Epidermal patterning and stomatal development in Gnetales

Stomatal development in Ephedra differs significantly from that of Gnetum and Welwitschia, more closely resembling that of other extant gymnosperms. Differences in epidermal pre-patterning broadly reflect differences in growth habit between the three genera.

A new study by Rudall and Rice in Annals of Botany looks at Epidermal patterning and stomatal development in Gnetales. The Gnetales are three families of plants that diverged in the Jurassic, before flowering plants, so they are ancient. However, just three genera have survived to the current day. That means they provide a useful group of plants if you want to examine how stomata have developed over millions of years. Dr Paula Rudall made some time to talk to Botany One about her research.

Why focus on the Gnetales for a study like this? Dr Rudall said: “Gnetales are extraordinary plants that are of considerable general interest to all botanists because they represent prehistoric relics (“living fossils”). The three extant genera (Ephedra, Gnetum and Welwitschia) are very different from each other in their morphology: Ephedra has minute scale-like leaves, Gnetum leaves have a petiole and a leaf blade, and Welwitschia, represented by a single extant species confined to the deserts of southwestern Africa, bears only a single pair of leaves throughout its life, which can be 1000 years or more.

“We embarked on this project as part of a broader study of stomatal development in land plants, partly because we realised that most studies of Gnetales stomata rely on data that is very old. For example, our study is the first since 1934 to examine stomatal development in Welwitschia, and the first to illustrate this with photomicrographs.”

Mature stomata on a leaf of Gnetum gnemon
Mature stomata on a leaf of Gnetum gnemon. Image: Rudall and Rice 2019.

The evolutionary history of Gnetales spans hundreds of millions of years, so there has been plenty of time for the plants’ stomata to diverge. Dr Rudall noted this: “Profound differences exist in early development, notably in the development of the cells located on either side of the guard cells. In Ephedra, these lateral subsidiary cells are derived from adjacent cell files, whereas in Gnetum and Welwitschia they are derived from the same cell lineage that forms the guard cells.

“The main difference between Gnetum and Welwitschia is in epidermal prepatterning, which is linear in Welwitschia, so that all the stomata are parallel with each other, but formed in quartets of expanding cells in Gnetum, so that stomata can be in either parallel or perpendicular orientation. These developmental differences are partly related to differences in organ growth.

“Studies on model organisms suggest that they are governed by different genetic factors, though this aspect remains to be evaluated in Gnetales.”

The research supports the idea that Gnetum and Welwitschia are a sister pair, and Ephedra is more distantly related. Tracking the development of stomata in Gnetales could also have applications elsewhere. Dr Rudall recently published a paper on epidermal structure in another seed-plant order, Bennettittales, which became extinct in the Cretaceous. Dr Rudall said: “Bennettites are widely considered to be close to the angiosperm stem-lineage, and stomata are important in their identification. In this paper, we search for “fossil fingerprints” for development, which is difficult (often impossible) to infer from fossils. We use our results on Gnetales to hypothesise that Gnetum and Welwitschia represent the closest living analogues to Bennettitales with respect to stomatal development.”

Further reading

Rudall, P. J., & Bateman, R. M. (2019). Leaf surface development and the plant fossil record: stomatal patterning in Bennettitales. Biological Reviews. https://doi.org/10.1111/brv.12497

Rudall, P. J., & Rice, C. L. (2019). Epidermal patterning and stomatal development in Gnetales. Annals Of Botany. https://doi.org/10.1093/aob/mcz053