Research Paper

Studies on anatomical characters indicating C3 and C4 photosynthetic metabolism in the genus Boerhavia L. (Nyctaginaceae)

Abdulwakeel Ayokun-nun Ajao, Mahboob Adekilekun Jimoh and Sefiu Adekilekun Saheed

Published on: 17 July 2017

Page: 265 - 271

DOI: 10.6165/tai.2017.62.265

Abstract

The C3 and C4 photosynthetic pathways in dicotyledons were investigated with the four species of Boerhavia occurring in Nigeria using light microscopy. The study is not yet well reported on dicotyledons as done for monocotyledons. The features cross-examined were stomata index, stomata size, inter-stomatal distance, stomatal density, interveinal distance, intercellular air spaces, leaf thickness, mesophyll thickness, Kranz tissue, one cell distant count criterion, maximum lateral cell count criterion, vein density and vein distance. Based on these features, these species (B. erecta, B. coccinea and B. repens) were grouped into C4 while B. diffusa was grouped as a C3 plant. In particular, interveinal distance less than 166µm and maximum lateral count ranging 2 to 6 will help in grouping C4 dicotyledons species while those that were greater than these values are useful in grouping C3 and plants.

Keyword: Boerhavia, C3 Plant, C4 Plant, Kranz tissue, Leaf anatomy, Photosynthesis

Literature Cited

Adedeji, O. and O.A. Jewoola. 2008. Importance of leaf epidermal characters in the Asteraceae family. Not. Bot. Horti. Agrobot. Cluj-Napoca 36(2): 7-16.

Ayeni, O.B., M.A. Jimoh and S.A.Saheed. 2015. Leaf anatomical characters in relation to C3 and C4 photosynthetic pathway in Cyprus (Cyperaceae). Nord. J. Bot. 33(3): 318-323.
DOI: 10.1111/njb.00710View Article Google Scholar

Brodribb, T.J., T.S. Field and G.J. Jordan. 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol. 144(4): 1890-1898.
DOI: 10.1104/pp.107.101352View Article Google Scholar

Bruhl, J.J., N.E. Stone and P.W. Hattersley. 1987. C4 acid decarboxylation enzymes and anatomy in sedges (Cyperaceae): first record of NAD-malic enzyme species. Aust. J. Plant Physiol. 14(6): 719-728.
DOI: 10.1071/PP9870719View Article Google Scholar

Bruhl, J.J. and K.L. Wilson. 2007. Towards a comprehensive survey of C3 and C4 photosynthetic pathways in Cyperaceae. Aliso 23(1): 99-148.
DOI: 10.5642/aliso.20072301.11View Article Google Scholar

Chen, S.-H. and M.-J. Wu. 2005. Note on three newly naturalized plants in Taiwan. Taiwania 50(1): 29-39.
DOI: 10.6165/tai.2005.50(1).29View Article Google Scholar

Chou, F.-S., H.-.Y Liu and C.-R. Sheue. 2004. Boerhavia erecta L. (Nyctaginaceae), a new adventive plant in Taiwan. Taiwania 49(1): 39-43.
DOI: 10.6165/tai.2004.49(1).39View Article Google Scholar

Crookston, R.K. and D.N. Moss. 1974. Interveinal distance for carbohydrate transport in leaves of C3 and C4 grasses. Crop Sc. 14(1): 123-125.
DOI: 10.2135/cropsci1974.0011183X001400010038xView Article Google Scholar

Dengler, N.G., R.E. Dengler, P.M. Donnelly and P.W. Hattersley. 1994. Quantitative leaf anatomyof C3 and C4 grasses (Poaceae): bundle sheath and mesophyll surface area relationships. Ann. Bot. 73(3): 241-255.
DOI: 10.1006/anbo.1994.1029View Article Google Scholar

Diana, M., L. Marshall, M. Riyadh, J. Naomi, L. Zheng, S. Susan, G. Howard, R.F. Sage and J.M. Hibberd. 2007. Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis. Plant J. 51(5): 886-896.
DOI: 10.1111/j.1365-313X.2007.03188.xView Article Google Scholar

Edwards, G.E., V. R. Franceschi and E.V.Voznesenskaya. 2004. Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Ann. Rev. Plant Biol. 55(1): 173-196.
DOI: 10.1146/annurev.arplant.55.031903.141725View Article Google Scholar

Ehleringer, J.R., T.E. Cerling and B.R. Helliker. 1997. C4 photosynthesis, Atmospheric CO2 and Climate. Oecologia 112(3): 285-299.
DOI: 10.1007/s004420050311View Article Google Scholar

Faniyan, M.M., D.O. Olatunde, O.B. Ayeni, M.A. Jimoh and S.A. Saheed. 2013. Functional leaf anatomical characters in relation to C3 and C4 photosynthetic pathways in four species of Euphorbia L. in Southwestern Nigeria. Nig. J. Bot. 26(1): 19-28.

