Scientific Papers. Series A. Agronomy, Vol. LX, 2017 ISSN 2285-5785; ISSN CD-ROM 2285-5793; ISSN Online 2285-5807; ISSN-L 2285-5785 Biological material conducting fascicules and, in central, the According to IUCN Red List of Threatened medullary lacuna (Figure 3b). MORPHOLOGICAL CHARACTERIZATION OF Alisma plantago-aquatica L. Species, A. plantago-aquatica is an herbaceous (Alismataceae): A CASE STUDY AND LITERATURE REVIEW amphibious helophyte (Lansdown, 2014). For the vegetation of Bugeac Lake, water- Emilia Brînduşa SĂNDULESCU, Nicoleta OLTENACU, plantain was reported as helohydatophyte Mala-Maria STAVRESCU-BEDIVAN species, belonging to Schoenoplectetum taber- naemontani association (Dinu and Radu, 2004). University of Agronomic Sciences and Veterinary Medicine of Bucharest, Faculty of Agriculture, 59 Mărăşti Blvd., 011464, Bucharest, Romania
Corresponding author email: [email protected] Figure 3 a. A. plantago-aquatica: cross section of the stem (magnification x6) Abstract
This study focuses on some structural features noticed in Alisma plantago-aquatica. With plant material collected from assimilating Bugeac Lake (Dobrudja), the morphological analysis of water-plantain’s vegetative organs is reported herein. In our parenchyma survey, cross-sections were performed throughout the stem and stalk. Also, we examined the literature knowledge on A. Figure 1. Wetland ecosystem hosting Nymphoides plantago-aquatica, in terms of importance and adaptative changes of this perennial plant to wetland ecosystems peltata, Butomus umbellatus and A. plantago-aquatica sclerenchyma highlighted by characteristics of leaves and root system. (Bugeac Lake, August 2014)
Key words: Alisma plantago-aquatica, wetland, vegetative organs, cross section. For this report, we used ethanol preserved
material belonging to Alisma plantago-
aquatica. The plants were collected by hand- INTRODUCTION (Savinykh et al., 2015). Regarded as a desirable pulling, in August 2014 (Figure 2). species in wetlands, water-plantain may be Several transversal sections were performed The species of Alisma aquatic genus are mainly used to stabilize the metals in the substrate and Figure 3 b. Cross section of the stem in through the stem and stalks of inflorescence A. plantago-aquatica, showing parenchyma found in the northern hemisphere, growing in can be eaten by animals (Fritioff, 2005; (peduncle) of water-plantain, using razor and mechanical tissues (magnification x20) the muddy edges of marshes and lakes http://www.pir.sa.gov.au/). blades. (Robinson, 2004). Common water-plantain, The human interest in studying this plant species The morphological features were described The mixed conducting fascicules are Alisma plantago-aquatica L. (Alismatales. is based on its use in ornamental gardens and for with an ML-4M IOR microscope. collaterally closed-type, arranged in two-three Alismataceae) is a shoreline plant, charac- medicinal purposes (Lansdown, 2014). concentric circles. terized by lance-shaped leaves, with many tiny The aim of this paper is to list and describe the The small, external (Figure 4a) and the large, pale lilac flowers blooming from June to main features and morpho-anatomical struc- internal ones (Figure 4b) are surrounded by August, each with three petals and three sepals, tures, responsible for living of water-plantain in sclerenchyma. disposed on a pyramid-shape inflorescence, wetland environments. taller than the rest of the plant As Kırım et al. (2014) suggested, all the
(http://www.nzpcn.org.nz/; https://agr.mt.gov/). inhabitants of the wetland have to be protected, Also known as devil's spoons, mad dog weed since they are important for biological or thumbwort, this wetland perennial plant is a diversity. widespread species occurring from Northern
