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

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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.

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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.

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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.

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The pattern of cellulose crystallinity in stomata of floating plants was altered as a consequence of similar evolutionary pressures

Floating aquatic plants have stomata with an altered pattern of cellulose crystallinity. Crystallinity patterns in the land plant Cyclamen persicum (A,B); and aquatic plant Nuphar lutea (D,E) shown by liquid crystal polarized light microscopy (LC-PolScope). A schematic representation of the regular crystallinity pattern in angiosperm kidney-shaped stomata (C) and the altered pattern in the stomata of floating plants (F). The retardance color scale bar codes the retardance range. Scale: 25 µm.

 

Permanently open stomata of aquatic angiosperms display modified cellulose crystallinity patterns

by Shtein J., Popper Z. A., Harpaz-Saad S. (2017)

Ilana_Shtein
Ilana Shtein, Department of Mechanical Engineering, Ben-Gurion University of the Negev, Beer Sheva, Israel
Zoe_Popper
Zoë A. Popper, Botany and Plant Science, Ryan Institute for Environmental, Marine and Energy Research, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
Smadar_Harpaz-Saad
Smadar Harpaz-Saad, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel
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in Plant Signal Behav.  12(7): e1339858 – doi:  10.1080/15592324.2017.1339858 – 

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5586356/

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Figure 2. Stomatal crystallinity patterns of floating aquatic plant species. Liquid crystal polarized light microscopy (LC-PolScope) images of the adaxial leaf epidermis from the early-diverging angiosperms Nuphar lutea (A), Nymphaea alba (B), and the monocotyledons Limnobium laevigatum (C) and Alisma plantago-aquatica (D). The retardance color scale bar codes the retardance range. Scale: 50 µm.

Abstract

Most floating aquatic plants have stomata on their upper leaf surfaces, and usually their stomata are permanently open. We previously identified 3 distinct crystallinity patterns in stomatal cell walls, with angiosperm kidney-shaped stomata having the highest crystallinity in the polar end walls as well as the adjacent polar regions of the guard cells.

A numerical bio-mechanical model suggested that the high crystallinity areas are localized to regions where the highest stress is imposed. Here, stomatal cell wall crystallinity was examined in 4 floating plants from 2 different taxa: basal angiosperms from the ANITA grade and monocots.

It appears that the non-functional stomata of floating plants display reduced crystallinity in the polar regions as compared with high crystallinity of the ventral (inner) walls. Thus their guard cells are both less flexible and less stress resistant.

Our findings suggest that the pattern of cellulose crystallinity in stomata of floating plants from different families was altered as a consequence of similar evolutionary pressures.

 

Stomata in 30 plant families

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Morphological characteristics of leaves and stems of selected Texas woody plants

by Meyer R. E., Meola S. M. (1978)

R. E. MEYER, PLANT PHYSIOLOGIST, AGRICULTURAL RESEARCH SERVICE DEPARTMENT OF RANGE SCIENCE, TEXAS A&M UNIVERSITY COLLEGE STATION, TEX. 77843

S. M. MEOLA, RESEARCH ENTOMOLOGIST, AGRICULTURAL RESEARCH SERVICE VETERINARY TOXICOLOGY AND ENTOMOLOGY RESEARCH LABORATORY COLLEGE STATION, TEX. 77840

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in Texas Agricultural Experiment Station – USDA Tech. Bulletin 1564

https://naldc.nal.usda.gov/download/CAT78702502/PDF

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Abstract

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Stomata in 40 angiosperms

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Fig. 1: Photographs of leaf epidermal cells (a), Abaxial surface of Vaccaryia pyramedica (20X); (b), Abaxial surface of Polygonum plebijum (40X); (c), Abaxial surface of Poa annua (40X); (d), Abaxial surface of Ochthochloa compressa (20X); (e), Adaxial surface of Lathyrus aphaca (40X); (f), Adaxial surface of Lycopersicon esculentum (20X)

Taxonomic diversity in epidermal cells of some sub-tropical plant species.

by Ahmad K., Khan M. A., Ahmad M., Shaheen N., Nazir A. (2010)

KHALID AHMAD, MIR AJAB KHAN, MUSHTAQ AHMAD, NIGHAT SHAHEEN, ABDUL NAZIR,

Department of plant sciences, Quaid-i-Azam University, Islamabad, Pakistan

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Fig. 2: Photographs of leaf epidermal cells (a), Adaxial surface of Melilotus indica (40X); (b), Abaxial surface of Melilotus indica (20X); (c), Adaxial surface of Vicia faba (40X); (d), Adaxial surface of Euphorbia helioscopia (40X); (e), Abaxial surface of Tribulus teristris (40X); (f), Abaxial surface of Polypogan monspeliensis (40X)

in Int. J. Agric. Biol. 12: 115–118  – ISSN Print: 1560–8530; ISSN Online: 1814–9596 –

https://www.researchgate.net/profile/Abdul_Nazir2/publication/267822076_Taxonomic_Diversity_in_Epidermal_Cells_of_some_Sub-tropical_Plant_Species/links/5469d8120cf2f5eb180530d2.pdf

ABSTRACT

A total of 40 angiosperm plant species from 38 genera of 22 families were investigated for the type and shape of leaf epidermal cells.

