Stomata in Drymoglossum

Morphology, Physiology, and Anatomy of Penny Fern (Drymoglossum phyloselloides) and Its Effect on Cocoa

Yuliasmara F., Ardyani F. (2013)

Fitria Yuliasmara

Indonesian Coffee and Cocoa Research Institute

Fitria Ardyani

Indonesian Coffee and Cocoa Research Institute


Pelita Perkebunan (a Coffee and Cocoa Research Journal) 29(2): –


This study aims to determine the anatomy, physiology and morphology of penny fern (Drimoglosum phylloseloides) and its effect on cocoa. Morphological observation of penny fern used microscope to observe the roots, stems, leaves and spores. Physiology of penny fern was observed based on number of stomata and stomatal conductance using stomata printing method, while the amount of chlorophyll based on spectrophotometric method and rate of transpiration used cobalt chloride paper.

Penny fern anatomy on cross-sectional and longitudinal in roots, stems and leaves. Penny fern growth was observed based the length of tendrils once a week during rainy and dry season. While the effect of penny fern invasion was observed based on variable leaf area with gravimetric method, the cross-section of attacked cacao branch using microtom and microscope and chlorophyll content by chlorophyll meter. Results showed that penny fern is a epiphytic weed which was crassulaceae acid metabolism plants that have the ability to absorb carbon dioxide at night and carry out photosynthesis during the day with closed stomata. Penny ferns reproduce using spores. The growth rate of penny fern 2.18 cm/week during the dry season and while in rainy season 3.89 cm/week. Penny fern leaf contains 0.0212 mg/g chlorophyll.

Penny fern stomata density was 18.33/mm 2 with a width of opening stomata at night 26.3 µm which caused a veryslow rate of transpiration of 0.69 mm 2 /seconds. The existence penny fern on cocoa decreased leaf area and chlorophyll content decreased crop productivity which was indicated by decreasing in number of flowers, number of small, medium fruit, and large pods. However it had no effect on the number of leaves on one side flush cocoa.

New molecular and physiological evidence for the presence of active stomatal control in ferns

Evolutionary conservation of ABA signaling for stomatal closure

Cai S., Chen G., Wang Y., Huang Y., Marchant B., Wang Y., Yang Q., Dai F.,
Hills A., Franks P. J., Nevo E., Soltis D. E., Soltis P. S., Sessa E., Wolf P. G., Xue D., Zhang G., Pogson B. J., Blatt M. R., Chen Z. H. (2017)

Shengguan CaiGuang ChenYuanyuan WangYuqing HuangD. Blaine MarchantYizhou WangQian YangFei DaiAdrian HillsPeter J. FranksEviatar NevoDouglas E. SoltisPamela S. SoltisEmily SessaPaul G. WolfDawei XueGuoping ZhangBarry J. PogsonMichael R. BlattZhong-Hua Chen

Plant Physiol 174(2): 732-747 –


Abscisic acid (ABA)-driven stomatal regulation reportedly evolved after the divergence of ferns, during the early evolution of seed plants approximately 360 million years ago. This hypothesis is based on the observation that the stomata of certain fern species are unresponsive to ABA, but exhibit passive hydraulic control. However, ABA-induced stomatal closure was detected in some mosses and lycophytes. Here, we observed that a number of ABA signaling and membrane transporter protein families diversified over the evolutionary history of land plants. The aquatic ferns Azolla filiculoides and Salvinia cucullata have representatives of 23 families of proteins orthologous to those of Arabidopsis (Arabidopsis thaliana) and all other land plant species studied. Phylogenetic analysis of the key ABA signaling proteins indicates an evolutionarily conserved stomatal response to ABA. Moreover, comparative transcriptomic analysis has identified a suite of ABA-responsive genes that differentially expressed in a terrestrial fern species, Polystichum proliferum. These genes encode proteins associated with ABA biosynthesis, transport, reception, transcription, signaling, and ion and sugar transport, which fit the general ABA signaling pathway constructed from Arabidopsis and Hordeum vulgare. The retention of these key ABA-responsive genes could have had a profound effect on the adaptation of ferns to dry conditions. Furthermore, stomatal assays have shown the primary evidence for ABA-induced closure of stomata in two terrestrial fern species Pproliferum and Nephrolepis exaltata. In summary, we report, to our knowledge, new molecular and physiological evidence for the presence of active stomatal control in ferns.