Europe to Africa and Southeast Asia and is MATERIALS AND METHODS reported native in Romania a (http://www.kew.org/science-conservation/; Area description Figure 2. A. plantago-aquatica growing on the shores of Lansdown, 2014). In a previous study, we described the Bugeac Bugeac Lake (see the arrow)
As far as we know, A. plantago-aquatica was Lake area from southwest of Dobrudja analyzed before in terms of phytochemical (44°05'30.6"N, 27°25'45.2"E), where another RESULTS AND DISCUSSIONS compounds (Chau et al., 2007), water and os- freshwater plant - Nymphoides peltata - was motic potentials (Klymchuk et al., 2008), collected and cross-sectioned in order to follow The morphological features of water- plantain from Bugeac Lake phenotypic plasticity (Kordyum et al., 2012), the morpho-anatomy adaptations to environ- In cross section, the stem of water-plantain embryogenesis (Świerczyńska and Bohdanowicz, ment (Săndulescu et al., 2016). b 2014), heavy metal adsorption (Ushakumary Bugeac Lake, a natural wetland ecosystem (Figure 3a) collected from the lakeshore of and Madhu, 2014), genome size (Hidalgo et al., hosting several species, including water-plan- Bugeac Lake presented: epidermis, assimilating Figure 4. Conducting fasicules in A . plantago-aquatica: 2015) and biomorphological adaptations tain is represented in Figure 1. parenchyma, sclerenchyma (mechanical tissue), a. external; b. internal (magnification x 20) 526
Biological material conducting fascicules and, in central, the According to IUCN Red List of Threatened medullary lacuna (Figure 3b). MORPHOLOGICAL CHARACTERIZATION OF Alisma plantago-aquatica L. Species, A. plantago-aquatica is an herbaceous (Alismataceae): A CASE STUDY AND LITERATURE REVIEW amphibious helophyte (Lansdown, 2014). For the vegetation of Bugeac Lake, water- Emilia Brînduşa SĂNDULESCU, Nicoleta OLTENACU, plantain was reported as helohydatophyte Mala-Maria STAVRESCU-BEDIVAN species, belonging to Schoenoplectetum taber- naemontani association (Dinu and Radu, 2004). University of Agronomic Sciences and Veterinary Medicine of Bucharest, Faculty of Agriculture, 59 Mărăşti Blvd., 011464, Bucharest, Romania
Corresponding author email: [email protected] Figure 3 a. A. plantago-aquatica: cross section of the stem (magnification x6) Abstract
This study focuses on some structural features noticed in Alisma plantago-aquatica. With plant material collected from assimilating Bugeac Lake (Dobrudja), the morphological analysis of water-plantain’s vegetative organs is reported herein. In our parenchyma survey, cross-sections were performed throughout the stem and stalk. Also, we examined the literature knowledge on A. Figure 1. Wetland ecosystem hosting Nymphoides plantago-aquatica, in terms of importance and adaptative changes of this perennial plant to wetland ecosystems peltata, Butomus umbellatus and A. plantago-aquatica sclerenchyma highlighted by characteristics of leaves and root system. (Bugeac Lake, August 2014)
Key words: Alisma plantago-aquatica, wetland, vegetative organs, cross section. For this report, we used ethanol preserved
material belonging to Alisma plantago-
aquatica. The plants were collected by hand- INTRODUCTION (Savinykh et al., 2015). Regarded as a desirable pulling, in August 2014 (Figure 2). species in wetlands, water-plantain may be Several transversal sections were performed The species of Alisma aquatic genus are mainly used to stabilize the metals in the substrate and Figure 3 b. Cross section of the stem in through the stem and stalks of inflorescence A. plantago-aquatica, showing parenchyma found in the northern hemisphere, growing in can be eaten by animals (Fritioff, 2005; (peduncle) of water-plantain, using razor and mechanical tissues (magnification x20) the muddy edges of marshes and lakes http://www.pir.sa.gov.au/). blades. (Robinson, 2004). Common water-plantain, The human interest in