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The Operculum in Pollen of Monocotyledons Carol A Aliso: A Journal of Systematic and Evolutionary Botany Volume 22 | Issue 1 Article 15 2006 The Operculum in Pollen of Monocotyledons Carol A. Furness Royal Botanic Gardens, Kew Paula J. Rudall Royal Botanic Gardens, Kew Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Botany Commons Recommended Citation Furness, Carol A. and Rudall, Paula J. (2006) "The Operculum in Pollen of Monocotyledons," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 22: Iss. 1, Article 15. Available at: http://scholarship.claremont.edu/aliso/vol22/iss1/15 Pollen Evolution ~9at~2gcyodan Evolution TS Excluding Poales Aliso 22, pp. 191-196 © 2006, Rancho Santa Ana Botanic Garden THE OPERCULUM IN POLLEN OF MONOCOTYLEDONS CAROL A. FURNESS 1 AND PAULA J. RUDALL Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK 1 Corresponding author ( c.furness@ rbgkew.org. uk) ABSTRACT Within monocotyledons, monosulcate pollen is the predominant type and probably represents the plesiomorphic condition, but considerable variation occurs in sulcus morphology. An operculum is an exine thickening that covers most of an aperture. Monocot opercula are usually associated with sulci, although they can occur in ulcerate apertures, as in Poaceae. There are several other aperture types closely related to the monosulcate-operculate type, and confusion occurs in the palynological literature between monosulcate-operculate, pontoperculate, disulculate, disulcate, and zona-aperturate (zonasul­ culate or zonasulcate) pollen. Transmission electron microscopy (TEM) was used to determine the distribution of the thick apertural intine and to accurately identify these aperture types. Operculate pollen most frequently was present in Asparagales (particularly Agavaceae, Doryanthaceae, lridaceae, and Tecophilaeaceae), Liliales (particularly Liliaceae, Melanthiaceae, and Uvulariaceae), and relatively infrequently among commelinid monocots, except for some Arecaceae, Dasypogonaceae, and Poales. Thus, we conclude that opercula have probably evolved several times independently within monocots, particularly in taxa from dry or seasonally dry habitats, and that this adaptation may be related to their function in protecting the aperture. Two transformation series of related aperture types are pro­ posed, one of which involves monosulcate-operculate pollen, although further testing will be required. Key words: aperture, commelinids, lilioids, monocotyledons, monosulcate, operculum, pollen, trans- formation series. INTRODUCTION pontoperculate, disulculate, disulcate, zonasulculate, and zonasulcate (or meridionosulcate ). The monosulcate condition is the most common aperture type found in monocotyledons and is probably the plesiom­ DISTRIBUTION OF MONOSULCATE-OPERCULATE orphic state (Furness and Rudall 1999). However, there is POLLEN IN MONOCOTYLEDONS considerable diversity among monosulcate apertures. Sulci may be diffuse, extended, insulate (with scattered islands of Operculate pollen is entirely absent from basal monocots, exine), operculate, or with banded opercula (Halbritter and but relatively common in lilioid and commelinid monocots Hesse 1993). As Halbritter and Hesse (1993) pointed out, it (Furness and Rudall 2003). Pollen of Acarus L. (Acoraceae), is necessary to examine unacetolysed pollen in a turgid state which is the basal monocot in most recent molecular anal­ to accurately observe details of the sulcus, since acetolysis yses (e.g., Chase et a!. 2000), is monosulcate without an causes the collapse of thin-walled monocot pollen and the operculum (Grayum 1992; Rudall and Furness 1997). Oper­ removal of structures associated with the sulcus, including culate pollen appears to be entirely absent from Alismatales. opercula. Many alismatids are inaperturate or have weakly defined ap­ Here we review the distribution of operculate pollen in ertures, or are porate with granular or spiny pore membranes monocots in a systematic context. In the palynological lit­ (Chanda et al. 1988; Grayum 1992; El-Ghazaly and Rowley erature, the term "operculum" refers to an exinous thick­ 1999; Furness and Rudall 1999, 2000). Tofieldia Huds. (To­ ening which covers a large part of an aperture (e.g., Punt et fieldiaceae) is disulcate (Huynh 1976; Takahashi and Ka­ al. 1994). The operculum may be fused to the surrounding wano 1989; Diaz Lifante et al. 1990) and zona-aperturate exine at both ends; apertures with this type of structure are pollen occurs in some Araceae (Grayum 1992; Hesse et al. termed "pontoperculate." Since the pontoperculum effec­ 200 I ; Zetter et al. 200 1). tively divides the sulcus into two, when viewed using scan­ ning electron microscopy (SEM) such an aperture may be Lilioid Monocots indistinguishable from the disulculate