What do megaspores form

Based on stronger comparative data and evidence from tetrad morphology, we reinterpret the structures observed by Gaikwad and Yadav as two adjacent embryo sacs rather than as a single tetrasporic eight-nucleate embryo sac, although the majority of ovules of T.

In ovules of Trithuria with double gametophytes, the chalazal one is usually but not always the larger of the two, although the distinction between them is not always clear Figs 9— In many ovules of T. Interestingly, similar cases of paired embryo sacs are common among other early-divergent angiosperms such as Nymphaeaceae Cook, ; and Schisandraceae Friedman et al. In Kadsura Schisandraceae , one of the two gametophytes is frequently binucleate, and passage of nuclei sometimes occurs between the two embryo sacs Friedman et al.

Otherwise, such compound embryo sacs are rare in other angiosperms; Maheshwari cited some examples, but these records apparently differ from Trithuria in that each embryo sac is reportedly derived from a different cell in a multicellular archesporium. Batygina et al. By contrast, gametophytic doubling in Trithuria apparently occurs during megasporogenesis.

Given the frequency of compound embryo sacs in early-divergent angiosperms, it is possible that species of these ancient lineages are relatively tolerant of major gametophytic teratologies.

Such a high degree of plasticity is surprising given the apparently rigorous genetic constraints and otherwise conservative organization of the angiosperm embryo sac Skinner et al. A different type of mutation presumably stabilized into the nine-nucleate embryo sac reported in Amborella Friedman, , which has no obvious homologue among other angiosperms.

Exploring the enigmatic evolutionary origin of the angiosperm embryo sac requires comparison with the condition in gymnosperms, particularly extant species, because the data on fossil gymnosperms are relatively sparse. Admittedly, such comparisons are highly speculative given the vast lacuna that separates extant gymnosperms from extant angiosperms e.

Bateman et al. In most extant gymnosperms a variable number of archegonial initials develop at the micropylar end of a polarized female gametophyte during megagametogenesis Biswas and Johri, A gymnosperm archegonial initial is therefore not homologous with an angiosperm archesporial cell reviewed by Favre-Duchartre, The origin of the Polygonum -type embryo sac was probably of major adaptive significance in angiosperms, because it allowed stabilization of triple fusion and triploid endosperm formation.

Could the Polygonum -type embryo sac be derived from fusion of two gametophytes, as we have observed in Trithuria? Several authors have plausibly postulated derivation of the angiosperm megagametophyte by fusion of two or more gymnosperm archegonia within the same megagametophyte, assuming reduction of sterile tissue of the gymnosperm megagametophyte reviewed by Favre-Duchartre, ; Rudall, Alternatively, a pair of four-celled embryo sacs could represent a step towards an eight-nucleate Polygonum-type gametophyte.

One counter-argument to this is that the innermost chalazal embryo sac has the same polarity as the supernumerary one in early-divergent angiosperms, including Trithuria , i. Such a reorientation has been described in Nuphar lutea , in which Winter and Shamrov a reported four of more than ovules containing developing embryo sacs with inverted polarity.

Assuming that morphological evolution results from changes in developmental pathways, the fusion hypothesis does not necessarily contradict the duplication hypothesis, because both hypotheses imply insertion of an additional mitosis after megaspore formation.

Such highly speculative hypotheses will become testable when more is known about the developmental genetics of embryo sac organization. The fusion hypothesis differs from formation of bisporic and tetrasporic embryo sacs, in which a single embryo sac develops from two or four megaspores.

In theory, formation of a bisporic female gametophyte would appear to be the easiest way to combine two four-celled embryo sacs, but bisporic embryo sacs are extremely rare among primitive angiosperms although rarity does not in itself negate the argument. Interestingly, the most common types of bi- and tetrasporic embryo sacs are superficially extremely similar to monosporic Polygonum -type female gametophytes i. All of these eight-nucleate types are non-homologous by developmental origin via different cell lineages, but show a high degree of similarity, which cannot be explained solely by similarity of function.

Regarding the ovular i. Most current evidence suggests that two conditions are ancestral within angiosperms: 1 the presence of two integuments bitegmy , and 2 the crassinucellate condition — the presence of micropylar parietal tissue that crucially is derived from the archespore. These conditions are prevalent among early-divergent angiosperms Winship Taylor, ; Herr, , ; Endress and Igersheim, ; Shamrov, , but there have been numerous shifts within angiosperms to both unitegmy and the tenuinucellate condition in which a hypodermal archesporial cell gives rises directly to the megasporocyte.

