Leaf micromorphology and anatomy in the tribe Aristideae (Poaceae) in Iran and its systematic implications

ZAHRA MAASOUMI; MANEEZHEH PAKRAVAN; BEHNAM HAMZEE; ROGHAIEH ZAREI

doi:10.11646/phytotaxa.578.1.4

Issue: Vol. 578 No. 1: 4 January 2023

Type: Article

Published: 2023-01-04

DOI: 10.11646/phytotaxa.578.1.4

Page range: 75-92

Abstract views: 55

PDF downloaded: 1

Leaf micromorphology and anatomy in the tribe Aristideae (Poaceae) in Iran and its systematic implications

ZAHRA MAASOUMI⁺⁻
MANEEZHEH PAKRAVAN⁺⁻
BEHNAM HAMZEE⁺⁻
ROGHAIEH ZAREI⁺⁻

Department of Plant sciences, Faculty of Biological Sciences, Alzahra University, Tehran, Iran

Research Institute of Forests and Rangelands, Agricultural Research, Education and Extention Organization (AREEO), Tehran, Iran

Department of Plant sciences, Faculty of Biological Sciences, Alzahra University, Tehran, Iran

Aristida Leaf epidermis SEM Stipagrostis transverse section Monocots

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Abstract

The present study investigated the leaf anatomy of 12 species belonging to the genera Aristida and Stipagrostis of the Aristideae tribe in Iran. Scanning electron microscopy (SEM) and light microscopy (LM) were used to observe the epidermal characteristics and transverse sections of the leaves to assess taxonomic applications of these traits. The main distinguishing traits of the species included: the presence of prickles, macrohairs and microhairs, papillae and type of wax, adaxial ribs, number of bulliform cells, number of sclerenchymatous layers and shape of silica bodies. When constructing the phenogram of Aristideae using WARD’s method and based on the 7 qualitative and 18 quantitative anatomical traits showed four taxonomic-anatomic clades with a cophenetic correlation coefficient of 1.75. Kranz anatomy in S. raddiana differed from the one seen inS. paradisea. The presence of papillae and lack of macrohairs on the leaf epidermis in S. karelinii distinguished it from S. pennata. By present findings the placement of A. coerulescens as a variety of A. adscensionis has not been ascertained. An identification key is providedbased on anatomical traits.The anatomical features of the leaves were proved to be useful for species delimitation and as a supplementary tool for identifying taxa and macromorphological traits.