aperture type. Simi­ There are unconfirmed reports of monosulcate-operculate larly, confusion may arise between monosulcate-operculate pollen in Barbacenia Vand. (Velloziaceae-Pandanales) and and zona-aperturate (zonasulcate or zonasulculate) apertures. Metanarthecium Maxim. (Nartheciaceae-Dioscoreales) The orientation of monocot pollen apertures cannot be de­ (Furness and Rudall 2003), although TEM sections are re­ termined without reference to the tetrad stage of pollen de­ quired to confirm the position of the thickened apertural in­ velopment, and examination of sections of fresh pollen using tine. Within Liliales, operculate pollen is common in Al­ TEM is also necessary in order to determine the position of stroemeriaceae, Liliaceae, Melanthiaceae, and Uvulariaceae the thickened apertural intine and thus the type of aperture. (Furness and Rudall 2003; Fig. 1-4), and is apparently a There is therefore much confusion in the pollen literature synapomorphy for Melanthieae-Melanthiaceae (Colosante about the application of the terms monosulcate-operculate, and Rudall 2000; Rudall et a!. 2000). 192 F urness and RudaJI ALISO Fig. 1- 12.-0percul ate and related pollen apertures in monocots.-1. Erythronium elegans P. C. Hammond & K. L. Chambers (Li liaceae­ Lili ales), monosul cate-opercul ate poiJ en (SEM ).-2-4. Zigadenus venenosus S. Wats. (Melanthiaceae-Liliales).-2. Monosulcate-operculate poll en (SEM).-3. Detail of the sul cus with an operculum with layers of thick in ti ne, including a channell ed layer, beneath (TEM).--4. Section showing the operculum, thick apertural intine and non-apertural exine with a prominent foot layer.-5. Iris reticulata M. Bieb. (lridoideae-Iridaceae-Asparagales), zona-aperturate (zonasulculate) poll en (SEM).-6--7. Gladiolus tristis L. (Ixioideae-[ridaceae-Aspara­ gales).-6. Detail of the sul cus with two exine bands with thi ck intine beneath (TEM).- 7. Monosul cate-operculate poll en with a two­ banded sul cus (SEM).-8-9. Aristea ecklonii Baker (Ni veni oideae-Iridaceae-Asparagales).-8. Zona-aperturate poll en (SEM).-9. Tetrad of zona-aperturate (zonasulcate) grains (SEM).-10. Odontostomum hartwegii Torr. (Tecophilaeaceae-AsparagaJes), monosul cate-opercul ate VOLUME 22 The Operculum in Monocot Pollen 193 Within Asparagales, operculate pollen is relatively rare in Commelinid Monocots the higher asparagoid clade, but occurs in representatives of several families of the lower asparagoid grade, including Ir­ Opercula are common in Poales, in which they character­ ize Anarthriaceae, Ecdeiocoleaceae, and Poaceae, which all idaceae (Fig. 5-9), Orchidaceae, Hypoxidaceae, Tecophilae­ have ulcerate apertures (Linder and Ferguson 1985; Fig. 12). aceae (Fig. 10, 11), and Doryanthaceae (Furness and Rudall The operculum in Poaceae often becomes detached in ace­ 2003). Nair and Sharma (1965) also reported monosulcate­ tolysis. Operculate pollen also occurs in some species of operculate pollen in Dianella Lam. (Hemerocallidaceae), al­ Tillandsia L. (Bromeliaceae-Poales: Halbritter 1992) and though we found only trichotomosulcate pollen in this genus Xyris (Xyridaceae-Poales: Rudall and Sajo 1999). Extended (Rudall eta!. 1997). Monosulcate-operculate pollen is a syn­ sulcate, zona-aperturate, and disulculate apertures occur in apomorphy for six genera of Tecophilaeaceae (Simpson Rapateaceae (Carlquist 1961). Opercula are absent from 1985b; Fig. 10, 11). Pollen apertures are diverse within Iri­ most other commelinids apart from Calectasia R. Br. (Da­ daceae, including highly variable apertures within the genus sypogonaceae: Chanda and Ghosh 1976), and Chamaerops Aristea Sol. ex Aiton (Nivenioideae: Goldblatt and Le L., possibly Iriartella H. A. Wend!., and Sclerosperma G. Thomas 1992b, Goldblatt et a!. 2004; Fig. 8, 9), and oper­ Mann & H. A. Wend!. (Arecaceae: Furness and Rudall2003; culate pollen occurs in three subfamilies. For example, in Harley and Dransfield 2003). In many Commelinales the Iridoideae there appears to be a gradation from monosulcate­ pollen sulci have scattered exine elements on the surface: operculate (e.g., Hermodactylus Mill.) to zonasulculate (Iris granules, scabrae, verrucae, or insulae (Poole and Hunt danfordiae (Baker) Boiss., I. reticulata M. Bieb.: Goldblatt 1980; Simpson 1983, 1985a, 1987). Pontederiaceae (Com­ and Le Thomas 1992a; Furness and Rudall 2003; Fig. 5). melinales) have disulculate pollen (Simpson 1987; Ressayre Many members of Iridaceae subfamily Ixioideae have pollen 2001). with an operculum composed of two separate bands of exine which is probably synapomorphic for the subfamily, al­ DISCUSSION though a variety of other aperture types also occur including monosulcate with one-banded opercula or with insulae, and Monosulcate-operculate pollen is primarily
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