Stomata in Osmunda

Stomatal traits in Iberian populations of Osmunda regalis (Osmundaceae, Polypodiopsida) and its relationship with bioclimatic variables

Lavilla M., Seral A., Murciano A., Molino S., Fuente P. D. L., Galan J. M. G. Y. (2017)

Mikel Lavilla, Andrea Seral, Antonio Murciano, Sonia Molino, Pablo de la Fuente, Jose María Gabriel y Galán,

Acta Botanica Malacitana 42: 5-13 – DOI:


Stomata are very conserved structures in plants, which allows and control the  gas exchange. This ecophysiological fact appears to be critical in the ecology  and adaptation of plants to environment. Plant individuals can, among other  issues, adjust size and density of the stomata to adapt themselves to hydric,  thermic and light regimes. In turn, this led to the reduction of transpiration and  control of water losses, which is crucial in areas with Mediterranean climate. The  fern  Osmunda regalis  has populations in both biogeographical regions of the  Iberian Peninsula (Eurosiberian and Mediterranean regions), but when locations  are highly continental the populations are scarce and isolated. The objective of  this study is to characterize the stomatal morphological traits in both regions, to  detect possible adaptations in individuals occurring in Mediterranean locations.  26 individuals of 17 different populations were sampled. Applying microscopic  techniques, 4447 observations of length and width, and 234 of density and PCI  were done. The sampling spots were characterized by two bioclimatic indices of  Emberger and Gorzynski, and also mean maximum and minimum temperature  values were obtained. All the information was included in a dataset that was  statistically analyzed with the software SPSS. Our results show that  Osmunda  regalis  fronds have higher PCI and density values in the Eurosiberian region,  as expected. Gorczynski continentality index (K), and the mean maximum and  minimum annual temperatures influences over stomatal traits. This is clearly  informing that in the Mediterranean region, the temperature is an important  factor that triggers stomatal adaptations of  O. regalis  to continental locations with  higher levels of environmental stress. On the contrary, Emberger pluviometric  index (Q) seems to be less explicative by its own. Perhaps this is related with  the habitat of  O. regalis  in soils with high freatic level, fact which could lead to a  more independent stomata from rainfall.

Stomata in Microgramma (Polypodiaceae)

On the histochemical diagnostic characters of leaves from Microgramma squamulosa (Kaulf.) Sota (Polypodiaceae)

Jaime G. S., Barboza G., Vattuone M. A. (2007)

Gloria S. Jaime1 , G. Barboza2, M.A. Vattuone3,
1 Cátedra de Botánica y Cátedra de Fitoquímica

2 IMBIV.UNC. Argentina

3 Instituto de Estudios Vegetales. Fac. Bioq.Qca.y Farm. UNT. Ayacucho 471. San
Miguel de Tucumán.


Boletín Latinoamericano y del Caribe de
Plantas Medicinales y Aromáticas

Bol. Latinoam. Caribe Plant. Med. Aromaticas 6(5):195-196 – ISSN: 0717-7917 –


En este trabajo se realiza el estudio exo-endomorfológico e histoquímico de las frondes de Microgramma squamulosa (Kaulf.) Sota,
“calaguala del mate”, especie empleada en medicina popular como antiulcerosa. Se obtuvieron parámetros micrográficos diagnósticos de M. squamulosa:
hojas hipostomáticas, estomas estaurocíticos, índice estomático = 5.76, hipodermis colenquimática en lámina y esclerenquimática en nervio medio; en
pecíolo esclerenquimática, con desarrollo de esclereidas en parénquima peciolar de hojas maduras que permiten reconocer la droga cruda ante eventuales
controles de calidad. Los tests histoquímicos demostraron la presencia de compuestos fenólicos y flavonoides de interés farmacológico.


The aim of this work was to study leaf, and petiole anatomical and histochemical characters of Microgramma squamulosa (Kaulf.) Sota, a fern belonging to Polypodiáceas (Pteridofitas). This species, popularly known as “calaguala del mate” in Argentina, is used in our folk medicine as antiulcer. In this contribution we describe the histological aspects that could help to identify the crude drug. Diagnostic micrographic parameters were obtained of this species: hipostomatic leaf, staurocytic stomata, stomata index = 5.76, collenchymatous hypodermis in blade and midrib with sclerenchyma; alone sclerenchymatic in petiole of mature leaves.