For example, a major shift to unitegmy occurred at the base of the asterid eudicot clade e. Young and Watson, ; Philipson, ; Albach et al. In contrast to most other authors, Shamrov a distinguished three rather than two ovule types by nucellar morphology: crassinucellate, medionucellate and tenuinucellate. He defined the tenuinucellate condition by a combination of characters, such as 1 the nucellus consists of a single dermal layer, and 2 the nucellus normally degenerates prior to fertilization.

Since Trithuria does not fits the second criterion, its ovule would be medionucellate in Shamrov's classification. The shift to unitegmy has frequently been correlated with other evolutionary transitions, especially from the crassinucellate to the tenuinucellate condition e.

Albach et al. The tenuinucellate condition in angiosperms is normally regarded as the derived state e. Herr, , and in Trithuria it is presumably a result of reduction, although subsequent divisions in the micropylar nucellus result in formation of a short nucellar beak.

Such apparently minor differences in the ontogenetic derivation of micropylar nucellar tissue whether from the archespore or the nucellus may appear trivial when applied within the angiosperms, but gains more significance in comparison with other seed plants, because in crassinucellate ovules the nucellus can be interpreted as a sporangiophore—sporangium complex Bouman, ; Herr, , in contrast to the tenuinucellate condition.

In Trithuria and other Nymphaeales e. Cabomba and Brasenia : Fig. Precocious perisperm development is not uniform in all Trithuria species examined, and is least prominent in the Indian species, T.

Perisperm is rare in eudicots, but relatively common in early-divergent angiosperms such as Piperaceae e. Perisperm is also a feature of some monocots, including Poales Rudall, , , the order in which Hydatellaceae were formerly placed. Cabombaceae ovules oriented with micropyle uppermost. A Cabomba aquatica , megaspore mother cell stage with inner integument almost closed at micropyle.

E—H Brasenia schreberi , different four-nucleate stages. Arrowheads indicate positions of other embryo sac nuclei. The multinucleate perisperm in Trithuria is unusual, although a similar condition may occur in another early-divergent angiosperm family, Piperaceae Johnson, , Maheshwari cited some monocots Hedychium and Pandanus in which the nucellar nuclei wander from cell to cell and collect together in groups, sometimes entering the embryo sac.

Conversely, we found no counterpart in Trithuria for the haustorium that grows into the perisperm after fertilization in some of its close relatives in Nymphaeales, such as Cabomba , Brasenia and Nymphaea e. Cook, ; Khanna, , ; Schneider, ; Schneider and Jeter, This will be further explored in studies of later embryo development and early seed germination.

Both conditions, with intermediates, occur in Nymphaeaceae Shamrov and Winter, ; Winter and Shamrov, a , b ; Igersheim and Endress, ; Yamada et al.

Yamada et al. Given placement of Trithuria as sister to other Nymphaeales Saarela et al. Amborella ; Endress and Igersheim, ; Igersheim and Endress, Since Nuphar is putative sister to all other Nymphaeaceae Les et al. However, in Trithuria both integuments form the micropyle; the tissues of the two integuments are closely pressed to each other and to the funicle to form a single pathway Fig. Parsimonious optimization suggests that this is a unique condition for Trithuria.

During ovule ontogeny in Trithuria , the curiously retarded development of the inner integument relative to the outer i. Endress pointed out that integument initiation is distinctly acropetal in Gnetales, compared with distinctly basipetal, or almost simultaneous, in angiosperms.

In general, miniaturization of all parts, including the ovule, makes nucellar structure much less complex in Hydatellaceae than in Nymphaeaceae. For example, Shamrov b described a complex nucellar morphology in Nuphar Nymphaeaceae ; in addition to the nucellar cap and parietal tissue, he distinguished structures that he termed a postament, podium and hypostase. The postament, a column of tissue between the chalazal side of the ovule and the embryo sac, possesses longitudinally elongated and densely cytoplamic cells, some of which degenerate when the embryo sac enlarges towards the chalazal side of the ovule, where a haustorium forms.

The postament is completely destroyed by the globular stage of embryo development. The podium is a densely cytoplamic cup-like region in the chalazal part of the nucellus. Both podium and postament cells lack starch accumulation before fertilization.

After fertilization, most podium cells accumulate tannins and their walls become lignified. Shamrov b also distinguished a disk-shaped group of cells in the chazalal region, just below the podium, which he termed a hypostase, although it is clearly non-homologous with the hypostase of some other early-divergent angiosperms, such as Acorus Rudall and Furness, Most hypostase cells are thin-walled and accumulate starch, although some central hypostase cells also accumulate tannins and develop lignified walls.