References

Anderson, T. (1860) Florule Adenensis. Journal of the Proceedings of the Linnean Society. Botany, London 5 (Suppl. 1): 40.
Balkwill, K., Campbell-Young, G.J., Fish, L., Munday, J., Frean, M.L. & Stalmans, M. (2011) A new species of Sartidia (Graminae), endemic to ultramafic soils. South African Journal of Botany 77: 598–607. http://doi.org/10.1016/ j.sajb.2010.12.003
Barthlott, W., Neinhuis, C., Cutler, D., Ditsch, F., Meusel, I., Theisen, I. & Wilhelmi, H. (1998) Classification and terminology of plant epicuticularwaxes. Botanical Journal of the Linnean Society 126: 237–260. https://doi.org/10.1111/j.1095-8339.1998.tb02529.x
Boissier, E. (1884) Flora Orientalis: sive, Enumeratio plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatarum. vol. 5. H. Georg, Geneva and Basel, pp. 496. https://doi.org/10.5962/bhl.title.20323
Bor, N.L. (1970) Aristideae. In: Rechinger, K.H. (Ed.) Flora Iranica,70. Graz.Akademische Druck-Und Verlagsanstalt, pp. 363–376.
Boykin, L.M., Pokman, W.T., Lowrey, T.K. (2008) Leaf anatomy of Orcuttleae (Poaceae: Chloridoideae): more evidencs of C4 photosynthesis without kranz anatomy. Madrono 55: 143–150.
Brown, W.V. (1977) The Kranz syndrome and its subtypes in grass systematics. In: Jacobs, S.W.L. & Everett, J. (Eds.) Grasses: Systematics and Evolution, CSIRO publishing, Australia. pp. 40.
Cerros-Tlatilpa, R., Columbus, T.J. & Barker, N.P. (2011) Phylogenetic relationships of F Aristida and relatives (Poaceae, Aristoloideae) based on noncoding chloroplast (TRNL-F, RPL16 ) abd nuclear (ITS)DNA sequences. American Journal of Botany 98: 1868–1886. https://doi.org/10.3732/ajb.1100103
Chiovenda, E. (1903) In: Pirotta, R. (ed.) Flora della Colonia Eritrea. Annuario del Reale Istituto Botanico di Romav 3: 48.
Christin, P.A. & Besnard, G. (2009) Two independent C4 origins in Aristidoideae (Poaceae) revealed by the recruitment of distinct phosphoenolpyruvate carboxylase genes. American Journal of Botany 96: 2234–2239.
Clayton, W.D., Harman, K.T. & Williamson, H. (2006) World grass species-synonymy database. The board of trustees of the royal botanical garden, Kew. 
Cope, T.A., Knees, S.G. & Miller, A.G. (2007) Flora of the Arabian peninsula and Socotra, vol. 5 (1). Edinburgh. 387 pp. 
Danin, A.(1996) Adaptations of Stipagrostis species to desert dunes In: Ghasemkhani, M., Akhani, H., Sahebi, J., Scholz, H. The genera Aristida and Stipagrostis (Poaceae) in Iran. Willdenowia 38: 135–148 .
Desfontaines, R. (1798) Flora Atlantica, vol. 1. Sive historia plantarum quae in Atlante, agro tunetano et algeriensi crescunt. Parisiis. pp. 109.
Desfontaines, R.(1809) Emendatio altera ad floram Atlanticam, volumen primum. Neues Journal für die Botanik 3: 255.
De Winter, B. (1963) Notes on the genus Aristida. Kirkia 3: 132–137.
De Winter, B. (1965) The South African Stipeae and Aristideae (Gramineae). Bothalia 8: 201–404.
Edgeworth, M.P. (1847) A couple of hour’s Herborization at Aden. Journal of the Asiatic Society of Bengal 16: 1219.
Ellis, R.P. (1977) Distribution of the Kranz syndrome in the Southern AfricanEragrostoideae and Panicoideae according to bundle sheath anatomyand cytology. In: Sanchez, E., Arriaga, M.O. & Ellis, R.P. KranzDistinctive cells in the culm of Arundinella (Arundinelleae; Panicoideae; Poaceae). Bothalia 19: 45–52.
Ellis, R.P. (1987) A review of comparative leaf blade anatomy in the systematics of the Poaceae: The past twenty-five years. In: Soderstrom, T.R., Hilu, K.W., Campbell, C.S. & Barkworth, M.E. (eds.) Grass Systematics and Evolution. Washington, DC, Smithsonian Institution Press, pp. 3–10.
