figs. 9, 14, 15) and scanning (Figs. 10–13, 16–19) electron micrographs of Pariana, Zea (Figs. 16, 17), Agropyron (Fig. 18), and Festuca (Fig. 19) pollen. 9–11. Pariana bicolor. 9. The arrows indicate the thickened lower layer, the problematic endexine, surrounding the pore. 10. While an annulus is not apparent, exine elements appear to be slightly concentrated around the pore (see Fig. 4 ). 11. Freeze fracture through the pore area. Note smooth exterior curvature of exine in pore area (compare with distinct annulate areas in Figs. 16–19) and thickened layer beneath pore (arrow). 12–15. Pariana radiciflora. 12. Freeze fracture through area slightly away from pore (same as Fig. 16) showing smooth exterior curvature of exine and slight thickening of lower exine layer. 13. Freeze fracture through edge of pore. Note smooth exterior curvature of exine as previously noted in Figs. 9–12 and narrow layer (arrows) beneath the pore similar to that in Figs. 9 and 11. 14. Edge of pore area showing prominent development of the lower thickened layer (arrows) surrounding the pore. 15. Section directly through pore suggesting an endexine origin for the lower thickened layer. 16, 17. Zea mays. 16. Freeze fracture through edge of pore showing prominent annulus (a) and lower thickened layer. Note distinct break in curvature of exine surface over the pore area in comparison with Pariana (Figs. 11–14). 17. Freeze fracture directly through pore showing annulus (a) and lower thickened layer. Compare with Fig. 11. 18. Agropyron repens. Freeze fracture similar to Zea (Fig. 16) but with less pronounced annulus and lower thickened layer. 19. Festuca elatior. Freeze fracture on edge of annulus showing elevation of annulus above curvature of exine surface and the lower thickened layer. Unless indicated, bar = 1 µm.

The complexity of the pore region was appreciated early on by the statement of Faegri and Iversen (1964) , who raised the question of "whether costae and annuli are simple thickenings of the respective layers, bulges filled with some other material, or more complicated conduplications. . . ." Faegri and Iversen (1964) considered these thickenings to be of great theoretical interest but acknowledged that they would be difficult to observe. We interpret the annulus and lower thickened endexine layer as part of one developmental sequence. The thickening of the endexine when pressed outward by cytoplasmic expansion resulted in an annulus manifested by a bulging ectexine ring around the pore. Thus, the annulus is a product of a layer within the exine that is developed sufficiently to "raise" the ectexine or cytoplasmic expansion sufficiently to press the layer within the exine outward. When an annulus appears to be absent as it is in some Pariana species, our work suggests that the layer responsible for the ectexine bulge is present. However, the layer may not be developed to the extent of elevating the ectexine, or the cytoplasm of Pariana may not provide the pressure required to press out the endexine layer from a "costa pori" condition to an annulus. Furthermore, SEM micrographs of Zea (Figs. 16, 17) and TEM micrographs of Poa annua (Figs. 20–26) indicate that annulus and lower (proximal) thickened layer are one and the same. The proximal thickened layer either remains proximal, as in Pariana, or is moved developmentally to the position of the annulus, as in most grass taxa. Components of the lower (proximal) thickened layers first developed inward toward the cytoplasm, but later they were pushed outward as the cytoplasm expanded, resulting in the typical raised annulus of grass pollen.

View larger version (88K): [in this window] [in a new window]   Figs. 20–26. Transmission electron micrographs (Figs. 20, 22–26) and sketch (Fig. 21) of Poa annua illustrating annulus development. 20. Early development of the aperture (asterisk) and internal thickenings (arrowheads) that will become the annulus around the pore. Embedding resin removed and section shadowed with Pt. 21. Sketch of TEM showing early development of the components of the future annulus that are mostly arranged toward the cytoplasm. 22. Thickened components (arrowheads) of the annulus just prior to the vacuolate microspore stage. At this stage, these components form a ring-shaped bulge into the cytoplasm. 23, 24. (Fig. 24 is an enlargement of Fig. 23). Components of the annulus during the vacuolate stage are pressed outward. These components have much less inward bulging (arrowheads) than in Fig. 22. An operculum (arrow) covers part of the pore. 25, 26. Portions of the TEMs in Figs. 25 and 26 are from the work of Rowley, 1964 . 25. In the pollen grain stages following microspore mitosis, the annulus (arrowheads) is elevated. There are still uncompressed components of the annulus. 26. In mature pollen of Poa annua, the annulus is elevated and the components of the annulus are greatly compressed internally. An arrow marks the operculum. Embedding resin removed and section shadowed with Pt. Bar = 1 µm