According to Shamrov's terminology, we can distinguish in Trithuria only a very small, central portion of both hypostase and podium below the perisperm. The postament is absent, corresponding to the absence of a well-developed chalazal haustorium in the embryo sac of Trithuria. Hamann et al. This character is probably also of adaptive significance. Both precocious cuticle formation and precocious perisperm formation could facilitate rapid fruit development, which is important for short-lived annuals.

Previous authors e. Hamann, have suggested that apomixis agamospermy could occur in the New Zealand species Trithuria inconspicua , because males are extremely rare, and plants consist mostly of female individuals, although embryos develop and fertile seeds are produced Hamann, Asexual reproduction is a frequent strategy of aquatic plants e.

Les, However, pollen-tube growth is common in some other species of Trithuria. For example, Gaikwad and Yadav reported pollen germination on stigmatic hairs of T. By contrast, pollen tubes were entirely absent from our material of T. Thus, we hypothesize that T. Several relatively unusual features of the Trithuria ovule, notably the four-nucleate embryo sac, copious perisperm and seed operculum, are consistent with a close relationship with Nymphaeales. Furthermore, the hood-shaped outer integument supports a close affinity with Cabombaceae.

In light of the sister-group relationship demonstrated by Saarela et al. The ovule of Trithuria is tenuinucellate, rather than crassinucellate as in most Nymphaeales, perhaps reflecting the high degree of morphological reduction in Hydatellaceae. The frequent occurrence of double megagametophytes in the same ovule, especially in Trithuria , but also in other early-divergent angiosperms, indicates considerable developmental flexibility, and could provide a clue to the evolutionary origin of the Polygonum -type of the angiosperm embryo sac, and hence the enigmatic transition from the gymnosperm to the angiosperm condition.

We thank Margaret Ramsay for growing plants of Trithuria submersa at Kew, Peter Endress for helpful discussion, and Richard Bateman for critically reading the manuscript. Google Scholar. Google Preview. Oxford University Press is a department of the University of Oxford.

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Sign In or Create an Account. Sign In. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Rudall , Paula J. E-mail p. Oxford Academic. Margarita V. Anton S. Elizabeth Bradshaw. Dennis W. Terry D. Renee E. Shrirang R. Dmitry D. Revision received:. Cite Cite Paula J. Select Format Select format. Permissions Icon Permissions. Words nearby megaspore megarectum , Megaris , megaron , megascopic , megasporangium , megaspore , megaspore mother cell , megasporocyte , megasporogenesis , megasporophyll , megass.

How to use megaspore in a sentence In Welwitschia also the megaspore is filled with prothallus-tissue, but single egg-cells take the place of archegonia. Also called: macrospore the larger of the two types of spore produced by some spore-bearing plants, which develops into the female gametophyte Compare microspore def. Derived forms of megaspore megasporic , adjective. Cytological basis for a tetraspory in Cupressus sem-pervirens L. Theoretical Applied Genetics. Emig, W. The megagametophyte of Pinus.

Engels, F. The basic anatomy of Metasequoia female gametophytes. Acta Botanica Neerlandica — Ferguson, M. Contributions to the life history of Pinus with special reference to sporogenesis, the development of gametophytes and fertilization.

Proceedings of the Washington Academy of Sciences 6: 1— Greenwood, M. Reproductive development in loblolly pine. The early development of male and female strobili in relation to the long shoot growth behavior.

Haig, D. Brood reduction in gymnosperms. Editors: M. Elgar and B. Oxford University Press, Oxford, pp. Harrison, D. Long shoot terminal bud development and the differentiation of pollen- and seed-cone buds in Pinus caribaea var. Canadian Journal of Forest Research — Hart, J. A cladistic analysis of conifers: preliminary results. Journal of Arnold Arboretum — Haupt, A.

Oogenesis and fertilization in Pinus lambertiana and P. Botanical Gazette — Konar, R. Ultrastructure, cyto- and histochemistry of female gametophyte of gymnosperms. Gamete Research 3: 67— Recent work on reproductive structures of living conifers and taxads — a review.

Botanical Review 89— Lawson, A. The gametophytes, archegonia, fertilization and the embryo of Sequoia sempervirens. Annals of Botany 1— The gametophytes and embryo of the Cupressineae with special reference to Libocedrus decurrens.

Annals of Botany — Lill, B. Ovule and seed development in Pinus radiata , postmeiotic development, fertilization and embryogeny.

Canadian Journal of Botany — Matten, L. Fine, et al.