Observations on ptyxis, phenology, and trichomes in the Cycadales and their systematic implications
Stevenson D.W. (1981)
Dennis W. Stevenson,
American Journal of Botany 68: 1104–1114 – https://doi.org/10.2307/2442720 –
Haworth M., Fitzgerald A., McElwain J. C. (2011)
Australian Journal of Botany 59: 629–638 – DOI: 10.1071/BT11009 –
The stomatal density (SD) and index (SI) of fossil plants are widely used in reconstructing palaeo-atmospheric CO2 concentration (palaeo-[CO2]). These stomatal reconstructions depend on the inverse relationship between atmospheric CO2 concentration ([CO2]) and SD and/or SI. Atmospheric oxygen concentration ([O2]) has also varied throughout earth history, influencing photosynthesis via the atmospheric CO2 : O2 ratio, and possibly affecting both SD and SI.
Cycads formed a major component of Mesozoic floras, and may serve as suitable proxies of palaeo-[CO2]. However, little is known regarding SD and SI responses of modern cycads to [CO2] and [O2]. SD, SI and pore length were measured in six cycad species (Cycas revoluta, Dioon merolae, Lepidozamia hopei, Lepidozamia peroffskyana, Macrozamia miquelii and Zamia integrifolia) grown under elevated [CO2] (1500 ppm) and subambient [O2] (13.0%) in combination and separately, and compared with SD, SI and pore length under control atmospheric conditions of 380 ppm [CO2] and 20.9% [O2].
The cycad species analysed showed no significant SD, SI or pore-length response to changes in [CO2] or [O2].
Coiro M., Pott C. (2017)
BMC Evolutionary Biology 17: 97 – https://doi.org/10.1186/s12862-017-0943-x –
Even if they are considered the quintessential “living fossils”, the fossil record of the extant genera of the Cycadales is quite poor, and only extends as far back as the Cenozoic. This lack of data represents a huge hindrance for the reconstruction of the recent history of this important group. Among extant genera, Bowenia (or cuticles resembling those of extant Bowenia) has been recorded in sediments from the Late Cretaceous and the Eocene of Australia, but its phylogenetic placement and the inference from molecular dating still imply a long ghost lineage for this genus.
We re-examine the fossil foliage Almargemia incrassata from the Lower Cretaceous Anfiteatro de Ticó Formation in Patagonia, Argentina, in the light of a comparative cuticular analysis of extant Zamiaceae. We identify important differences with the other member of the genus, viz. A. dentata, and bring to light some interesting characters shared exclusively between A. incrassata and extant Bowenia. We interpret our results to necessitate the erection of the new genus Eobowenia to accommodate the fossil leaf earlier assigned as Almargemia incrassata. We then perfom phylogenetic analyses, including the first combined morphological and molecular analysis of the Cycadales, that indicate that the newly erected genus could be related to extant Bowenia.
Eobowenia incrassata could represent an important clue for the understanding of evolution and biogeography of the extant genus Bowenia, as the presence of Eobowenia in Patagonia is yet another piece of the biogeographic puzzle that links southern South America with Australasia.
Coiro M., Jelmini N., Neuenschwander H., Calonje M. A., Vovides A. P., Mickle J. E., Barone Lumaga M. R. (2020)
Mario Coiro, Nicola Jelmini, Hanna Neuenschwander, Calonje Michael A., Vovides Andrew P., MickleJ. E., Maria Rosaria Barone Lumaga,
International Journal of Plant Sciences 181(7): 697-715 – DOI: 10.1086/709372 –
Premise of the Research:
The morphology of leaves is shaped by both historical and current selection acting on constrained developmental systems. For this reason, the phylogenetic signal of these characters is usually overlooked.
We investigate morphology of the leaflets of all genera of the Zamiaceae using multiple microscopical techniques to test whether leaf characters present a phylogenetic signal, and whether they are useful to define clades at a suprageneric level.
