Influence of stomatal rings on movements of guard cells

Anatoly A. Pautov, Svetlana M. Bauer, Olga V. Ivanova, Elena G. Krylova, Olga V. Yakovleva, Yulia O. Sapach, Irina A. Pautova

Research output


Cuticular folds have been described for nearly all above-ground surfaces of plants including their leaf epidermis (Koch et al., 2009). They are often present on the stomatal complex cells. The guard cells of some plants bear folds of cuticle, so called stomatal rings. These rings can be located either immediately on guard cell walls around the outer ledges (marginal stomatal rings), or on the outer ledges themselves (rings of ledges). Light, scanning, and transmission electron microscopy were used to study the stomata of the leaf epidermis in Viburnum suspensum Lindl. (Caprifoliaceae), Lauro-cerasus officinalis M. Roem. (Rosaceae), Sarcococca humilis Stapf (Buxaceae), Artocarpus heterophyllus Lam. (Moraceae), Exbucklandia populnea (R.Br. ex Griff.) R.W. Brown (Hamamelidaceae), Carissa spectabilis (Sond.) Pichon, Acokanthera oblongifolia (Hochst.) Codd and Acokanthera oppsitifolia (Lam.) Codd (Apocynaceae), which have stomatal rings. All plant material was collected in the Botanical gardens of St. Petersburg State University and Komarov Botanical Institute (St. Petersburg, Russia).
All studied species are represented by evergreen plants with dense or leathery leaves. Their mesophyll is differentiated into palisade and spongy tissues and the latter makes up the bulk of it. The leaves are hypostomatic. The stomatal complexes are anomocytic in L. officinalis and A. heterophyllus, mainly laterocytic in V. suspensum and S. humilis, mainly cyclocytic in E. populnea, C. spectabilis, A. oblongifolia and A. oppositifolia. The guard cells of all studied species are located on the subsidiary or neighbouring cells.
The stomata of V. suspensum, L. officinalis, A. heterophyllus, S. humilis have marginal stomatal rings. These rings are usually formed by cuticular folds and pectin-like material which fills the subcuticular space of the folds. The guard cell walls lying under marginal stomatal rings can be deformed. It was discovered that the marginal stomatal ring arises in the early stages of stoma development. After its arising, the ring stretches together with the growing stoma. The squeeze of stoma by ring can happen if the stretching of stomatal ring ceases before the stoma growth is completed. The stomata of E. populnea, C. spectabilis, A. oblongifolia and A. oppositifolia have rings of ledges. They are located on the hypertrophycally developed outer ledges. These rings are formed exclusively by the cuticle.
To elucidate the role of the rings, we have applied dynamic modelling using the finite-element method (FEM), also called finite element analysis (FEA) (Basov, 2005; Madenci, Guven, 2006). The data on the shape of the guard cells, uneven thickness of their walls, localization and the relative sizes of stomatal ledges and rings were exactly reproduced during model stomata construction. We have taken the approach to the studying of stomatal mechanics, according to which the wall material of the guard cells is isotropic, homogeneous and follows Hooke’s law (Sharpe et al., 1987). The Poisson’s ratio values of the cell walls are generally estimated to range from 0.45 to 0.5 (Fung, 1993; Braybrook, 2015). In our computations, it was assumed that the Poisson’s ratio was 0.48. The turgor pressure was simulated by creating the load distributed on the inner surface of the guard cells.
The dynamic modelling has shown that the marginal stomatal rings are able to influence the movements of guard cells located on the subsidiary cells. The turgid guard cells which have no outer ledges and marginal stomatal rings bulge above the leaf surface. The wide opening pore between such guard cells moves in the same direction and rises above the leaf surface as well. The influence of marginal rings on stomatal movements depends on the mechanical characteristics of the rings, namely on their rigidity and squeezing of stoma by them. According to modelling results, the formation of rigid rings or rings squeezing stoma in addition to rigid ledges leads to deep sinking of the open pore below the leaf surface. The main movements in such stoma happen in central parts of the inner tangential walls of the guard cells.
It has already been shown that large outer ledges prevent wide opening of the stomatal pore and cause it to become sunk below the leaf surface. The more is the rigidity of the ledges, the narrower is the open pore and the deeper is its sinking into the epidermis (Pautov et al., 2017). Rings of ledges are ribs of rigidity. They rib the outer ledges. Like mechanical characteristics of marginal rings do, this property of ledges influence the stomatal pore position of the open stoma.
The studied plants belong to different taxonomic groups, grow in different environments and have different life forms. Judging by widespread occurrence, their leaf structure is adaptive to different environmental conditions. It resembles the leaf structure of evergreen sclerophyllous plants which are connected, according to Axelrod (1975), in their origin with subhumid tertiary laurophyllous forests. It is possible that the stomatal complexes with rings were typical of a part of the woody plants which grew in these forests. According to current concepts, the stomatal movements depend on turgor pressure in the guard cells, their shape and wall structure (Sharpe et al., 1987; Wilmer, Fricker, 1996). The present study has shown that stomatal rings are essential functional elements of the stomata of some extant plants. According to the results of modelling, they are able to influence the stomatal movements.
This study was supported by the Russian Foundation for Basic Research (grant No. 17-04-01213a to AAP). The study was carried out using laboratory facilities of the Research Resource Centres for molecular and cell technologies of St Petersburg State University and Komarov Botanical Institute RAS.
Original languageEnglish
Title of host publicationPlant anatomy: traditions and perspectives
Subtitle of host publicationMaterials of the International Symposium dedicated to the 90th anniversary of Prof. Ludmila Ivanovna Lotova. September 16–22, 2019. In two parts
Publication statusPublished - 2019
EventSymposium “Plant anatomy: traditions and perspectives” is dedicated to the 90th anniversary of Prof. Ludmila Ivanovna Lotova, an outstanding Russian plant anatomist - Москва
Duration: 16 Sep 201922 Sep 2019


ConferenceSymposium “Plant anatomy: traditions and perspectives” is dedicated to the 90th anniversary of Prof. Ludmila Ivanovna Lotova, an outstanding Russian plant anatomist
CountryRussian Federation

Scopus subject areas

  • Agricultural and Biological Sciences(all)

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