The result showed substantial variations in the type and shape of epidermal cells from straight to polygonal up to wavy.

The present results showed that the shape of leaf epidermal cells can not play its role in correlating the taxa but is significant in delimiting the related taxa.

Structure and development of stomata in some angiosperms

 

 

Structure and development of stomata in some angiosperms

by Gopal B. V. (1970)

Ph.D. Thesis, Sardar Patel Univ., Vallabh Vidyanagar, Gujarat, India –

http://shodhganga.inflibnet.ac.in/bitstream/10603/76141/25/25_summary%20and%20conclusions.pdf

SUMMARY AND CONCLUSIONS

The structure and development of stomata are studied in 114 genera and 237 species “belonging to 17 gamopetalous families of Angiosperms. The investigation is made largely on leaves hut in 25 species vegetative and floral organs are also studied.

For comparing the structure and ontogeny of stomata with the members of the Gesneriaceae, three species of the genus Begonia also are studied in addition to 237 species of the gamopetalae. So in all 240 species have been worked out. The mature aspect of the epidermis, types of stomata and their ontogeny, abnormalities studied for each family are summarised as follows:

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Artificial key for the identification of families studied of Gamopetalae on leaf characters:

An attempt has been made to classify the gamopetalous families studied on the basis of the data presented above regarding the stomatal types and modes of development. The seventeen gamopetalous families can be conveniently grouped as under:

STOMATA:

I. One stomatal type:

1. Uniform mode of stomatal development:

A. Perigenous anomocytic:

(i) Ebenaceae (leaves large foliage)

(ii) Orobanchaceae (Leaves small scale like and not green)

(iii) Lentibulariaceae (Leaves small, bladders present)

B. Mesogenous-diacytic:

(iv) Aeanthaceae (occurrence of single or double cystolith is also a distinctive feature of the epidermis)

 

II. Diverse stomatal types:

1. Uniform mode of stomatal development:

A. Perigenous:

(a) Anisocytic. anomocytic. diacytic and paracytic:

(v) Myrsinaceae

(b) Anomocytic. paracytic and stomata with a single subsidiary cell:

(vi) Pedaliaceae incl. Martyniaceae

2. Diverse modes of stomatal development:

(A). Perigenous and mesogenous:

(a) Anisocytic. anomocytic. diacytic and paracytic:

(vii) Rubiaceae – (Stipules present paracytic stomata more monocyclic, completely or incompletely amphicyclic)

(viii) Sapotaceae – (anomocytic stomata more, paracytic stomata not amphicyclic)

(ix) Verbenaceae – (Stipules absent)

(b) Anisocytic. anomocytic. paracytic and cyclocytic:

(x) Plumbaginaceae (division of subsidiary cells common)

(c) Diacytic and anomocytic: (xi) Labiatae

(d) Anisocytic. anomocytic. diacytic. paracytic and stomata with a single subsidiary cell:

(xii) Compositae (anomocytic stomata more)

(xiii) Gesneriaceae (anisocytic stomata more) (abnormalities more)

(xiv) Bignoniaceae (Peltate glands and extra-floral nectaries present)

(B) Perigenous. mesoperigenous and mesogenous:

(a) Anomocytic. anisocytic. diacytic, paracytic and stomata with a single subsidiary cell:

(xv) Scrophulariaceae

(b) Anomocytic. paracytic and stomata with a single subsidiary cell:

(xvi) Primulaceae (Anomocytic & stomata with a single subsidiary cell common)

(xvii) Plantaginaceae (Anomocytic common)

Stomata on Angiosperm seedling roots

 

 

Stomata on the seedling roots in the representatives of four families of angiosperms

by Staszewska U. M., Tarkowska J. A. (1992)

  • Uniwersytet Warszawski

in Fragmenta Floristica et Geobotanica 37(2): 425-430 – ISSN :0015-931X –

https://www.infona.pl/resource/bwmeta1.element.agro-article-a06f15ae-ae69-4713-acc6-58959010ab23