Other orders having porate pollen with annuli include Restionales (Chanda and Erdtman, 1965 ; Chanda, 1966 ; Chanda and Rowley, 1967 ; Ladd, 1977 ; Linder, 1984 ; Linder and Ferguson, 1985 ) and Plantaginales (Cartier, 1970 ; Clarke and Jones, 1980 ; Ubera et al., 1988 ). The Restionaceae have two major types of ulcerate apertures, graminoid and centrolepidoid (Chanda, 1966) . Linder (1984) described eight annulus/foot layer thickening combinations and used them in phylogenetic classification of the family. Similarly, remarkable annulate and non-annulate pollen forms were enumerated for Plantago (Plantaginaceae) and successfully utilized in taxonomic clarification of the genus (Ubera et al., 1988 ).

In summary, several ideas emerge from this report. From a structural/developmental standpoint, the prominently thickened foot layer in porate pollen grains without traditional annuli requires additional study and detailed description. Further, this study should be extended beyond Poaceae to include all similarly constructed porate apertures, such as the thick annuli with markedly thin (i.e., not expanded) foot layers. These can be seen in the TEM micrographs of the restionaceous taxa Hypolaena digitata and Chondropetalum ebracteatum (Linder, 1984 ), in the many species of the Haloragaceae illustrated with LMs, SEMs, and TEMs (Praglowski, 1970 ), and in SEM/TEM sections of Myriophyllum (Skvarla et al., 1988 : figs. 49, 50). Resistance to shear and compressive forces as detailed by Payne (1981) and lucidly illustrated by El-Ghazaly and Jensen (1986a) may be a necessary element in maintaining pollen grain integrity in the Poaceae. Secondly, from a taxonomic/phylogenetic standpoint, the occurrence of annulate pollen in some species of Pariana (Salgado-Labouriau et al., 1993 ) clearly indicates the need to systematically investigate this primitive bamboo genus (Soderstrom, 1974 ) of approximately 40 or more species (Hollowell, 1997 ). These bambusoid grasses affined to tribe Olyreae are found in moist, shaded habitats across Neotropical forests from Costa Rica south to Bahia, Brazil. Insect associations with Pariana inflorescences have long been noted (Davis and Richards, 1933), and entomophily recognized for the genus (Soderstrom and Calderon, 1971 ) in a family where most grasses are typically wind-pollinated. Differences of notable significance, especially at the interspecific level, in the morphology of grass pollen grains are so rare that the lack of an annulus in the pore of Pariana may be unique. Perhaps further investigation of this genus and other bambusoid grasses will reveal more non-annulate pollen to clarify their systematic position within the Gramineae, as the work of Linder (1984) and Ubera et al. (1988) has done for the Restionaceae and Plantaginaceae.

	FOOTNOTES

 
¹ The authors thank Greg Strout of the Samuel Roberts Noble Microscopy Laboratory, University of Oklahoma, for his expert assistance with the transmission electron microscopy. We also thank our reviewers for many helpful comments. Special thanks to Dr. Beth E. Hazen, Cortland, New York, for invaluable copyediting.

⁶ Author for reprint requests

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION LITERATURE CITED

 
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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (2) Citing Articles via Google Scholar Google Scholar Articles by Skvarla, J. J. Articles by Chissoe, W. F. Search for Related Content PubMed Articles by Skvarla, J. J. Articles by Chissoe, W. F. Agricola Articles by Skvarla, J. J. Articles by Chissoe, W. F.