studying this plant species The morphological features were described The mixed conducting fascicules are Alisma plantago-aquatica L. (Alismatales. is based on its use in ornamental gardens and for with an ML-4M IOR microscope. collaterally closed-type, arranged in two-three Alismataceae) is a shoreline plant, charac- medicinal purposes (Lansdown, 2014). concentric circles. terized by lance-shaped leaves, with many tiny The aim of this paper is to list and describe the The small, external (Figure 4a) and the large, pale lilac flowers blooming from June to main features and morpho-anatomical struc- internal ones (Figure 4b) are surrounded by August, each with three petals and three sepals, tures, responsible for living of water-plantain in sclerenchyma. disposed on a pyramid-shape inflorescence, wetland environments. taller than the rest of the plant As Kırım et al. (2014) suggested, all the
(http://www.nzpcn.org.nz/; https://agr.mt.gov/). inhabitants of the wetland have to be protected, Also known as devil's spoons, mad dog weed since they are important for biological or thumbwort, this wetland perennial plant is a diversity. widespread species occurring from Northern
Europe to Africa and Southeast Asia and is MATERIALS AND METHODS reported native in Romania a (http://www.kew.org/science-conservation/; Area description Figure 2. A. plantago-aquatica growing on the shores of Lansdown, 2014). In a previous study, we described the Bugeac Bugeac Lake (see the arrow)
As far as we know, A. plantago-aquatica was Lake area from southwest of Dobrudja analyzed before in terms of phytochemical (44°05'30.6"N, 27°25'45.2"E), where another RESULTS AND DISCUSSIONS compounds (Chau et al., 2007), water and os- freshwater plant - Nymphoides peltata - was motic potentials (Klymchuk et al., 2008), collected and cross-sectioned in order to follow The morphological features of water- plantain from Bugeac Lake phenotypic plasticity (Kordyum et al., 2012), the morpho-anatomy adaptations to environ- In cross section, the stem of water-plantain embryogenesis (Świerczyńska and Bohdanowicz, ment (Săndulescu et al., 2016). b 2014), heavy metal adsorption (Ushakumary Bugeac Lake, a natural wetland ecosystem (Figure 3a) collected from the lakeshore of and Madhu, 2014), genome size (Hidalgo et al., hosting several species, including water-plan- Bugeac Lake presented: epidermis, assimilating Figure 4. Conducting fasicules in A . plantago-aquatica: 2015) and biomorphological adaptations tain is represented in Figure 1. parenchyma, sclerenchyma (mechanical tissue), a. external; b. internal (magnification x 20) 527
In cross section, the cut edges stalk of the The relatively few studies on A. plantago- As in literature a full study regarding the Klymchuk D., Vorobyova T., Sivash O., Jadko S., 2008. inflorescence (peduncle) has epidermis with aquatica reveal some features of leaves and histoanatomy of A. plantago-aquatica almost Effects of water deficit on the water relations of Alisma plantago-aquatica L. under natural one-layer of large cells, covered by well- root. lack, we anticipate that more research papers environment. Gen. Appl. Plant Physiology, 34(3-4): developed cuticle (Figure 5). Thus, in water-plantain, aerenchyma – repre- are required in order to understand its life and 227-238. sented by large intercellular spaces designed adaptative changes in different environments Kordyum Y.L., Kozeko L.Y., Ovcharenko Y.V., 2012. for oxygen uptake – appears to be present in subject to fluctuating water levels. Phenotypic plasticity of aerial-aquatic plants Alisma stem, leaves and root (Kordyum et al., 2012). plantago-aquatica L. and Sium latifolium L.: structural and molecular aspects. Botanica 3 (52): 11-16. As Jung et al. (2008) stated, a well-developed ACKNOWLEDGEMENTS Lamberti-Raverot B., Puijalon S., 