(No abstract found)

Ontogenetic stomatal types in the Angiosperms (in Spanish)

 

 

Los tipos de desarollo estomatico en las Angiospermas

por Roth I., Clausnitzer I. (1969)

Instituto Experimental Jardín Botánico “Dr. Tobías Lasser”

Ingrid Roth,  Ingrid Clausnitzer

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in Acto Bot. Venez. 4: 259-292 –

https://www.jstor.org/stable/41740431?seq=1#page_scan_tab_contents

Abstract

1) En el desarrollo del aparato estomático se reconocen dos tipos principales: el tipo perigéneo de las células auxiliares en el cual las células acompañantes se originan de células epidérmicas vecinas a la célula madre de las oclusivas y el tipo mesogéneo en el cual se forman tanto las células acompañantes como las oclusivas de la misma célula madre
2) El tipo perigéneo encontrado principalmente en las monocotiledóneas (Gramíneas, Commelinaceae, Palmae, Marantaqeae, Musaceae etc.) se divide en cuatro subtipos:
a) El subtipo de Saccharum, común de la mayoría de las gramineae, en el cual las células acompañantes se inician en células epidérmicas de dos diferentes hileras celulares adyacentes a la hilera de la cual procede la célula madre de las oclusivas.
b) El subtipo de Pariana en el cual se forman también dos células acompañantes que proceden de la célula epidérmica superior e inferior adyacentes a la célula madre de las oclusivas, es decir que se forman de la misma hilera celular que el estoma el cual está dispuesto perpendicular a las hileras longitudinales de células epidérmicas.
c) El subtipo de Rhoeo discolor y de las Commelinaceae en general en el cual se forman cuatro células acompañantes de cuatro diferentes células epidérmicas adyacentes a la célula madre de las oclusivas (dos laterales, una superior y una inferior).
d) Por último, el subtipo actinocítico que es característico de las dicotiledóneas; aqui las células epidérmicas que rodean la célula madre de las oclusivas se alargan radialmente y se dividen a lo largo de los radios de un círculo formando un dibujo de estrella alrededor de la célula madre central; en este caso, las relaciones entre estoma y células acompañantes son menos estrictas, ya que esta agrupación de células se encuenta también alrededor de pelos e idioblastos.
3) El tipo mesogéneo puede subdividirse en cuatro ubtipos:
a) El subtipo lateral-paralelo de dos caras en el cual la célula madre se divide a manera de una célula inicial que forma segmentos en dos caras produciendo células acompañantes hacia ambos lados; el número de células acompañantes puede variar entre dos y seis.
b) El subtipo perpendicular o transversal en el cual la célula madre se divide de la misma manera que en a), pero el poro está perpendicular al eje divisorio de las células acompañantes (en vez de paralelamente como en a), ya que en la última división que da origen a las dos células oclusivas el eje divisorio da una vuelta de 90°. Por lo tanto, consideramos el subtipo lateral-paralelo y el subtipo perpendicular como dos variaciones de la misma forma fundamental.
c) El subtipo espiral, realizado p. e. en Sedum en el cual la célula madre triangular forma segmentos sucesivamente a lo largo de las tres caras siguiendo un espiral; el modo de división es comparable al mismo de una célula inicial que se divide a tres caras. Como caso deducido del subtipo espiral consideramos la forma con tres células acompañantes que rodean a la célula madre de las oclusivas; se supone que se trata de una reducción del número de las células acompañantes.
d) El suptipo irregular en el cual se inician las células acompañantes de la misma célula madre que las oclusivas, pero el número de las células acompañantes, su disposición y el modo de dividirse de la célula madre es indefinido.
4) Los tiops de desarrollo hallados por nosotras coinciden muy bien con los tipos establecidos a base de la forma adulta del aparato estomático. El tipo de Saccharum coincide con el tipo de las gramíneas de Stebbins & Khush. El tipo de Rhoeo discolor coincide con los dos tipos de cuatro o más células acompañantes (Rhoco, palmae) de Stebbins y Khush. El tipo lateral-paralelo coincide con el tipo paracítico de Metcalfe & Chalk; el tipo perpendicular o transversal coincide con el tipo diacítico de Mefcalfe & Chalk; el tipo espiral coincide con el tipo anisocítico de Metcalfe & Chalk; y el tipo irregular coincide más o menos con el tipo anomicítico de Metcalfe & Chalk.
5) Las divisiones desiguales (Bünning 1953) son muy comunes en la formación de las células acompañantes, especialmente de las Gramineae, Commelinaceae y otras monocotiledóneas.