Hypodermal tissue and the occurrence of stomata at the abaxial face are typical characteristics of xeromorphic leaves

Leaf dimorphism of Microgramma squamulosa (Polypodiaceae): a qualitative and quantitative analysis focusing on adaptations to epiphytism

Rocha L. D., Droste A., Gehlen G., Schmitt J. L. (2013)

Ledyane Dalgallo Rocha1, Annette Droste1, Günther Gehlen1 , Jairo Lizandro Schmitt1

Rev. biol. trop 61(1) –  San José Mar. – Revista de Biología Tropical – On-line version ISSN 0034-7744 – Print version ISSN 0034-7744 –


The epiphytic fern Microgramma squamulosa occurs in the Neotropics and shows dimorphic sterile and fertile leaves. The present study aimed to describe and compare qualitatively and quantitatively macroscopic and microscopic structural characteristics of the dimorphic leaves of M. squamulosa, to point more precisely those characteristics which may contribute to epiphytic adaptations. In June 2009, six isolated host trees covered by M. squamulosa were selected close to the edge of a semi-deciduous seasonal forest fragment in the municipality of Novo Hamburgo, State of Rio Grande do Sul, Brazil. Macroscopic and microscopic analyzes were performed from 192 samples for each leaf type, and permanent and semi-permanent slides were prepared. Sections were observed under light microscopy using image capture software to produce illustrations and scales, as well as to perform quantitative analyses. Fertile and sterile leaves had no qualitative structural differences, being hypostomatous and presenting uniseriate epidermis, homogeneous chlorenchyma, amphicribal vascular bundle, and hypodermis. The presence of hypodermal tissue and the occurrence of stomata at the abaxial face are typical characteristics of xeromorphic leaves. Sterile leaves showed significantly larger areas (14.80cm2), higher sclerophylly index (0.13g/cm2) and higher stomatal density (27.75stomata/mm2) than fertile leaves. The higher sclerophylly index and the higher stomatal density observed in sterile leaves are features that make these leaves more xeromorphic, enhancing their efficiency to deal with limited water availability in the epiphytic environment, compared to fertile leaves.


El helecho epífito Microgramma squamulosa se encuentra en el Neotrópico y tiene hojas estériles y fértiles dimorfas. El objetivo de este estudio fue describir y comparar cuantitativa y cualitativamente la  organización estructural de las hojas de la M. squamulosa, investigando las características morfológicas y anatómicas, y señalando los factores que contribuyen a la adaptación al  ambiente epífito. Los análisis macroscópicos y microscópicos se realizaron a partir de 192 muestras de hojas de cada tipo. Láminas permanentes y semi-permanentes fueron  preparadas y las secciones fueron observadas en el microscopio de luz. Hojas fértiles y estériles no mostraron diferencias estructurales  cualitativas, son hipostomáticas, presentan epidermis uniseriada, haz vascular anficrival e hipodermis. La presencia de hipodermis y aparatos estomáticos en la nsuperficie abaxial de la epidermis son típicas de hojas xeromórficas. Hojas estériles presentaran  áreas significativamente mayores, tasa más alta de esclerofilia y mayor densidad de estomas que hojas fértiles. La mayor tasa de esclerofilia y mayor densidad de estomas son características que hacen las hojas estériles más xeromórficas, aumentando su eficiencia para hacer frente a la disponibilidad de agua limitada en el ambiente epífito, en comparación con las hojas fértiles.

Stomata in the Lateral-Line Aerenchyma in Bracken Ferns

Structure and Development of the Lateral-Line Aerenchyma in Bracken Ferns (Pteridium: Dennstaedtiaceae)

Barton D. A., Overall R. L., Thomson J. A. (1979)

Deborah A. BartonRobyn L. OverallJohn A. Thomson,

International Journal of Plant Sciences 176(7): –


Premise of research. Bracken ferns have a worldwide distribution. Plants consist of aerial fronds with petioles (stipes) that extend underground to specialized subterranean stems (rhizomes). A narrow continuous surface strip of specialized aerenchyma on each side of rhizomes and stipes, referred to as the lateral line, forms a pathway for gases. Developmental changes in the lateral line appear to affect gas exchange and influence water relations, soil exploitation, dormant survival, and disease resistance in these plants. An integrated account of the ontogeny and cytochemistry of the lateral line in the rhizomes and stipes of Pteridium has not been published.

