What is the difference between cycads gymnosperms and angiosperms

Here, we used 31, nucleotide sites obtained from orthologous genes across a wide taxonomic sampling that includes representatives of most conifers, cycads, ginkgo, and many angiosperms with a sequenced genome. Our results suggest that angiosperms and gymnosperms differ considerably in their rates of molecular evolution per unit time, with gymnosperm rates being, on average, seven times lower than angiosperm species.

Longer generation times and larger genome sizes are some of the factors explaining the slow rates of molecular evolution found in gymnosperms. In contrast to their slow rates of molecular evolution, gymnosperms possess higher substitution rate ratios than angiosperm taxa. First brought over to the U.

The species is also widely used in the ethnomedicinal trade. Vessel-bearing gymnosperms, but apparently the vessels are convergent with angiosperms. Molecular systematic evidence is suggesting these are closely related if not imbedded in conifers, rather than close to angiosperms as usually assumed.

Three families each with a single genus, none of which are found in Wisconsin. Gnetum : 30 species of trees and climbing vines, with large leathery leaves that resemble dicots Ephedra or mormon tea with about 35 species, profusely branched shrubs with small scalelike leaves Welwitschia is one of the most bizarre organisms - most of the plant is buried in sandy soil of the coastal desert of southwestern Africa. The exposed part consists of a massive woody, concave disk that produces only two strap-shaped leaves with the cone bearing branches arising from meristematic tissue on the margin of disk.

Known from the late Carboniferous, some million years ago. Now dominant only in boreal forests and often found in higher elevations, but as a group they also do well in dry environments.

Pines, spruces, and firs are of great commercial value. The tallest coastal redwood , most massive giant sequoia , and oldest bristle cone pine are members of this group. All 3 families and 13 species of gymnosperms found in Wisconsin belong to this group:.

Cupressaceae - cypress family. Foliage leaves needlelike or scalelike, alternate opposite or whorled, persistent on branches. Cone scale valvate or imbricate; the bract-scales are intimately fused for most of their common length, seeds per scale. Heartwood of many species is resistant to termite damages and fungal decay and is widely used in contact with soil. No members of the family attain dominance over immense geographic range, but they can achieve considerable local and regional prominence - eg.

The cedars belong to this group and wooden pencils are made form incense cedar. Thuja occidentalis - eastern arborvitae, northern white cedar. Leaves opposite in four ranks. Leaves heteromorphic the leaves on larger branches with sharp erect, free apices to 2 mm; those on flatten lateral branchlets crowded , appressed, scale-like. Small hard cones.

Seed cones closed for many years or until opened by fire, scales persistent. Winter deer food. Juniperus communis subsp. Leaves closely appressed to divergent and scale like; can be dimorphic with scale and awl shaped leaves.

Dieocious, sometimes monoecious. The cone fleshy and berry like and remaining closed. Can be used to flavor gin. Taxaceae - yew family. Taxus canadensis - American yew, ground hemlock. No cones, single seed in fleshy aril, but seeds still naked.

Heavily browsed by deer. Taxol which is produced from the bark of western yew, T. Florin, ; Pant and Mehra, , and variation within Zamiaceae is hitherto unknown.

In his description of the stomata of Dioon edule , Florin identified two different cell types in the stomatal apparatus: Nebenzellen neighbour cells, directly flanking the guard cells and Kranzzellen crown cells, at the poles of the guard cells, as well as the three layers of cells overlying the Nebenzellen. Greguss instead translated Nebenzellen as neighbour cells and Kranzzellen as accessory cells. To avoid confusion about the use of subsidiary cells, we follow the nomenclature from Coiro et al.

The material examined is listed in Table 1. Seeds of four species Table 1 were germinated on a perlite substrate and transferred to pumice after the emergence of the first prophyll before sampling the first developing leaflets Fig. Leaflet structure differs between species examined Table 2 ; Fig. In all species, leaflets were sampled at different developmental stages and immediately fixed in formalin—acetic acid—alcohol.

The embedded specimens were sectioned on a Microm HM rotary microtome using a conventional microtome knife D. Sections of mature leaflets of D. Light and fluorescence micrographs were obtained using a Zeiss Axioscope using a brightfield filter. PS-PI-stained samples of B. Excitation was obtained using either nm excitation and a DAPI emission filter or nm excitation and a PI emission filter. Each stoma has two to five subsidiary cells Fig. Mature subsidiary cells have a thicker cuticle than surrounding pavement cells and contain denser cytoplasm.

Mature guard cells contact the subsidiary cells on their dorsal wall and contact the specialized cells of the substomatal apparatus on their inner wall Fig.