Our investigation shows that most genera are quite uniform in their leaflet anatomy, with the largest genera (Zamia, Encephalartos) presenting the highest degree of variation. Using both Bayesian and Parsimony methods on two different molecular scaffolds, we are able to show that leaflet anatomy has a strong phylogenetic signal in the Zamiaceae, and that many clades retrieved by molecular analyses present potential synapomorphies in their leaflet anatomy. Particularly, the placement of Stangeria in a clade with Zamia and Microcycas is supported by the presence of both an adaxial and abaxial girder sclerenchyma and the absence of sclerified hypodermis. The placement of Stangeria as sister to Bowenia, on the other hand, is not supported by our analysis. Instead, our results put into question the homology of the similar guard cell morphology in the two genera.
We show that leaflet anatomy has a substantial amount of phylogenetic signal in the Zamiaceae, supporting relationships that are not supported by general morphology. Therefore, anatomical investigation represent a promising avenue for plant systematists.
Coiro M., Barone Lumaga M. R., Rudall P. J. (2021)
Annals of Botany 128(5): 577–588 – https://doi-org.eres.qnl.qa/10.1093/aob/mcab095 –
Background and Aims
The gymnosperm order Cycadales is pivotal to our understanding of seed-plant phylogeny because of its phylogenetic placement close to the root node of extant spermatophytes and its combination of both derived and plesiomorphic character states. Although widely considered a ‘living fossil’ group, extant cycads display a high degree of morphological and anatomical variation. We investigate stomatal development in Zamiaceae to evaluate variation within the order and homologies between cycads and other seed plants.
Leaflets of seven species across five genera representing all major clades of Zamiaceae were examined at various stages of development using light microscopy and confocal microscopy.
All genera examined have lateral subsidiary cells of perigenous origin that differ from other pavement cells in mature leaflets and could have a role in stomatal physiology. Early epidermal patterning in a ‘quartet’ arrangement occurs in Ceratozamia, Zamia and Stangeria. Distal encircling cells, which are sclerified at maturity, are present in all genera except Bowenia, which shows relatively rapid elongation and differentiation of the pavement cells during leaflet development.
Stomatal structure and development in Zamiaceae highlights some traits that are plesiomorphic in seed plants, including the presence of perigenous encircling subsidiary cells, and reveals a clear difference between the developmental trajectories of cycads and Bennettitales. Our study also shows an unexpected degree of variation among subclades in the family, potentially linked to differences in leaflet development and suggesting convergent evolution in cycads.
by Barone Lumaga M. R., Coiro M., Erdei B., Mickle J. (2012)
In Conference Botany 2012, Columbus, Ohio, USA, July 7–11, Abstract ID: 306 –
The genus Ceratozamia (Cycadales; Zamiaceae) was classically divided into two groups based on gross leaf morphology, but recent molecular phylogenetic analyses has identified three clades. On a larger scale, Ceratozamia appears closely related to Stangeria and to the neotropical genera Microcycas and Zamia. Whole leaf and isolated cuticle specimens from eight Ceratozamia species (C. euryphyllidia, C. hildae, C. kuesteriana, C. latifolia, C. matudae, C. mexicana, C. miqueliana, C. norstogii), Stangeria eriopus, Microcycas calocoma, and Zamia amblyphyllidia were examined using SEM for features of inner and external surfaces.
Samples were collected from the middle region of leaflets of mature leaves of greenhouse-grown plants. For external surfaces, samples were air dried or fixed in FAA (10:5:50) and critical-point dried. For the inner cuticle surface, isolated cuticles were obtained using 20% CrO3.
Characteristics in common to these species include hypostomy with the exception of S. eriopus showing stomata also on the adaxial side (near the midrib), occasional presence of hair scars, adaxial epidermal cells longitudinally elongated and arranged in rows, and smooth adaxial exterior cuticle (with the exception of S. eriopus showing irregular ridges).
Stomatal complexes are not contiguous and are oriented parallel to the leaflet axis (with the exception of S. eriopus showing randomly oriented stomata), and are of the diperigenous to tetraperiginous type in Ceratozamia species, M. calocoma and Z. amblyphyllidia, with S. eriopus showing stomata of polyperigenous type.