Methodology. LM with fluorescence cytochemistry, supported by SEM, was used to compare developmental changes in tissues of the lateral-line aerenchyma in the stipes (petioles) and rhizomes (stems) of representative bracken taxa.

Pivotal results. The lateral lines of the rhizome and stipe in Pteridium aquilinum and Pteridium esculentum are a continuous organ. Developmental changes in the lateral lines of stipe and rhizome are similar. Cell walls of the closed lateral line but not the rind of the mature rhizome and the stipe belowground are rich in tannins. Intercellular protuberances extending from the walls of parenchyma cells below the lateral lines are primarily composed of pectin and polyphenols and contain tannin only late in development. Stomata of the lateral lines of the stipe above ground remain functional until frond senescence.

Conclusions. The lateral-line aerophores in the stipe and rhizome of bracken ferns are continuous, with similar anatomy, development, and likely roles in aeration and resistance to waterlogging.

Stomata of Pteridaceae

Leaf epidermal micromorphology and its implications in systematics of certain taxa of the fern family Pteridaceae from Northern Pakistan

Shah S. N., Celik A., Ahmad M., Ullah F., Zaman W., Zafar M., Malik K., Rashid N., Iqbal M., Sohail A., Bahadur S. (2019)

Syed Nasar Shah 1Ali Celik 2Mushtaq Ahmad 1Fazal Ullah 1 3 4Wajid Zaman 1 5 4Muhammad Zafar 1Khafsa Malik 1Neelam Rashid 1Majid Iqbal 1Aamir Sohail 6Saraj Bahadur 1

  • 1Department of Plant Sciences, Quaid-i-Azam University Islamabad, Islamabad, Pakistan.
  • 2Department of Biology, Faculty of Arts and Sciences, Pamukkale University, Denizli, Turkey.
  • 3CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China.
  • 4University of Chinese Academy of Sciences, Beijing, China.
  • 5State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China.
  • 6Department of Botany, University of Peshawar, Peshawar, Pakistan.


PMID: 30582243 – DOI: 10.1002/jemt.23174


The present study is insights into foliar epidermal anatomy for characterizing clades, and their utility in taxonomic segregation of certain species of Pteridaceae from Northern Pakistan. The leaf epidermal anatomy of 10 species of Pteridaceae representing four genera were examined using light and scanning electron microscope. A micromorphological matrix was constructed for eight qualitative and 12 quantitative characters. unweighted pair group method with arithmetic means and principal components analysis statistical analysis were performed to test the validity of foliar epidermal anatomical features as method of separating species and genera, and phylogenetic clusters among species are constructed using qualitative and quantitative traits. The qualitative characters described here are shape of epidermal cells, stomata, guard cell and subsidiary cells, anticlinal wall pattern, and trichomes types which is helpful in defining groups within Pteridaceae. In addition, the size of stomata, guard cells, subsidiary cells, stomatal pore epidermal cells, and trichomes are quantitatively analyzed. All species have hypostomatic leaves. Two types of stomata were observed in studied species, anomocytic and polocytic. Anomocytic stomata were observed in three genera namely: Adiantum, Onychium, and Chielanthes whereas Pteris can be discriminated from other genera by its polocytic stomata. On the basis of multivariate analysis present study does provides sufficient information on the taxonomic importance of foliar anatomy which validate its efficacy in species and genera discrimination. From result obtained here it is further possible to use leaf micromorphologic data in ferns phylogeny and providing basis for future taxonomic delimitation in other taxa.

‘Floating’ guard cell mother cells in Anemia

Studies on the formation of ‘floating’ guard cell mother cells in Anemia

Galatis B., Apostolakos P., Palafoutas D. (1986)

