Stomatal development in early-divergent angiosperms

Amborella trichopoda, abaxial surface of mature leaf. (A) SEM showing stomatal distribution, primarily intercostal, but with some stomata present over veins. (B, C) Details of intercostal stomata (SEM). (D) Paradermal view of a single stoma (TEM). (E) Transverse section of a single stoma showing differential wall thickenings, prominent outer cuticular ridges and less conspicuous ridging inside stomatal chamber (TEM). (F) Transverse section (LM) of a single stoma showing differential wall thickenings, prominent outer cuticular ridges and inconspicuous ridging inside stomatal chamber. (G) Transverse section of leaf (LM). (H) Paradermal section of stoma (LM). Abbreviations: ir = inner ridging, n = nucleus, ocr = outer cuticular ridge, s = stoma, st = starch, vb = vascular bundle, wt = wall thickening. Scale bars: (A) = 1 mm, (B) = 100 µm, (C, G) = 50 µm, (D) = 2 µm, (E, F, H) = 10 µm.

Ultrastructure of stomatal development in early-divergent angiosperms reveals contrasting patterning and pre-patterning

by Rudall P. J.,paula-rudall-cropped

Knowles E. V. W.

Paula J. Rudall, Emma V. W. Knowles,

Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK.(2013)

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in Annals of Botany 111: 1031-1043 – doi: 10.1093/aob/mct169 – Epub 2013 Aug 21.

CrossRef Google Scholar

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3783234/

Screen Shot 2018-08-10 at 20.10.39
Austrobaileya scandens: SEM micrographs of abaxial leaf surfaces. (A–C) Mature leaves, showing giant stoma with radiating striations in (B) and broken stoma with encircling striations in (C). (D–G) Developing leaves. (D) Stoma with encircling striations starting to develop. (E, F) Young surfaces with pre-patterning still visible, linear patterning outlined in (E) and squared patterning outlined in (F). (G) Young surface with a single pair of guard cells. Scale bars: (A, B, E, F) = 100 µm, (C) = 10 µm, (D, G) = 50 µm.

Abstract

Background and Aims

Angiosperm stomata consistently possess a pair of guard cells, but differ between taxa in the patterning and developmental origin of neighbour cells. Developmental studies of phylogenetically pivotal taxa are essential as comparative yardsticks for understanding the evolution of stomatal development.

Screen Shot 2018-08-10 at 20.18.24
Amborella trichopoda: diagrams to illustrate different orientations of cell division. (A) Protodermal ‘squared’ division. Each cell divides symmetrically across its narrowest width, so that each division is usually perpendicular to the previous one. (B, C) Two contrasting trajectories of stomatal formation from squared pattern: (B) perigenous stoma formed by symmetric division of protodermal cells; (C) mesoperigenous stoma formed by asymmetric division of protodermal cells to form a guard-mother cell (GMC: red) and a stomatal-lineage ground cell (SLGC: yellow). Stomata are coloured green, GMC red and SLGC yellow. Other cells are not coloured.

 

Methods

We present a novel ultrastructural study of developing stomata in leaves of Amborella (Amborellales), Nymphaea and Cabomba(Nymphaeales), and Austrobaileya and Schisandra (Austrobaileyales), representing the three earliest-divergent lineages of extant angiosperms (the ANITA-grade).

 

Key Results

Alternative developmental pathways occur in early-divergent angiosperms, resulting partly from differences in pre-patterning and partly from the presence or absence of highly polarized (asymmetric) mitoses in the stomatal cell lineage. Amplifying divisions are absent from ANITA-grade taxa, indicating that ostensible similarities with the stomatal patterning of Arabidopsis are superficial. In Amborella, ‘squared’ pre-patterning occurs in intercostal regions, with groups of four protodermal cells typically arranged in a rectangle; most guard-mother cells are formed by asymmetric division of a precursor cell (the mesoperigenous condition) and are typically triangular or trapezoidal. In contrast, water-lily stomata are always perigenous (lacking asymmetric divisions). Austrobaileya has occasional ‘giant’ stomata.

 

Conclusions

Similar mature stomatal phenotypes can result from contrasting morphogenetic factors, although the results suggest that paracytic stomata are invariably the product of at least one asymmetric division. Loss of asymmetric divisions in stomatal development could be a significant factor in land plant evolution, with implications for the diversity of key structural and physiological pathways.

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Published by

Willem Van Cotthem

Honorary Professor of Botany, University of Ghent (Belgium). Scientific Consultant for Desertification and Sustainable Development.

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