Developmental and morphogenetic factors govern the evolution of stomatal patterning

Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants

by Rudall P. J., Hilton J., Bateman R. (2013)

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In New Phytologist 200(3): 598-614 – DOI: 10.1111/nph.12406 –

https://www.researchgate.net/publication/255174678_Several_developmental_and_morphogenetic_factors_govern_the_evolution_of_stomatal_patterning_in_land_plants

Summary

We evaluate stomatal development in terms of its primary morphogenetic factors and place it in a phylogenetic context, including clarification of the contrasting specialist terms that are used by different sets of researchers. The genetic and structural bases for stomatal development are well conserved and increasingly well understood in extant taxa, but many phylogenetically crucial plant lineages are known only from fossils, in which it is problematic to infer development. For example, specialized lateral subsidiary cells that occur adjacent to the guard cells in some taxa can be derived either from the same cell lineage as the guard cells or from an adjacent cell file. A potentially key factor in land-plant evolution is the presence (mesogenous type) or absence (perigenous type) of at least one asymmetric division in the cell lineage leading to the guard-mother cell. However, the question whether perigenous or mesogenous development is ancestral in land plants cannot yet be answered definitively based on existing data. Establishment of ‘fossil fingerprints’ as developmental markers is critical for understanding the evolution of stomatal patterning. Long cell-short cell alternation in the developing leaf epidermis indicates that the stomata are derived from an asymmetric mitosis. Other potential developmental markers include nonrandom stomatal orientation and a range of variation in relative sizes of epidermal cells. Records of occasional giant stomata in fossil bennettites could indicate development of a similar type to early-divergent angiosperms.

Stomatal patterning in Bennettitales

Leaf surface development and the plant fossil record: stomatal patterning in Bennettitales

by Rudall P. J., Bateman R. M. (2019)

Paula J. Rudall, Richard M. Bateman,

Royal Botanic Gardens, Kew, Richmond, United Kingdom

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In Biological Reviews 94(3) – https://doi.org/10.1111/brv.12497 –

https://onlinelibrary.wiley.com/doi/abs/10.1111/brv.12497

Abstract

Stomata play a critical ecological role as an interface between the plant and its environment. Although the guard‐cell pair is highly conserved in land plants, the development and patterning of surrounding epidermal cells follow predictable pathways in different taxa that are increasingly well understood following recent advances in the developmental genetics of the plant epidermis in model taxa. Similarly, other aspects of leaf development and evolution are benefiting from a molecular–genetic approach. Applying this understanding to extinct taxa known only from fossils requires use of extensive comparative morphological data to infer ‘fossil fingerprints’ of developmental evolution (a ‘palaeo‐evo‐devo’ perspective).

The seed‐plant order Bennettitales, which flourished through the Mesozoic but became extinct in the Late Cretaceous, displayed a consistent and highly unusual combination of epidermal traits, despite their diverse leaf morphology. Based on morphological evidence (including possession of flower‐like structures), bennettites are widely inferred to be closely related to angiosperms and hence inform our understanding of early angiosperm evolution. Fossil bennettites – even purely vegetative material – can be readily identified by a combination of epidermal features, including distinctive cuticular guard‐cell thickenings, lobed abaxial epidermal cells (‘puzzle cells’), transverse orientation of stomata perpendicular to the leaf axis, and a pair of lateral subsidiary cells adjacent to each guard‐cell pair (termed paracytic stomata). Here, we review these traits and compare them with analogous features in living taxa, aiming to identify homologous – and hence phylogenetically informative – character states and to increase understanding of developmental mechanisms in land plants.