2012. Nutrient aerenchyma is an important feature of wetland enrichment affects the mechanical resistance of plants. This article was financed by the Faculty of aquatic plants. J Exp Bot. 63(17): 6115–6123. The adventive roots of A. plantago-aquatica Agriculture, University of Agronomic Sciences Robinson P., 2004. Rock and water plants. Practical are characterized by the presence of aeren- and Veterinary Medicine of Bucharest. gardening handbook. Anness Publishing, London, 132 pp. chyma surrounded with epidermis and one Savinykh N.P., Shabalkina S.V., Lelekova E. V., 2015. cortex layer. Kordyum et al. (2012) who REFERENCES Biomorphological adaptations of helophytes. studied the root anatomy of mature A. Contemporary Problems of Ecology 8 (5): 550–559. Bercu R., 2009. Histonanatomy of Echinodorus Figure 5. A. plantago-aquatica: cross sections plantago-aquatica, have noted that the Săndulescu E.B., Vasile Scăeţeanu G., Şchiopu T., cordifolius (L.) Griseb. (Alismataceae). Studia (x6; x 20) of the stalk Oltenacu N., Stavrescu-Bedivan M.M., 2016. presence or absence of aerenchima depends on Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii Morpho-anatomy and adaptation to some Romanian changes in water supply: in plant species 19, 2: 283-286. aquatic environments of Nymphoides peltata (Gmel.) The conducting tissues of the stalk is growing on riverside, the root system has small Chau V.M., Phan V.K., Pham H.Y., Tran T.H., Braca A., O. Kuntze (Asterales: Menyanthaceae). Scientific represented by both phloem and xylem bundles, intercellular spaces, similar to terrestrial plants 2007. Protostane-type triterpenes from the rhizomes Papers. Series A. Agronomy, LIX: 537-542. collaterally-closed type, irregularly disposed in of the same species. of Alisma plantago-aquatica. Tap Chi Hoa Hoc. Seago Jr. J., Marsh L., Stevens K., Soukup A., two rows, surrounded by mechanical tissue of 45(1):120-125. Votrubova O., Enstone D., 2005. A re-examination of Furthermore, according to Seago et al. (2005), Fritoff A., 2005. Metal accumulation by plants. sclerenchyma (Figure 6). the root cortex in wetland flowering plants with there are wetland plant roots which do not have Evaluation of the use of plants in storm water respect to aerenchyma. Annals of Botany 96: 565– any aerenchyma tissue. treatment. PhD thesis, pp.56, https://www.diva- 579. The light micrograph of a section through a leaf portal.org/smash/. Świerczyńska J., Bohdanowicz J., 2014. Alisma stalk (petiole) of A. plantago-aquatica, showed: Hidalgo O., Garcia S., Garnatje T., Mumbrú M., plantago-aquatica L.: the cytoskeleton of the Patterson A., Vigo J., Vallès J., 2015. Genome size in suspensor development. Acta Soc Bot Pol 83(2): 159- an epidermis covered by a thin cuticle, outer aquatic and wetland plants: fitting with the large 166. cortex represented by three layers of paren- genome constraint hypothesis with a few relevant Ushakumary E.R., Madhu G., 2014. Studies on Zinc (II) chyma cells, middle cortex with lacunar spaces, exceptions. Plant Systematics and Evolution 301(7): Adsorption Using Alisma plantago-aquatica. Journal inner cortex and large vascular bundles 1927-1936. of Clean Energy Technologies, 2 (2): 112-117. consisting in endodermis, a ring of phloem, a Jung J., Lee S.C., Choi H-K., 2008. Anatomical patterns ***http://www.nzpcn.org.nz/flora_details.aspx?ID=2433 of aerenchyma in aquatic and wetland plants. Journal ***https://agr.mt.gov/Portals/168/Documents/Archive/W ring of xylem and the pith at the centre of Plant Biology 51 (6): 428-439. eeds/Aquatics_Guide-Shoreline_Plants.pdf (http://www.sciencephoto.com/). Kırım B., Coban D., Güler M., 2014. Floating aquatic ***http://www.kew.org/science-conservation/plants- plants and their impact on wetlands in Turkey. fungi/alisma-plantago-aquatica-common-water- Available on: plantain CONCLUSIONS http://www.limnology.ro/water2014/proceedings/13_ ***http://www.sciencephoto.com/media/663212/view Figure 6. Conducting fascicules in the stalk Birsen.pdf