Ghasemkhani, M., Akhani, H., Sahebi, J. & Scholz, H. (2008) The genera Aristida and Stipagrostis (Poaceae) in Iran. Willdenowia 38: 135–148. https://doi.org/10.3372/wi.38.38108
Gill, L.S. & Mensah, J.K. (1993) Leaf anatomical studies and its bearing on the taxonomy of the tribe Aristideae (Poaceae) from Nigeria. In: Cerros-Tlatilpa, R., Columbus,T.J., Barker, N.P. Phylogenetic relationships of F Aristida and relatives (Poaceae, Aristoloideae) based on noncoding chloroplast (TRNL-F , RPL16 ) abd nuclear (ITS)DNA sequences. American Journal of Botany 98: 1868–1886. https://doi.org/10.3732/ajb.1100103
GPWG [Grass Phylogeny Working Group] (2001) Phylogeny andsubfamilial classifi cation of the grasses (Poaceae). Annals Missouri Botanical Garden 88: 373–457.
Haberlandt, G. (1881)Vergleichende anatomie des assimilatorischen gewebesystems der pflazen. In: Sage, R.F., Li, M. & Monson, R.K. (eds.) C4 Plant Biology, Academic Press. pp. 149–152.
Hattersley, P.W. (1987) Variation in photosynthetic pathway. In: Soderstrom, T.R., Hilu, K.W., Campbell, C.S. & Barkworth, M.E. (eds.) Grass systematics and evolution, Smithsonian Institution Press, Washington, DC, pp. 49–64.
Hattersley, P.W. (1984) Characterization of C4 Type Leaf Anatomy in Grasses (Poaceae). Mesophyll: Bundle Sheath Area Ratios. In: Muhaidat, R., Sage, R.F., Dengler, N.G. Diversity of Kranz anatomy and biochemistry in C4 eudicots. American Journal of Botany 94: 362–381.
Henrard, J.Th. (1929) A monograph of the genus Aristida. Vol. 58. Mededeelingen van’s Rijks Herbarium, Leiden. pp. 1–153. 
Hsiao, C., Jacobs, S.W.L., Barker, P. & Chatterton, N.J. (1998) A molecular phylogeny of the subfamily Arundinoideae (Poaceae): based on sequences of rDNA. Australian Systematic Botany 11: 41–52. https://doi.org/10.1071/SB97001
Hsiao, C., Jacobs, S.W.L., Chatterton, N.J. & Asay, K.H. (1999) A molecular phylogeny of the grass family (Poaceae) based on the sequences of nuclear ribosomal DNA (ITS). In: Soderstrom, T.R., Hilu, K.W., Campbell, C.S. & Barkworth, M.E. (eds.) Grass systematics and evolution. Smithsonian Institution Press, Washington, DC. pp. 49–64
Hubbrad, C.E. (1960) Grasses of Burma, Ceylon, India and Pakistan (excluding Bambuseae). Pergamon Press Oxford UK. pp. 685.
Kalidass, C., Kottaimuthu, R. & Panda, P.C. (2018) Taxonomic enumeration of the tribe Aristideae (Aristidoideae: Poaceae) in India. Plant Science Research 40: 47–50.
Kesler, T.R., Anderson, L.C. & Hermann, S.M. (2003) A taxonomic reevaluation of Aristida stricta (Poaceae) using anatomy and morphology. Southeast Naturalist 2: 1–10. [http://www.jstor.org/stable/3878084]
Khan, R., Ullah, A., Khan, B., Shujaul Mulk Khan, S. & Abdur Rashid, A. (2017) Comparative foliar micromorphological studies of tribe Arundineae, Aristideae and Chlorideaefrom Malakand agency. Pakistan Journal of Botany 49: 33–42.
Koyro, H.W. & Huchzermeyer, B. (2004) Ecophysiological needs of the potential biomass crop Spartina townsendii Grov. Tropical Ecology 45: 123–139.
Linnaeus, C. (1753) Species Plantarum, ed.1, Laurentii Salvius, Stockholm, 560 pp.
Maricle, B.R., Koteyeva, N.K., Voznesenskaya, E.V., Thomasson, J.R. & Edwards, G.E. (2009) Diversity in leaf anatomy, and stomatal distribution and conductance, between salt marsh and freshwater species in the C4 genus Spartina (Poaceae). New Phytologist 184: 216–233. https://doi.org/10.1111/j.1469-8137.2009.02903.x
Martinez-Sagarra, G., Abad, P. & Devesa, J.A. (2017) Study of the leaf anatomy in cross- section in the Iberian species of Festuca L. (Poaceae) and its systematic significance. PhytoKeys 83: 43–74. http://doi.org/10.3897/phytokeys.83.13746
Metcalfe, C.R. (1960) Anatomy of the monocotyledons. Gramineae, Oxford: Clarendon Press.