We propose a range of models addressing different aspects of the bennettite epidermis. The lobed abaxial epidermal cells indicate adaxial–abaxial leaf polarity and associated differentiated mesophyll that could have optimised photosynthesis. The typical transverse orientation of the stomata probably resulted from leaf expansion similar to that of a broad‐leaved monocot such as Lapageria, but radically different from that of broad‐leafed eudicots such as Arabidopsis. Finally, the developmental origin of the paired lateral subsidiary cells – whether they are mesogene cells derived from the same cell lineage as the guard‐mother cell, as in some eudicots, or perigene cells derived from an adjacent cell lineage, as in grasses – represents an unusually lineage‐specific and well‐characterised developmental trait. We identify a close similarity between the paracytic stomata of Bennettitales and the ‘living fossil’ Gnetum, strongly indicating that (as in Gnetum) the pair of lateral subsidiary cells of bennettites are both mesogene cells. Together, these features allow us to infer development in this diverse and relatively derived lineage that co‐existed with the earliest recognisable angiosperms, and suggest that the use of these characters in phylogeny reconstruction requires revision.

Epidermal patterning and stomatal development in Gnetales (Gymnospermae)

Epidermal patterning and stomatal development in Gnetales

by Rudall P. J., Rice C. L. (2019)

Paula J. Rudall, Callie L. Rice,

Royal Botanic Gardens, Kew, Richmond, TW9, UK

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In Annals of Botany, mcz053 – https://doi.org/10.1093/aob/mcz053 –

https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz053/5482537?redirectedFrom=fulltext

Abstract

Background and Aims

The gymnosperm order Gnetales, which has contentious phylogenetic affinities, includes three extant genera (EphedraGnetumWelwitschia) that are morphologically highly divergent and have contrasting ecological preferences: Gnetum occupies mesic tropical habitats, whereas Ephedraand Welwitschia occur in arid environments. Leaves are highly reduced in Ephedra, petiolate with a broad lamina in Gnetum and persistent and strap-like in Welwitschia. We investigate stomatal development and prepatterning stages in Gnetales, to evaluate the substantial differences among the three genera and compare them with other seed plants.

Methods

Photosynthetic organs of representative species were examined using light microscopy, scanning electron microscopy and transmission electron microscopy.

Key Results

Stomata of all three genera possess lateral subsidiary cells (LSCs). LSCs of Ephedra are perigene cells derived from cell files adjacent to the stomatal meristemoids. In contrast, LSCs of Gnetumand Welwitschia are mesogene cells derived from the stomatal meristemoids; each meristemoid undergoes two mitoses to form a ‘developmental triad’, of which the central cell is the guard mother cell and the lateral pair are LSCs. Epidermal prepatterning in Gnetum undergoes a ‘quartet’ phase, in contrast with the linear development of Welwitschia. Quartet prepatterning in Gnetum resembles that of some angiosperms but they differ in later development.

Conclusions

Several factors underpin the profound and heritable differences observed among the three genera of Gnetales. Stomatal development in Ephedra differs significantly from that of Gnetum and Welwitschia, more closely resembling that of other extant gymnosperms. Differences in epidermal prepatterning broadly reflect differences in growth habit between the three genera.

Stomata in Quillajaceae and Surianaceae (Fabales)

FIG. 3. Quillaja saponaria, flower and inflorescence structure. – (K) A single stomata from a nectary

Floral Morphology and Development in Quillajaceae and Surianaceae (Fabales), the Species-poor Relatives of Leguminosae and Polygalaceae

by Bello Gutierrez M. A., Hawkins J. A., Rudall P. J. (2008)

Maria Angélica Bello Gutierrez, Julie A. Hawkins, Paula J. Rudall,

In Ann. Bot. 101(9): 1433, 1491-1505 – DOI: 10.1093/aob/mcn073 –

https://www.researchgate.net/publication/5356515_Floral_Morphology_and_Development_in_Quillajaceae_and_Surianaceae_Fabales_the_Species-poor_Relatives_of_Leguminosae_and_Polygalaceae

Abstract:

Molecular phylogenies have suggested a new circumscription for Fabales to include Leguminosae, Quillajaceae, Surianaceae and Polygalaceae. However, recent attempts to reconstruct the interfamilial relationships of the order have resulted in several alternative hypotheses, including a sister relationship between Quillajaceae and Surianaceae, the two species-poor families of Fabales. Here, floral morphology and ontogeny of these two families are investigated to explore evidence of a potential relationship between them. Floral traits are discussed with respect to early radiation in the order. Floral buds of representatives of Quillajaceae and Surianaceae were dissected and observed using light microscopy and scanning electron microscopy. Quillajaceae and Surianaceae possess some common traits, such as inflorescence morphology and perianth initiation, but development and organization of their reproductive whorls differ. In Quillaja, initiation of the diplostemonous androecium is unidirectional, overlapping with the petal primordia. In contrast, Suriana is obdiplostemonous, and floral organ initiation is simultaneous. Independent initiation of five carpels is common to both Quillaja and Suriana, but subsequent development differs; the antesepalous carpels of Quillaja become fused proximally and exhibit two rows of ovules, and in Suriana the gynoecium is apocarpous, gynobasic, with antepetalous biovulate carpels. Differences in the reproductive development and organization of Quillajaceae and Surianaceae cast doubt on their potential sister relationship. Instead, Quillaja resembles Leguminosae in some floral traits, a hypothesis not suggested by molecular-based phylogenies. Despite implicit associations of zygomorphy with species-rich clades and actinomorphy with species-poor families in Fabales, this correlation sometimes fails due to high variation in floral symmetry. Studies considering specific derived clades and reproductive biology could address more precise hypotheses of key innovation and differential diversification in the order.

Loss of asymmetric divisions in stomatal development could be a significant factor in land plant evolution

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., Knowles E. V. W. (2013)

Paula J. Rudall, Emma V. W. Knowles,

Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK

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In Ann. Bot. 112: 1031–1043 – doi: 10.1093/aob/mct169 –

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

Amborella trichopoda: light micrographs and diagrams illustrating patterns of cell divisions during early development of the abaxial leaf epidermis. (A) Young developing leaf, with red lines outlining the likely boundaries of the original longitudinal cell files that existed prior to squared divisions. (B) Region with squared groups of cells. (C, D) Two versions of the same micrograph, with a group of cells outlined in red in (D) to illustrate division pattern. More recent walls are drawn as not interrupting older ones, to indicate their sequence of formation. (E) Group of cells highlighted in dark green box in (C), showing the squared pattern of division (diagram, Fig. 7A), and illustrating how sister cells divide at different rates. Cell A was sister to cell B; they each divided into A1 and A2 and B1 and B2, respectively. B2 has already divided again, forming B2a and B2b; A2 is in the process of dividing. (F) Diagram showing the series of divisions highlighted in (D). The cells would initially have been smaller and more regularly shaped than they appear at this stage. (G, H) stomata formed directly by symmetric division of protodermal cells, without asymmetric division (diagram, Fig. 5B). (I) Stoma and meristemoid both formed by asymmetric divisions (diagram, Fig. 5C). (J) Meristemoid formed by asymmetric division. (L) Stoma formed by asymmetric division. (L) Older stoma; developmental origin not clear. Abbreviations: g = guard cell, gmc = guard mother cell (GMC), m = meristemoid, sd = symmetric division, slgc = stomatal lineage ground cell (SLGC). Scale bars: (A, B) = 20 µm; (C–E, G–K) = 10 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.

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).

Amborella trichopoda: TEM micrographs illustrating patterns of cell divisions during stomatal development on the abaxial leaf epidermis. (A) Group of protodermal cells showing squared arrangement. (B, C) Meristemoids formed by asymmetric division (diagram, Fig. 5C). (D) Pair of guard cells formed by symmetric division of protodermal cells, without asymmetric division (diagram, Fig. 5B). (E) Pair of guard cells showing starch. (F) Pair of guard cells and SLGC. Abbreviations: dp = division plate, g = guard cell, m = meristemoid, sd = symmetric division, slgc = stomatal lineage ground cell (SLGC).