Fosberg, F.R. 1978. Studies in the genus Boerhavia L. (Nyctaginaceae). Smithson. Contrib. Bot. 39: 1-19.
DOI: 10.5479/si.0081024X.39View Article Google Scholar

Fosberg, F.R. 1999. Nyctaginaceae. In: Wagner, W. L. et al. (eds.), Manual of the Flowering Plants of Hawaii, rev. ed. 1: 976-988. Bishop Museum, Honolulu, USA.

Gentry, A.H. 1993. A field guide to the families and genera of woody plants of northwest South America (Colombia, Ecuador, Peru), with supplementary notes on herbaceous taxa. Conservation International Washington, DC.

Hattersley, P.W., L Watson, F.L.S. Johnston and C.R. Johnson. 1982. Remarkable leaf anatomical variations in Neurachne and its allies (Poaceae) in relation to C3 and C4 photosynthesis. Bot. J. Linaean Soc. 84(4): 265-272.
DOI: 10.1111/j.1095-8339.1982.tb00364.xView Article Google Scholar

Hattersley, P.W. and L. Watson. 1975. Anatomical parameters for predicting photosynthetic pathways of grass leaves: the

Hibberd, J.M. and W.P. Quick. 2002. Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415(6870): 451-454.
DOI: 10.1038/415451aView Article Google Scholar

Holmgren, P.K., W. Keuken and E.K. Schofield. 1981. Index Herbariorum. Part 1 The Herbaria of the World. Utrecht, Oosthoek, Scheltema & Holkema.

Hutchinson, J. and J.M. Dalziel. 1972. Flora of West Tropical Africa. Crown Agent for Overseas Government and Administration Nill Bank London S. Vol. 1

Huxman, T.E. and R.K. Monson. 2003. Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behavior. Plant Cell Environ. 26(2): 313-322.
DOI: 10.1046/j.1365-3040.2003.00964.xView Article Google Scholar

Illoh, H.C. 1995. Foliar epidermis and petiole anatomy of four species of CelosiaL. in Nigeria. Feddes Repert. 106(1-2):15-23.
DOI: 10.1002/fedr.19951060107View Article Google Scholar

Jorgensen, P.M. and C. Ulloa. 1994. Seed Plants of the High Andes of Ecuador - a checklist. AAU Reports 34:336-355.

Kanai, R. and M. Kashiwagi. 1975. Panicum milioides, a graminea plant having Kranz leaf anatomy without C4 photosynthesis. Plant Cell Physiol. 16(4): 669-679.
DOI: 10.1093/oxfordjournals.pcp.a075187View Article Google Scholar

Kim, C.Y. 2012. Stomatal responses of C3 and C4Cyprus species(Cyperaceae) in Korea to elevated CO2 concentration, M.S.D. Dissertation, Sungshin Women's University, Seoul, Korea. 203p

Li, M.R. and M.B. Jones. 1994. Kranzkette, unique C4 anatomy occurring in Cyperus japonicus leaves. Photosynthetica 30:117-131.

Li, M.-R., D.A. Wedin and L.L. Tieszen. 1999. C3 and C4 photosynthesis in Cyperus (Cyperaceae) in temperate eastern North America. Can. J. Bot. 77(2): 209-218.

Lin, Z.-F., S.-S. Li and G.-Z. Lin. 1986. Stomata occurrence on leaf epidermis and photosynthesis pathway. Acta Bot. Sin. 28: 387-395.

Martins, S and M. Alves. 2009. Anatomical features of species of Cyperaceae from Northeastern Brazil. Brittonia 61(2): 189-200.
DOI: 10.1007/s12228-009-9073-0View Article Google Scholar

Mckown, A.D., H. Cochard and L. Sack. 2010. Decoding leaf hydraulics with a spatially explicit model: principle of venation architecture and implication for its evolution. Am. Nat. 175(4): 447-460.
DOI: 10.1086/650721View Article Google Scholar

McKown, A.D. and N.G. Dengler. 2007. Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). Am. J. Bot. 94(3): 382-399.
DOI: 10.3732/ajb.94.3.382View Article Google Scholar

Monson, R.K., G.E. Edwards and M.S.B. Ku. 1984. C3-C4 intermediate photosynthesis in plants. Bioscience 34(9): 563-574.
DOI: 10.2307/1309599View Article Google Scholar

Muhaidat, R., R.F. Sage and N.G. Dengler. 2007. Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am. J. Bot. 94(3): 362-381.
DOI: 10.3732/ajb.94.3.362View Article Google Scholar

