Abstract
The micromorphology of the leaf epidermis of 11 species across four sections of southern African Strychnos was investigated using light microscopy and scanning electron microscopy. In addition to this, preliminary genome size was assessed with flow cytometry. Qualitative and quantitative results are presented for stomata, trichome and cuticular wax features with an emphasis on the abaxial epidermal surface. A correlated combination of these microscopic features was able to distinguish successfully among the 11 species of Strychnos found in the subcontinent. However, micromorphological evidence does not support the current circumscription of the sections. The often-confused S. gerrardii and S. madagascariensis are distinguishable on leaf micromorphological grounds. Stomata and trichome features show remarkable patterns that largely correlate with the ecological distribution of Strychnos species as either forest or savanna inhabitants. The significant variability in stomatal length across species is hypothesized to be indicative of possible existence of variable ploidy levels within the genus in southern African. However, preliminary genome size analyses with flow cytometry appear to be inconclusive.
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Apg II (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141:399–436
Aryavand A, Ehdaie B, Tran B, Waines JG (2003) Stomatal frequency and size differentiate ploidy levels in Aegilops neglecta. Genet Resour Crop Ev 50:175–182
Backlund M, Oxelman B, Bremer B (2000) Phylogenetic relationships within the Gentianales based on ndhF and rbcL sequences, with particular reference to the Loganiaceae. Am J Bot 87(7):1029–1043
Barthlott W (1981) Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nord J Bot 1:345–355
Beerling DJ, Chaloner WG (1993) Evolutionary responses of stomatal density to global CO2 change. Biol J Linn Soc 48:343–353
Bendre AM (1973) Studies in the family Loganiaceae I. Trichomes. J Indian Bot Soc 52:225–234
Bisset NG (1972) Chemical studies on the alkaloids of Asian and African Strychnos species. Lloydia 35:203–206
Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95
Chen G, Sun W, Sun H (2010) Leaf epidermal characteristics of Asiatic Buddleja L. under scanning electron microscope: insights into chromosomal and taxonomic significance. Flora 205:777–785
Cutler DF, Brandham PE (1977) Experimental evidence for the genetic control of leaf surface characters in hybrid Aloineae. Kew Bull 32:23–32
Deccetti SFC, Soares AM, Paiva R, de Castro EM (2008) Effect of the culture environment on stomatal features, epidermal cells and water loss of micro propagated Annona glabra L. plants. Sci Hort 117:341–344
Dilcher DL (1974) Approaches to the identification of angiosperms leaf remains. Bot Rev 40:1–157
Dolezel J, Bartos J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95:99–110
Ferris R, Taylor G (1994) Stomatal characteristics of four native herbs following exposure to elevated CO2. Ann Bot 73:447–453
Frasier LC (2008) Evolution and systematics of the angiosperm order Gentianales with an in-depth focus on Loganiaceae and its species-rich and toxic genus Strychnos. PhD Dissertation, Rutgers, The State University of New Jersey
Frederich M, Jacquier MJ, Thepenier P, De Mol P, Tits M, Philippe G, Delaude C, Angenot L, Zeches-Hanrot M (2002) Antiplasmodial activity of alkaloids from various Strychnos species. J Nat Prod 65:1381–1386
Gadella TWJ (1980) Cytology. In: Engler A, Prantl K (eds) Die Naturlicher Pflanzenfamilien. Duncker & Humbolt, Berlin, pp 203–210
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051
Galmes J, Flexas J, Save H, Medrano H (2007) Water relation and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil 290:139–155
GenStat Discovery Edition 3 (2007) VSN International Ltd., Hemel Hempstead, UK
Ghahremaninejad F, Khalili Z, Maassoumi AA, Mirzaie-Nodoushan H, Riahi M (2012) Leaf epidermal features of Salix species (Salicaceae) and their systematic significance. Am J Bot 99(4):769–777
Gianfagna TJ, Carter CD, Sacalis JN (1992) Temperature and photoperiod influence trichome density and sesquiterpene content of Lycopersicon hirsutum v. hirsutum. Plant Physiol 100:1403–1405
Giełwanowska I, Szczuka E, Bednara J, Gorecki R (2005) Anatomical features and ultrastructure of Deschampsia antarctica (Poaceae) leaves from different growing habitats. Ann Bot 96:1109–1119
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics software package for education and data analysis. Palaeo Electronica 4(1):1–9
Hanson L, Boyd A, Johnson MAT, Bennett MD (2005) First nuclear DNA C-Values for 18 eudicot families. Ann Bot 96:1315–1320
Haworth M, McElwain J (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeogeogr Palaeoclimatol Palaeoecol 262:79–90
Haworth M, Elliott-Kingston C, McElwain JC (2013) Co-ordination of physiological and morphological responses of stomata to elevated [CO] in vascular plants. Oecologia 171:71–82
Hickey LJ (1973) Classification of the architecture of dicotyledonous leaves. Am J Bot 60:17–35
Hlwatika CNM, Bhat RB (2002) An ecological interpretation in the difference in leaf anatomy and its plasticity in contrasting tree species in Orange Kloof, Table Mountain, South Africa. Ann Bot 89:109–114
Hodgson JG, Sharafi M, Jalili A, Díaz S, Montserrat-Martí G, Palmer C, Cerabolini B, Pierce S, Hamzehee B, Asri Y, Jamzad Z, Wilson P, Raven JA, Band SR, Basconcelo S, Bogard A, Carter G, Charles M, Castro-Díez P, Cornelissen JHC, Funes G, Jones G, Khoshnevis M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Boustani S, Dehghan M, Guerrero-Campo J, Hynd A, Kowsary E, Kazemi-Saeed F, Siavash B, Villar-Salvador P, Craigie R, Naqinezhad A, Romo-Díez A, Espuny LT, Simmons E (2010) Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Ann Bot 105(4):573–584