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.

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.

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.

Developmental and morphogenetic factors and the evolution of stomatal patterning in land plants

Stomata of extant ferns and gymnosperms (a, psilophyte; b, fern; c, cycad; d, ginkgophyte; e, f, conifers; all from Kew microscope slide collection, except b and f, which are differential-interference contrast images of cleared leaves). (a) Axis epidermis of Psilotum nudum, with linear cell files and anomocytic stomata. (b) Abaxial leaf surface of Pteridium aquilinum, showing epidermal cells with sinuous walls and anomocytic stomata mostly oriented in the same direction. (c) Abaxial leaf surface of Cycas circinalis, showing stephanocytic stomata. (d) Abaxial leaf surface of Ginkgo biloba, showing stomata with a ring of neighbouring cells. (e) Abaxial leaf surface of Podocarpus nivalis; showing guard cells uniformly axially oriented. (f) Abaxial leaf surface of Pinus flexilis, showing guard cells uniformly axially oriented. gc, guard cell; slgc, stomatal-lineage ground cell. Bars: (a, b, e, f) 20 μm; (c) 50 μm; (d) 10 μm.

 

Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants

by Rudall P. J., Hilton J., Bateman (2013)

Paula J. RudallRichard Bateman, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK.

Jason HiltonUniversity of Birmingham

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in New Phytologist 200(3) – DOI: 10.1111/nph.12406 –

https://www.ncbi.nlm.nih.gov/pubmed/23909825

Screen Shot 2018-11-02 at 21.54.57
Stomata of extinct medullosans (a–c), cordaites (d), cycads (e, f), ginkgophytes (g) and corystosperms (h, i), from Florin slides in the collection at the Swedish Museum of Natural History. (a–c) Cyclopteris orbicularis S010965. (d) Cordaites sp. S20514. (e) Ptilozamites sp. S113982. (f) Ctenis nathorstii S113983. (g) Baiera furcata S113993. (h, i) Dicroidium feistmantelii S113986. Bars: (a, e) 100 μm; (b, c, f, h) 20 μm; (d, g, i) 50 μm.

Abstract

We evaluate stomatal development in terms of its primary morphogenetic factors and place it in a phylogenetic context, including clarification of the contrasting specialist terms that are used by different sets of researchers.

The genetic and structural bases for stomatal development are well conserved and increasingly well understood in extant taxa, but many phylogenetically crucial plant lineages are known only from fossils, in which it is problematic to infer development. For example, specialized lateral subsidiary cells that occur adjacent to the guard cells in some taxa can be derived either from the same cell lineage as the guard cells or from an adjacent cell file.

Screen Shot 2018-11-02 at 22.03.37
Stomata of extinct fossil bennettites (a–f), peltasperms (h) and conifers (h–j), from Florin slides in the collection at the Swedish Museum of Natural History. (a, b) Otozamites bornholmiensis S113984. (c–f) Dictyozamites johnstrupii S113977. (g) Callipteris conferta S113987. (h) Genitzia sp. S113966. (i, j) Abietites linkii S153062. (k) Androvettia sp. S153021. (l) Taxites sp. S1113961. Bars: (a, c, i) 100 μm; (b, d, e, g, h, j) 20 μm; (f, k, l) 50 μm.

A potentially key factor in land-plant evolution is the presence (mesogenous type) or absence (perigenous type) of at least one asymmetric division in the cell lineage leading to the guard-mother cell. However, the question whether perigenous or mesogenous development is ancestral in land plants cannot yet be answered definitively based on existing data.