of A. plantago-aquatica (x20) The case study and also the literature survey revealed some structural characteristics and The supporting tissues represented by adaptations of water-plantain for living under sclerenchyma characterized by thickened cell wetland conditions. cellulose walls, lead to strength and stiffness In terms of A. plantago-aquatica, we focused to involved in aquatic plant resistance (Lamberti- the knowledge of morphological structure of Raverot and Puijalon, 2012). this plant species, by describing the cross section of the stem and stalk. The previous The morphological features of water- reports investigated mainly the root ant the leaf plantain: a literature review of this species. As far as we know, the available data Unlike other reports, in the stem of A. concerning morpho-anatomy of the Alisma plantago-aquatica collected from the shore of genus members are still scarce. A Romanian Bugeac Lake in summer of 2014 the researcher investigated the anatomy of aerenchyma was not present, instead a central adventitious root, rhizome and leaf in Alisma medullary lacuna was present. cordifolia L. (Bercu, 2009). 528
In cross section, the cut edges stalk of the The relatively few studies on A. plantago- As in literature a full study regarding the Klymchuk D., Vorobyova T., Sivash O., Jadko S., 2008. inflorescence (peduncle) has epidermis with aquatica reveal some features of leaves and histoanatomy of A. plantago-aquatica almost Effects of water deficit on the water relations of Alisma plantago-aquatica L. under natural one-layer of large cells, covered by well- root. lack, we anticipate that more research papers environment. Gen. Appl. Plant Physiology, 34(3-4): developed cuticle (Figure 5). Thus, in water-plantain, aerenchyma – repre- are required in order to understand its life and 227-238. sented by large intercellular spaces designed adaptative changes in different environments Kordyum Y.L., Kozeko L.Y., Ovcharenko Y.V., 2012. for oxygen uptake – appears to be present in subject to fluctuating water levels. Phenotypic plasticity of aerial-aquatic plants Alisma stem, leaves and root (Kordyum et al., 2012). plantago-aquatica L. and Sium latifolium L.: structural and molecular aspects. Botanica 3 (52): 11-16. As Jung et al. (2008) stated, a well-developed ACKNOWLEDGEMENTS Lamberti-Raverot B., Puijalon S., 2012. Nutrient aerenchyma is an important feature of wetland enrichment affects the mechanical resistance of plants. This article was financed by the Faculty of aquatic plants. J Exp Bot. 63(17): 6115–6123. The adventive roots of A. plantago-aquatica Agriculture, University of Agronomic Sciences Robinson P., 2004. Rock and water plants. Practical are characterized by the presence of aeren- and Veterinary Medicine of Bucharest. gardening handbook. Anness Publishing, London, 132 pp. chyma surrounded with epidermis and one Savinykh N.P., Shabalkina S.V., Lelekova E. V., 2015. cortex layer. Kordyum et al. (2012) who REFERENCES Biomorphological adaptations of helophytes. studied the root anatomy of mature A. Contemporary Problems of Ecology 8 (5): 550–559. Bercu R., 2009. Histonanatomy of Echinodorus Figure 5. A. plantago-aquatica: cross sections plantago-aquatica, have noted that the Săndulescu E.B., Vasile Scăeţeanu G., Şchiopu T., cordifolius (L.) Griseb. (Alismataceae). Studia (x6; x 20) of the stalk Oltenacu N., Stavrescu-Bedivan M.M., 2016. presence or absence of aerenchima depends on Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii Morpho-anatomy and adaptation to some Romanian changes in water supply: in plant species 19, 2: 283-286. aquatic environments of Nymphoides peltata (Gmel.) The