Lightly granulate epicuticular wax borders stomatal pits in M. calocoma and Z. paucijuga, and it is granulate in C. matudae and C. robusta.
Epicuticular wax occuring as granules to ridges borders the pits in C. euryphyllidia, C. miqueliana, C. norstogii and as reticulate ridges in C. hildae, C. kuesteriana, C. latifolia, C. mexicana.
The distribution of different kinds of epicuticular waxes in Ceratozamia species closely reflect the phylogenetic relationships that has emerged from molecular data. The presence of granulated wax in M. calocoma and Z. amblyphyllidia suggests that this character is ancestral in Ceratozamia.
The closeness of S. eriopus to the other taxa is not supported by cuticular micromorphology. The close correspondence between molecular and micromorphogical data in Ceratozamia confirms that micromorphology can provide useful data for rapidly and efficiently assessing systematics in other cycad taxa.
by Barone Lumaga M. R., Moretti A., De Luca P. (1999)
in Plant Biosystems 133 (1): 47-53 – https://doi.org/10.1080/11263509909381531 –
Light and scanning electron microscopy were utilised to study stoma and cuticle morphology whereas transmission electron microscopy was used to observe plastid ultrastructure in Ceratozamia kuesteriana Regel (Zamiaceae).
Results show that in C. kuesteriana a diperigenous‐type stoma (or a derivation of a diperigenous type) occurs and that protein crystalloids and prolamellar bodies are simultaneously present in the chloroplast.
Fig 1. Dimensions taken from inner cuticle stomatal flange and polar cell flanges of Dioon: A, length and width of stomatal flange; B, length of polar cell flanges.
by Vovides A. P., Clugston J. A. R., Gutiérrez-Ortega J. S., Perez Farrera M. A., Sanchez Tinoco M. Y., Galicia S. (2017)
in Flora – Morphology Distribution Functional Ecology of Plants 239: 20–44 – DOI 10.1016/j.flora.2017.11.002 –
by Papadopoulos S. (1928)
in Botanical Gazette 85(1): 30–45 –
by Mickle J. M., Barone Lumaga M. R., Moretti A., De Luca P. (2011)
in Plant Biosystems 145: 191–201 – https://doi.org/10.1080/11263504.2010.547675 –
A scanning electron microscopy (SEM) study of Cycas cuticle characteristics was undertaken in order to expand our knowledge of microscopic characters not observable under light microscopy and to clarify unresolved affinitites among some species within the genus.
Whole leaf and isolated cuticle specimens from the middle region of leaflets of greenhouse-grown plants of Cycas revoluta, Cycas rumphii, Cycas circinalis, Cycas media, and Cycas normanbyana were examined using SEM for interior and exterior features.
Characteristics in common include hypostomy, hair bases on abaxial and adaxial surfaces, adaxial cells randomly arranged, adaxial exterior cuticle smooth, and stomata sunken to various degrees but stomatal pit always formed by two layers of epidermal cells.
Stomatal complex is of the polyperigenous type.
Stomata randomly dispersed and oriented, and except C. revoluta, are not contiguous.
Stomata deeply sunken in C. revoluta, intermediate in C. rumphii and C. normanbyana, and less sunken in C. circinalis and C. media.
Aperture between guard cells extends the entire stomatal length in C. rumphii and C. normanbyana, ∼80% in C. circinalis and C. media, and ∼50% in C. revoluta.
Cuticular features of C. revoluta show the greatest difference from the other species in complex relief of exterior cuticle and interior cuticular structure of subsidiary cells; C. media and C. circinalis show close similarity to each other and their stomatal complex dimensions fall within the same unique cluster using principal component analysis under normalized variables.
C. normanbyana and C. rumphii show the most similarity to each other in cuticular micromorphology. Stomatal complex dimensions of these two species fall into a second cluster that also includes C. revoluta. These data contrast with current taxonomy placing C. normanbyanasynonymous to C. media.