Screen Shot 2018-11-02 at 22.07.49
Stomata of extant angiosperms, imaged from the Kew microscope slide collection. (a–c) Monocots with linear leaves and mesoperigenous stomata (leaf axis oriented vertically on page). (a) Anomocytic stomata of Smilax trifolia (Smilacaceae). (b) Anomocytic stomata of Cardiocrinum giganteum (Liliaceae). (c) Paracytic stomata (grass type) of Zea mays (Poaceae). (d–f) Eudicots with reticulate venation. (d) Groups of mesogenous stomata in Brassica oleracea (Brassicaceae). (e) Anomocytic stomata of Vicia faba (Fabaceae). (f) Diacytic stomata of Asystasia bella (Acanthaceae). gc, guard cell; lsc, lateral subsidiary cell. Bars, 20 μm.

Establishment of ‘fossil fingerprints’ as developmental markers is critical for understanding the evolution of stomatal patterning. Long cell-short cell alternation in the developing leaf epidermis indicates that the stomata are derived from an asymmetric mitosis.

Other potential developmental markers include nonrandom stomatal orientation and a range of variation in relative sizes of epidermal cells. Records of occasional giant stomata in fossil Bennettites could indicate development of a similar type to early-divergent angiosperms.

The evolution of stomatal patterning in land plants

Screen Shot 2018-06-16 at 11.57.57
Fig. 3 Photomicrographs of meristemoids in Amborella trichopoda (for details see Rudall & Knowles, 2013). (a, b) Perigenous stomata: recently divided rectangular guard-mother cells (GMCs) resulting from symmetric division of a protodermal cell. (c, d) Mesoperigenous stomata: angular meristemoids resulting from asymmetric division of a protodermal cell. gc, guard cell; gmc, guard-mother cell; slgc, stomatal-lineage ground cell. Bars, 10 lm.

 

Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants

by Rudall P. J.Hilton J.Bateman R. M. (2013)

Paula J. Rudall, Jason Hilton, Richard M. Bateman,

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

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in New Phytol. 200(3): 98-614 – doi: 10.1111/nph.12406 – Epub 2013 Jul 26 –

https://www.ncbi.nlm.nih.gov/pubmed/23909825

Screen Shot 2018-06-16 at 12.00.12
Fig. 4 Stomata of extant ferns and gymnosperms (a, psilophyte; b, fern; c, cycad; d, ginkgophyte; e, f, conifers; all from Kew microscope slide collection, except b and f, which are differential-interference contrast images of cleared leaves). (a) Axis epidermis of Psilotum nudum, with linear cell files and anomocytic stomata. (b) Abaxial leaf surface of Pteridium aquilinum, showing epidermal cells with sinuous walls and anomocytic stomatamostly oriented in the same direction. (c) Abaxial leaf surface of Cycas circinalis, showing stephanocytic stomata. (d) Abaxial leaf surface of Ginkgo biloba, showing stomata with a ring of neighbouring cells. (e) Abaxial leaf surface of Podocarpus nivalis; showingguard cells uniformly axially oriented. (f) Abaxial leaf surface of Pinus flexilis, showingguard cells uniformly axially oriented. gc, guard cell; slgc, stomatal-lineage ground cell. Bars: (a, b, e, f) 20 lm; (c) 50 lm; (d) 10 lm.

Abstract

We evaluate stomatal development in terms of its primary morphogenetic factors and place it in a phylogenetic context, including clarification of the contrasting specialist terms that are used by different sets of researchers.

Screen Shot 2018-06-16 at 12.03.00
Fig. 5 Stomata of extinct medullosans (a–c), cordaites (d), cycads (e, f), ginkgophytes (g) and corystosperms (h, i), from Florin slides in the collection at the Swedish Museum of Natural History. (a–c) Cyclopteris orbicularis S010965. (d) Cordaites sp. S20514. (e) Ptilozamites sp. S113982. (f) Ctenis nathorstii S113983. (g) Baiera furcata S113993. (h, i) Dicroidium feistmantelii S113986.Bars: (a, e) 100 lm; (b, c, f, h)20 lm; (d, g, i) 50 lm.