Guard cells show differentiation of the cell wall potentially lignin or pectin impregnation on the dorsal and ventral sides of the cytoplasm Fig. Bowenia spectabilis. Transverse section of stomatal complex of an adult leaflet stained with pseudo-Schiff-propidium iodide observed using confocal laser scanning microscopy and imaged using A UV excitation, B propidium iodide excitation. C Fluorescence micrograph of isolated cuticle from adult leaflet stained with Auramine O, showing mature stomata in axial cell files.

D Fluorescence micrograph of isodiametric protodermal cells in developing leaflet. E—G Development of stomatal complexes at different stages. Early in development, the protodermal cells are isodiametric Fig. The GMCs differentiate directly from enlarged protodermal cells Fig.

Subsidiary precursor cells differentiate from the cell files adjacent to the GMCs, and sometimes undergo oblique divisions. Early development was observed in Ceratozamia hildae Fig.

Protodermal cells undergo both longitudinal and perpendicular divisions, resulting in a squared quartet arrangement Fig. The GMCs are isodiametric and originate by direct enlargement of one of the protodermal cells Fig. A Early development showing squared quartet arrangement of protodermal cells. B Slightly later stage, indicating protodermal cell enlarging to form a guard-mother cell GMC. C, D Tangential sections of developing leaflets showing developing stomata in an intercostal stomatal band, all similarly orientated in axial cell files along the leaflet axis.

Crystals are present in cells over veins in the slightly later stage in D. E, F Transverse sections of leaflets showing stomata; neighbour cells elongating periclinally in E and divided in F. Later development was observed in Dioon Fig.

Stomata develop in irregular cell files in the intercostal regions, resulting in a closely spaced arrangement with the apertures orientated parallel to the leaflet axis Fig. Subsidiary cells develop from axially elongated neighbour cells, which divide obliquely leading to distal encircling cells Fig. In the mature stomatal apparatus, three encircling cells with thick cell walls are placed distally to the subsidiary cells, which have a thinner wall than other pavement cells.

The subsidiary cells contact the dorsal outer wall of the guard cells and the guard cells are enclosed in a stomatal pit. In Macrozamia communis Fig. GMCs are oval or square and share the same lineage as one of the polar cells, which is therefore mesogenous Fig.

Other subsidiary cells originate from neighbour cells Fig. Two neighbour cells can divide further to give rise to three to five encircling cells; further divisions in the lateral neighbour cells result in two rings of proximal subsidiary and distal encircling cells. During development, the neighbour cells also elongate distally, resulting in a stomatal pit Fig. Macrozamia communis , developing leaflets imaged using A differential interference contrast, and B, D—H fluorescence micrography.

A, B GMCs in axial cell files. F—H Stomatal development in transverse section at successive stages. In Stangeria eriopus Fig. GMC differentiation commences early in leaflet differentiation and continues throughout leaf development, resulting in stomatal complexes at different developmental stages in close proximity to each other Fig.

Division and differentiation of new GMCs continues until late in leaflet differentiation, resulting in intercostal axial rows of stomata. Early-formed stomata are mostly axially orientated, but later-developing stomata are often randomly orientated Fig.

Subsidiary cells are formed from neighbour cells. They undergo divisions parallel to the margin of the guard cells, resulting in subsidiary cells Fig. Pavement epidermal cells often have slightly sinuous walls in surface view.

Subsidiary cells differ from pavement cells in their shape; some also maintain a nucleus and cytoplasm and have a slightly thicker cuticle Fig. Crystals are often present in the epidermal cells, often in the polar cell and encircling cells Fig. Mature guard cells are flush with the surface; they have a thickened cell wall both dorsally and ventrally; and they contact the subsidiary cells and some mesophyll cells on their dorsal wall Fig.

Stangeria eriopus. A Paradermal view of mature epidermis showing stoma with guard cells containing cytoplasm and nuclei; encircling subsidiary cells also with active nuclei. Calcium oxalate crystals present in surrounding intercostal epidermal cells. B Transverse section of stomatal complex showing guard cells with thickened cell walls containing lignin—pectin deposits, and encircling cells with calcium oxalate crystals.

C—F Fluorescence and differential interference contrast images of cleared leaflets showing stomatal development. C Protodermal cells interspersed with both GMCs and stomata. D Slightly later stage, with guard cells and a GMC undergoing division.

E Leaf clearing showing both differentiated and developing stomata in intercostal regions, most similarly axially orientated. Costal region in different focal plane with trichomes hairs.

F Later stage showing similarly orientated differentiated stomata; some smaller stomata in different orientation. In Zamia Fig. Protodermal cells are angular and isodiametric Fig. GMCs are angular in surface view Fig. Subsidiary cells develop from cells flanking the GMC. Later in development, stomata are orientated parallel to the leaflet axis Fig.