J Cell Sci. 80: 29-55 – PMID: 3722283 –


The protodermal cells producing the ‘floating’ guard cell mother cells (GMCs) in three Anemia species undergo an extraordinary polarization and an unexpected shaping. During interphase an intercellular space is initiated at the internal proximal end of the cell, while the polar region bulges outwards. At this stage a microtubule girdle traverses the cortical cytoplasm underneath the rims of the external periclinal wall curvature. In addition, another system of microtubules converges on a cortical site adjoining the wall delimiting the intercellular space and, or, the neighbouring region of the internal periclinal wall (internal polar cortical site, IPCS). Vacuoles are found in all regions of the cell except for that between the centrally located nucleus and the intercellular space. As the cell approaches mitosis, the growing vacuolar system retreats from the cytoplasmic region below the external periclinal wall curvature. In most cells the polarized cytoplasm forms an inclined truncated cone, the bases of which abut on the external periclinal wall curvature and the wall lining the IPCS. The organization of the cortical microtubule cytoskeleton does not change significantly during preprophase-prophase. A preprophase microtubule band (PMB) is localized in the cortex lining the rims of the external periclinal wall curvature, while some microtubules traverse the IPCS and the cytoplasm adjacent to the neighbouring wall regions. The mitotic spindle axis is diagonal, while the cell plate separating the GMCs exhibits an unusual mode of growth. It gradually encircles the proximal daughter nucleus, becoming funnel-shaped. One of its periclinal edges fuses with the external periclinal wall area lined by the PMB cortical zone and the other with the internal periclinal wall area adjoining the IPCS. The latter region seems to behave like the PMB cortical zone. The results show that the morphogenetic mechanism underlying the formation of the conical GMCs includes a series of highly integrated processes, initiated or carried out during cell polarization.

Stomata of the seed fern Alethopteris sullivanti

Stomata of Alethopteris sullivanti: a new stomatal type among seed ferns and vascular plants

Stidd B. M. (1988)

Benton M. Stidd, Western Illinois University, Macomb, Illinois 61455


American Journal of Botany 75(6): 790-796 – –  ISSN 0002-9122


Observations based on new preparations confirm the presence of four cells in parallel alignment in A. sullivanti stomata but not with two flanking subsidiary cells as in paracytic stomata. Rather, each guard cell contains in its interior a smaller inner cell. The stomatal pore is formed by walls of the larger cells and it is not known what role, if any, the interior cells may have played in opening and closing the pore. This cell-within-a-cell arrangement is unknown among stomata elsewhere in the plant kingdom. The inner cells have the appearance of guard cells, especially when the poral walls of the larger cells are removed, and were so designated by Oestry Stidd and Stidd (1976). Cuticle preparations (Reihman and Schabilion, 1985) leave most of the cell structure of the stomatal apparatus intact among other leaf tissues (are not removed with the cuticle) and therefore do not reveal essential features.

An active mechanism of stomatal regulation in response to reduced air humidity is present in some ferns.

Fern Stomatal Responses to ABA and CO 2 Depend on Species and Growth Conditions

Hõrak H., Kollist H., Merilo E. (2017)

Hanna Hõrak 1, Hannes Kollist 1, Ebe Merilo 2

  • Plant Signal Research Group, University of Tartu, Institute of Technology, Tartu 50411, Estonia.
  • 2Plant Signal Research Group, University of Tartu, Institute of Technology, Tartu 50411, Estonia


Plant Physiol. 174(2): 672-679 – doi: 10.1104/pp.17.00120. Epub 2017 Mar 28 –


Changing atmospheric CO2 levels, climate, and air humidity affect plant gas exchange that is controlled by stomata, small pores on plant leaves and stems formed by guard cells. Evolution has shaped the morphology and regulatory mechanisms governing stomatal movements to correspond to the needs of various land plant groups over the past 400 million years. Stomata close in response to the plant hormone abscisic acid (ABA), elevated CO2 concentration, and reduced air humidity. Whether the active regulatory mechanisms that control stomatal closure in response to these stimuli are present already in mosses, the oldest plant group with stomata, or were acquired more recently in angiosperms remains controversial. It has been suggested that the stomata of the basal vascular plants, such as ferns and lycophytes, close solely hydropassively. On the other hand, active stomatal closure in response to ABA and CO2 was found in several moss, lycophyte, and fern species. Here, we show that the stomata of two temperate fern species respond to ABA and CO2 and that an active mechanism of stomatal regulation in response to reduced air humidity is present in some ferns. Importantly, fern stomatal responses depend on growth conditions. The data indicate that the stomatal behavior of ferns is more complex than anticipated before, and active stomatal regulation is present in some ferns and has possibly been lost in others. Further analysis that takes into account fern species, life history, evolutionary age, and growth conditions is required to gain insight into the evolution of land plant stomatal responses.