Holmgren PK, Holmgren NH, Barnett LC (eds) (1990) Index Herbariorum. Part 1: the Herbaria of the World, 8th edn. New York Botanical Garden, New York
Inceer H, Hayirlioglu-Ayaz S (2010) Chromosome numbers in Tripleurospermum Sch. Bip. (Asteraceae) and closely related genera: relationships between ploidy level and stomatal length. Plant Syst Evol 285:149–157
Jordan GJ, Weston PH, Carpenter RJ, Dillon RA, Brodribb TJ (2008) The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae. Am J Bot 95(5):521–530
Klich MG (2000) Leaf variations in Elaeagnus angustifolia related to environmental heterogeneity. Environ Exp Bot 44:171–183
Knight CA, Beaulieu JM (2008) Genome size scaling through phenotype space. Ann Bot 101:759–766
Leeuwenberg AJM (1969) The Loganiaceae of Africa VIII. Strychnos III: revision of the African species with notes on the extra-African. Mededel Landbouwhogeschool Wageningen 69:1–316
Liakoura V, Stefanou M, Manetas Y, Cholevas C, Karabourniot G (1997) Trichome density and its UV-B protective potential are affected by shading and leaf position on the canopy. Environ Exp Bot 38:223–229
Lomax BH, Woodward FI, Leitch IJ, Knight CA, Lake JA (2009) Genome size as a predictor of guard cell length in Arabidopsis thaliana is independent of environmental conditions. New Phytol 181:311–314
Marciniuk J, Rerak J, Grabowska-Joachimiak A, Jastrząb I, Musiał K, Joachimiak AJ (2010) Chromosome numbers and stomatal cell length in Taraxacum sect. Palustria from Poland. Acta Biol Craco Series Botanica 52(1):117–121
Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436(11):866–870
Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264(5157):421–424
Mishra LC (1982) Effect of environmental pollution on the morphology and leaf epidermis of Commelina benghalensis Linn. Environ Pollut (Series A) 28:281–284
Mishra MK (1997) Stomatal characteristics at different ploidy levels in Coffea L. Ann Bot 80:689–692
Mwamba CK (2006) Fruits for the Future. 8. Monkey Orange. Strychnos cocculoides. University of Southampton International Centre for Underutilised Crops. Southampton UK
Ohiri FC, Verpoorte R, Svendsen AB (1983) The African Strychnos species and their alkaloids: a review. J Ethnopharmacol 9:167–223
Pathan AK, Bond J, Gaskin RE (2008) Sample preparation for scanning electron microscopy of plant surfaces—horses for courses. Micron 39:1049–1061
Pérez-Estrada LB, Cano-Santana Z, Oyama K (2000) Variation in leaf trichomes of Wigandia urens: environmental factors and physiological consequences. Tree Physiol 20:629–632
Philippe G, Angenot L, Tits M, Frederich M (2004) About the toxicity of some Strychnos species and their alkaloids. Toxicon 44:405–416
Rossatto DR, Kolb RM (2010) Gochnatia polymorpha (Less.) Cabrera (Asteraceae) changes in leaf structure due to differences in light and edaphic conditions. Acta Bot Bras 24(3):605–612
Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palynol 114:1–28
Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philos Trans R Soc Lond Ser B Biol Sci 216:1–65
Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, de Pamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96(1):336–348
Stace CA (1984) The taxonomic importance of the leaf surface. In: Heywood VH, Moore DM (eds) Current Concepts in Plant Taxonomy. (Systematic. Association special vol. 25). Academic Press, London, pp 67–94
Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York
Stenglein SA, Arambarri AM, Menendez-Sevillano MC, Balatti PA (2005) Leaf epidermal characters related with plant’s passive resistance to pathogens vary among accessions of wildbeans Phaseolus vulgaris var. aborigineus (Leguminosae–Phaseoleae). Flora 200:285–295
Verdoorn IC (1963) Loganiaceae. Flora of southern Africa 26:134–149
Wilkinson HP (1979) The plant surface (mainly leaf). In: Metcalfe CR, Chalk L (eds) Anatomy of the Dicotyledons, 2nd edn. Clarendon Press, Oxford, pp 97–167
Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327
Xiang CL, Dong ZH, Peng H, Liu ZW (2010) Trichome micromorphology of the East Asiatic genus Chelonopsis (Lamiaceae) and its systematic implications. Flora 205:434–441
Zhang L, Niu H, Wang S, Zhu X, Luo C, Li Y, Zhao X (2012) Gene or environment? Species–specific control of stomatal density and length. Ecol Evol 2(5):1065–1070
Zhou W, Xia NH (2012) Leaf epidermal features of Lithocarpus (Fagaceae) from China and their systematic significance. Bot J Linn Soc 168:216–228
Zou P, Liao J, Zhang D (2008) Leaf epidermal micromorphology of Cercis (Fabaceae: Caesalpiniodeae). Bot J Linn Soc 158:539–547
Acknowledgments
The authors thank Sharon Eggers of the Microscopy and Microanalysis Unit of University of KwaZulu-Natal, Westville for guidance on the SEM. AA and YN acknowledge the NRF-Thuthuka scheme for funding part of this research. The authors also thank two anonymous reviewers for their critical but helpful comments on the manuscript.
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Adebowale, A., Naidoo, Y., Lamb, J. et al. Comparative foliar epidermal micromorphology of Southern African Strychnos L. (Loganiaceae): taxonomic, ecological and cytological considerations. Plant Syst Evol 300, 127–138 (2014). https://doi.org/10.1007/s00606-013-0865-z
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DOI: https://doi.org/10.1007/s00606-013-0865-z