Nelson E.A. and R.F. Sage. 2008. Functional constraints of CAM leaf anatomy: tight cell packing is associated with increased CAM function across a gradient of CAM expression. J Exp. Bot. 59(7): 1841-1850.
DOI: 10.1093/jxb/erm346View Article Google Scholar

Nelson, E.A., T.L. Sage and R.F. Sage. 2005. Functional leaf anatomy of plants with crassulacean acid metabolism. Funct. Plant Biol. 32:409-419.
DOI: 10.1071/FP04195View Article Google Scholar

Nelson, T. and N.G. Dengler, 1997. Leaf vascular pattern formation. Plant Cell 9(7): 1121-1135.
DOI: 10.1105/tpc.9.7.1121View Article Google Scholar

Ogundare, C.S. and S.A. Saheed. 2012. Foliar epidermal characters and petiole anatomy of four species of Citrus L. (RUTACEAE) from South-western Nigeria. Bangl. J. Plant Taxon. 19(1): 25-31.
DOI: 10.3329/bjpt.v19i1.10938View Article Google Scholar

Oguro, H.O., K. Hinata and S. Tsunoda. 1985. Comparative anatomy and morphology of leaves between C3 and C4 Species in Panicum. Ann. Bot. 55(6): 859-869.
DOI: 10.1093/oxfordjournals.aob.a086967View Article Google Scholar

Ranson, S.C. and M. Thomas. 1960. Crassulacean acid metabolism. Annu. Rev. Plant Physiol. 11(1): 81-110.
DOI: 10.1146/annurev.pp.11.060160.000501View Article Google Scholar

Renvoize, S.A. 1987. A survey of leaf-blade anatomy in grasses XI. Paniceae. Kew Bull. 42(3): 739-768.
DOI: 10.2307/4110087View Article Google Scholar

Sack, L. and N.M. Holdbrook. 2006. Leaf hydraulics. Annu. Rev. Plant Biol. 57(1): 361-381.
DOI: 10.1146/annurev.arplant.56.032604.144141View Article Google Scholar

Saheed, S.A. and H.C. Illoh. 2010. A taxonomic study of some species in Cassinae (Leguminosae) using leaf epidermal characters. Not. Bot. Horti. Agrobot. Cluj-Napoca 38: 21-27.

Sage, R.F. 2002. C4 photosynthesis in terrestrial plants does not require Kranz anatomy. Trends Plant Sci. 7(7): 283-285.
DOI: 10.1016/S1360-1385(02)02293-8View Article Google Scholar

Sinha, N.R. and E.A. Kellogg. 1996. Parallelism and diversity in multiple origins of C4 photosynthesis in the grass family. Am. J. Bot. 83(11): 1458-1470.
DOI: 10.2307/2446101View Article Google Scholar

Soros, C.L. and N.G. Dengler. 1998. Quantitative leaf anatomy of C3 and C4 Cyperaceae and Comparism with Poaceae. Int. J. Plant Sci. 159(3): 480-491.
DOI: 10.1086/297565View Article Google Scholar

Spellenberg, R. 2003. Boerhavia. In: Flora of North America Editorial committee, Flora of North America. 4: 17-28. Oxford Univ. Press, New York, USA.

Takeda, T. and M. Fukuyama. 1971. Studies on the photosynthesis of the Gramineae. Differences in photosynthesis among sub-families and their relations with the systematics of the Gramineae. Jpn. J. Crop Sci. 40(1): 12-20.
DOI: 10.1626/jcs.40.12View Article Google Scholar

Takeda, T., O. Ueno, and W. Agata. 1980. The occurrence of C4 species in the genus Rhynchospora and its significance in Kranz anatomy of the Cyperaceae. Bot. Mag. Tokyo 9(1)3:55-65.
DOI: 10.1007/BF02489486View Article Google Scholar

Taylor, S.H., S.P. Hulme and C.P. Osborne. 2010. Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment. New Phytol. 185(3): 780-791.
DOI: 10.1111/j.1469-8137.2009.03102.xView Article Google Scholar

Ueno, O., K.Yukiko, W. Masataka and T. Tomoshiro. 2006. Leaf Vascular Systems in C3 and C4 Grasses: A Two-dimensional Analysis. Ann. Bot. 97(4): 611-621.
DOI: 10.1093/aob/mcl010View Article Google Scholar

Voznesenskaya, E.V., S.V.R. Franceschi, E.G. Artyusheva, H. Freitas and G.E. Edwards. 2002. Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J. 31(5): 649-662.
DOI: 10.1046/j.1365-313X.2002.01385.xView Article Google Scholar

Wang, R.Z. 2004. C4 species and their response to large scale longitudinal climate variables along the Northest China. Transect NECT. Photosynthetic 42(1): 71-79.
DOI: 10.1023/B:PHOT.0000040572.95053.76View Article Google Scholar