conducting tissues of the stalk is growing on riverside, the root system has small Chau V.M., Phan V.K., Pham H.Y., Tran T.H., Braca A., O. Kuntze (Asterales: Menyanthaceae). Scientific represented by both phloem and xylem bundles, intercellular spaces, similar to terrestrial plants 2007. Protostane-type triterpenes from the rhizomes Papers. Series A. Agronomy, LIX: 537-542. collaterally-closed type, irregularly disposed in of the same species. of Alisma plantago-aquatica. Tap Chi Hoa Hoc. Seago Jr. J., Marsh L., Stevens K., Soukup A., two rows, surrounded by mechanical tissue of 45(1):120-125. Votrubova O., Enstone D., 2005. A re-examination of Furthermore, according to Seago et al. (2005), Fritoff A., 2005. Metal accumulation by plants. sclerenchyma (Figure 6). the root cortex in wetland flowering plants with there are wetland plant roots which do not have Evaluation of the use of plants in storm water respect to aerenchyma. Annals of Botany 96: 565– any aerenchyma tissue. treatment. PhD thesis, pp.56, https://www.diva- 579. The light micrograph of a section through a leaf portal.org/smash/. Świerczyńska J., Bohdanowicz J., 2014. Alisma stalk (petiole) of A. plantago-aquatica, showed: Hidalgo O., Garcia S., Garnatje T., Mumbrú M., plantago-aquatica L.: the cytoskeleton of the Patterson A., Vigo J., Vallès J., 2015. Genome size in suspensor development. Acta Soc Bot Pol 83(2): 159- an epidermis covered by a thin cuticle, outer aquatic and wetland plants: fitting with the large 166. cortex represented by three layers of paren- genome constraint hypothesis with a few relevant Ushakumary E.R., Madhu G., 2014. Studies on Zinc (II) chyma cells, middle cortex with lacunar spaces, exceptions. Plant Systematics and Evolution 301(7): Adsorption Using Alisma plantago-aquatica. Journal inner cortex and large vascular bundles 1927-1936. of Clean Energy Technologies, 2 (2): 112-117. consisting in endodermis, a ring of phloem, a Jung J., Lee S.C., Choi H-K., 2008. Anatomical patterns ***http://www.nzpcn.org.nz/flora_details.aspx?ID=2433 of aerenchyma in aquatic and wetland plants. Journal ***https://agr.mt.gov/Portals/168/Documents/Archive/W ring of xylem and the pith at the centre of Plant Biology 51 (6): 428-439. eeds/Aquatics_Guide-Shoreline_Plants.pdf (http://www.sciencephoto.com/). Kırım B., Coban D., Güler M., 2014. Floating aquatic ***http://www.kew.org/science-conservation/plants- plants and their impact on wetlands in Turkey. fungi/alisma-plantago-aquatica-common-water- Available on: plantain CONCLUSIONS http://www.limnology.ro/water2014/proceedings/13_ ***http://www.sciencephoto.com/media/663212/view Figure 6. Conducting fascicules in the stalk Birsen.pdf of A. plantago-aquatica (x20) The case study and also the literature survey revealed some structural characteristics and The supporting tissues represented by adaptations of water-plantain for living under sclerenchyma characterized by thickened cell wetland conditions. cellulose walls, lead to strength and stiffness In terms of A. plantago-aquatica, we focused to involved in aquatic plant resistance (Lamberti- the knowledge of morphological structure of Raverot and Puijalon, 2012). this plant species, by describing the cross section of the stem and stalk. The previous The morphological features of water- reports investigated mainly the root ant the leaf plantain: a literature review of this species. As far as we know, the available data Unlike other reports, in the stem of A. concerning morpho-anatomy of the Alisma plantago-aquatica collected from the shore of genus members are still scarce. A Romanian Bugeac Lake in summer of 2014 the researcher investigated the anatomy of aerenchyma was not present, instead a central adventitious root, rhizome and leaf in Alisma medullary lacuna was present. cordifolia L. (Bercu, 2009). 529