Neighbour cells undergo divisions, resulting in subsidiary cells. Subsidiary cells also elongate distally to form a stomatal pit Fig. A Protodermal cells. B Early stage with GMCs undergoing division, arranged in axially orientated cell files. C Surface view showing stomatal openings surrounded by encircling cells. D Young stoma with dividing lateral subsidiary cells.

E Mature stoma with encircling cells and wall thickenings on guard cells. F, G Transverse sections showing successive stages of maturing stomata with guard cells already differentiated; in G the guard cells are sunken due to enlargement of the encircling subsidiary cells. Our investigation of stomatal and epidermal development and stomatal anatomy in six of the nine genera of Zamiaceae has highlighted traits shared with other gymnosperm groups as well as potentially synapomorphic traits of the cycads such as the presence of encircling cells and sunken stomata.

It has revealed a clear difference between the developmental trajectories of cycads and Bennettitales. The anatomy and consistent presence of subsidiary cells opens the possibility of investigating the functional role of the stomatal morphology of cycads. Moreover, we show an unexpected degree of variation between subclades in the family, potentially connected to differences in whole leaflet development, and validate hypothesis of convergent evolution of the stomatal morphology in the Stangeriaceae, while strengthening the relationship between Stangeria and the Ceratozamia — Zamia — Microcyas clade.

Our comparative observations confirm those of earlier researchers e. Florin, , in demonstrating the presence of a more or less distinct ring of subsidiary cells and polar cells in most extant Zamiaceae Fig. A similar arrangement also occurs in the sister genus Cycas Fig. The stomatal apparatus of Bowenia differs in lacking encircling cells in a mature stomatal complex due to the lack of divisions of the lateral neighbour cells Coiro and Pott, Based on mature leaflet anatomy, Coiro et al.

Our study shows that axial elongation is synchronous with GMC division in Bowenia , and that the neighbour cells undergo divisions in all species examined except B. In most cycads, mature stomata are predominantly axially orientated with their apertures more or less parallel to the long axis of the leaflet with some exceptions; see below and Table 3.

This pattern resembles the condition in most other land plants e. GMCs are more or less square in all species examined and no asymmetric divisions were observed, indicating the absence of amplifying divisions that would lead to random stomatal orientation.

A consistent axial orientation indicates linear epidermal expansion and an absence of amplifying divisions. Summary of stomatal patterning and development in the ten extant cycad genera. Although highly speculative, the consistent presence in cycad stomata of subsidiary cells, often with persistent cytoplasm and nucleus unlike the almost completely sclerified pavement cells , could indicate a physiological role.

A physiological connection between the guard cells and subsidiary cells is well known in grasses, where the lateral subsidiary cells are involved in the mechanisms of stomatal opening via exchange of osmolytes with the guard cells Franks and Farquhar, ; Raissig et al.

Some authors have reported a relatively rapid mechanism of closure and opening and high water efficiency in the Cycadales Haworth et al. On the other hand, encircling cells and polar cells are almost completely sclerified at maturity in all genera except Stangeria , in which they contain oxalate crystals. Mature stomata are sunken in stomatal pits in all species examined except B. As we have demonstrated, and Florin also demonstrated in D.

This convergent morphology could be linked to leaflet economics in these two genera. Both genera share a similar habit, with subterranean stems, few large leaves and growth mainly in shaded areas, although both Bowenia and Stangeria can also grow in sunny habitats. The sunken guard cells of most cycads have traditionally been associated with adaptation to aridity.

In some genera, such as Dioon Barone Lumaga et al. However, it is unclear whether the depth of the pits is an adaptation to avoid water loss, since there is little direct evidence either from models Roth-Nebelsick et al. Thicker leaves, which are potentially adaptive in arid climates, would necessitate deeper pits, in a similar fashion to the evolution of crypts in sclerophyllous taxa Hassiotou et al.

Bowenia and Stangeria have among the thinnest leaves in the Zamiaceae, and thus lack stomatal pits. Our comparative observations show that in Zamiaceae the stomatal subsidiary cells are derived from protodermal cells adjacent to the GMC, rather than from the sister cell to the GMC.

In a few cases where epidermal cell elongation precedes GMC formation, we did observe that one of the polar cells is mesogenous, for example in M. Indeed, as Rudall and Bateman noted, in narrow linear leaves with axially elongated cell files, the GMC is invariably sister to one of the polar neighbour cells, as also observed in conifers Pinus : Johnson and Riding, and monocots Rudall et al.

However, in most cycad species the protodermal cells are isodiametric and remain relatively short. This perigenous pattern of development agrees with the haplocheilic definition of Florin, and matches studies of early stomatal development in Cycas , Ceratozamia and Dioon Florin, , ; Pant and Mehra, ; Barone Lumaga et al.