The genetic and structural bases for stomatal development are well conserved and increasingly well understood in extant taxa, but many phylogenetically crucial plant lineages are known only from fossils, in which it is problematic to infer development. For example, specialized lateral subsidiary cells that occur adjacent to the guard cells in some taxa can be derived either from the same cell lineage as the guard cells or from an adjacent cell file.

Screen Shot 2018-06-16 at 12.05.29
Fig. 6 Stomata of extinct fossil bennettites (a–f), peltasperms (h) and conifers (h–j), from Florin slides in the collection at the Swedish Museumof Natural History. (a, b)Otozamites bornholmiensis S113984. (c–f)Dictyozamites johnstrupii S113977. (g) Callipteris conferta S113987. (h) Genitzia sp. S113966. (i, j) Abietites linkii S153062. (k) Androvettia sp. S153021. (l) Taxites sp. S1113961. Bars: (a, c, i) 100 lm; (b, d, e, g, h, j) 20 lm; (f, k, l) 50 lm.

A potentially key factor in land-plant evolution is the presence (mesogenous type) or absence (perigenous type) of at least one asymmetric division in the cell lineage leading to the guard-mother cell. However, the question whether perigenous or mesogenous development is ancestral in land plants cannot yet be answered definitively based on existing data.

Screen Shot 2018-06-16 at 12.07.49
Fig. 7 Stomata of extant angiosperms, imaged from the Kew microscope slide collection. (a–c) Monocots with linear leaves and mesoperigenous stomata (leaf axis oriented vertically on page). (a) Anomocytic stomata of Smilax trifolia (Smilacaceae). (b) Anomocytic stomata of Cardiocrinum giganteum (Liliaceae). (c) Paracytic stomata (grass type) of Zea mays (Poaceae). (d–f) Eudicots with reticulate venation. (d) Groups of mesogenous stomata in Brassica oleracea (Brassicaceae). (e) Anomocytic stomata of Vicia faba (Fabaceae). (f) Diacytic stomata of Asystasia bella (Acanthaceae). gc, guard cell; lsc, lateral subsidiary cell. Bars, 20 lm.

Establishment of ‘fossil fingerprints’ as developmental markers is critical for understanding the evolution of stomatal patterning. Long cell-short cell alternation in the developing leaf epidermis indicates that the stomata are derived from an asymmetric mitosis.

Screen Shot 2018-06-16 at 12.09.52
Fig. 2 Diagrams illustrating stomatal patterning. (a) Two contrasting trajectories of stomatal formation from squared pre-patterning (Box 1), in a specieswith reticulate-veined leaves: (a?b?c) perigenous stomaformedby symmetric division of protodermal cells. (a?d?e?f) mesoperigenous stoma formed by asymmetric division of protodermal cells to form a guardmother cell (GMC; red) and a stomatal-lineage ground cell (SLGC; yellow). (b) Development of paracytic stomata in a monocot species with linear leaves, mesoperigenous development and perigenous lateral subsidiary cells (e.g. grasses and Tradescantia), from linear pre-patterning in (g). (c) Mesoperigenous stomatal development in a species with reticulateveined leaves (e.g. Amborella; Rudall & Knowles, 2013). (d) Several contrasting trajectories of mesogenous stomatal formation by a series of amplifying divisions, in a species with reticulate-veined leaves (e.g. Arabidopsis). (e) Development of paracytic stoma with mesogene lateral subsidiary cells (e.g. Annonaceae). Key: protodermal cell that will give rise to the stomatal lineage, pale blue; paired guard cells, green; meristemoid orGMC, red; SLGCormesogene lateral subsidiary cells, yellow; perigene lateral subsidiary cells, purple.

Other potential developmental markers include nonrandom stomatal orientation and a range of variation in relative sizes of epidermal cells. Records of occasional giant stomata in fossil Bennettites could indicate development of a similar type to early-divergent angiosperms.