Metcalfe, C.R. & Clifford, H.T. (1968) Microhairs on grasses. In: Raole, V.M. & Desai, R.J. (2009) Epidermal Studies in some Members of Andropogoneae (Poaceae). Notula Botanicae Horti Agrobotanici Cluj-Napoca 37: 59–64.
Neesvon Esenbeck, C.G.D. (1832) Gramineae, Stipagrostis. Linnaea 7 (3): 290–291.
Nobarinezhad, M.H., Pakravan, M. & Pahlevani, A. (2018) A biosystematic study of Euphorbia subgenus Chamaesyce (Euphorbiaceae) in Iran. Phytotaxa 360: 179–200. https://doi.org/10.11646/phytotaxa.360.3.1
Rozhevitz, R.Y. & Shishkin, B.K. (1934) Flora of the SSSR, Vol. 2. Akademii Nauk SSSR, Leningrad.
Roth-Nebelsick, A., Ebner, M., Miranda, T., Gottschalk, V., Voigt, D., Gorb, S., Stegmaier, T., Sarsour, J., Linke, M. & Konrad, W. (2012) Leaf surface structures enable the endemic Namib desert grass Stipagrostis sabulicola to irrigate itself with fog water. Journal of the Royal Society Interface 9: 1965–1974. https://doi.org/10.1098/rsif.2011.0847.
Sage, R.F., Sage, T.L, Pearcy, R.W. & Borsch, T. (2007) The taxonomic distribution of C4Photosynthesis in Amaranthaceae sensu stricto. American Journal of Botany 94 (12): 1992–2003.
Sage, R.F., Li, M. & Monson, R.K. (1999) C4 Plant Biology, Academic Press. pp. 551–584.
Savi, C.G. (1837) Memorie di Matematica e di Fisica della Società Italiana delle Scienze Residente in Modena, Parte contenente le Memorie di Fisica 21: 198. 
Scholz, H. (1970) Stipagrostis scoparia (Trin. et Rupr.) de Winter auch in Libyen gefunden. Willdenowia 6 (1): 161–166.
Stace, C. (1984) The taxonomic importance of the leaf surface. In: Neinhuis, C. & Barthlott, W. Characterization and distribution of water-repellent, self-cleaning plant surfaces. Annals of Botany 79: 667–677.
Tabaipour, R., Keshavarzi, M. & Ullah, F. (2021) Micromorphological characters variation oflemma and palea in subtribe of Loliinae (Poaceae). Microscopy research and technique 85: 1–18. 
Theirs, B.M. (2019) The world’s herbaria 2018: a summary report based on data from Index Herbariorum, ISSU 3.0. New York.
Thomasson, J.R. (1978) Epidermal patterns of the lemma in some fossil and living grasses and their phylogenetic significance. Science 199: 975–977.
Trinius, C.B. (1818) Mémoires de l’Academie Imperiale des Sciences de St. Petersbourg. Avec l’Histoire de l’Academie 6: 488. 
Trinius, C.B. & Ruprecht, F.J. (1842) Species Graminum Stipaceorum. Academiae imperialis scientiarum, St. Petersburg, 189 pp.
Voznesenskaya, E.V. (1984) Ultrastructure of chlorenchayma in leaves of Stipagrostis karelinii and Stipagrostispennata (Poaceae).Botanicheskii Zhurnal 69: 1195–1198.
Voznesenskaya, E.V., Chuong, S.D.X., Kiirats,O., Franceschi, V.R. & Edwards, G.E. (2005a) Evidence that C4 species in genus Stipagrostis, family Poaceae, are NADP-malic enzyme subtype with nonclassical type of Kranz anatomy (Stipagrostoid). Plant Science 168: 731–739. https://doi.org/10.1016/j.plantsci.2004.10.005
Voznesenskaya, E.V., Chuong, S.D.X., Koteyeva, N.K., Edwards, G.E. & Franceschi, V.R. (2005b) Functional compartmentation of C4photosynthesis in the triple layered chlorenchyma of Aristida (Poaceae). Functional Plant Biology 32: 67–77.
Watson, L. & Dallwitz, M.J. (1992) Grass genera of the World, CAB International. Wallingford, Canada.
Wrobel, A., Nobis, M. & Nowak, A. (2017) Patterns of the lemma micromorphology: A useful tool in taxonomy of the middle Asian Eragrostisspecies (Poaceae). Botany Letter 164: 253–262. https://doi.org/10.1080/23818107.2017.1339293
Zhang, Y.X., Zhang, C.X. & Li, D.Z. (2014) Scanning electron microscopy of the leaf epidermis in Arundinarieae (Poaceae, Bambusoideae): Evolutionary implications of selected micrimorphological features. Botanical Journal of the Linnean Society 176: 45–65.