Morphological and Anatomical Variations in Rheophytic Ecotype of Violet, Viola mandshurica var. ikedaeana (Violaceae)

Ryosuke Matsui, Shogo Takei, Kyohei Ohga, Hiroshi Hayakawa, Masataka Yoshida, Jun Yokoyama, Katsura Ito, Ryo Arakawa, Toshiro Masumoto, Tatsuya Fukuda

Faculty of Agriculture, Kochi University, Kochi, Japan.
Faculty of Science, Yamagata University, Yamagata, Japan.
Graduate School of Integrated Arts and Sciences, Kochi University, Kochi, Japan.
Graduate school of Science and Engineering, Yamagata University, Yamagata, Japan.

DOI: 10.4236/ajps.2013.44106                

Abstract

We compared the leaf morphology and anatomy of the putative rheophytic ecotype of Viola mandshurica W. Becker var. ikedaeana (W. Becker ex Taken.) F. Maek. and its closely related variety, V. mandshurica var. mandshurica. We showed that the leaf of the rheophytic ecotype of V. mandshurica var. ikedaeana was narrower than that of V. mandshurica var. mandshurica. Moreover, the leaf thickness and guard cell size of the rheophytic ecotype of V. mandshurica var. ikedaeana were significantly larger than those of V. mandshurica var. mandshurica. We further showed that leaves of the rheophytic ecotype of V. mandshurica var. ikedaeana contained fewer cells than did those of V. mandshurica var. mandshurica. Our results suggest that the narrower leaves of V. mandshurica var. ikedaeana are caused by a decrease in the number of cells. A narrower leaf may enable the rheophytic ecotype of V. mandshurica var. ikedaeana to resist the strong flow of water that occurs after heavy rainfall, while a thicker leaf may enhance tolerance to desiccation and high- intensity light.

Keywords

Ecotype; Leaf; Rheophyte; Stenophyllization; Viola mandshurica

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	C. W. P. M. Blom and L. A. C. J. Voesenek, “Flooding: The Survival Strategies of Plants,” Trends in Ecology & Evolution, Vol. 11, No. 7, 1996, pp. 290-295. doi:10.1016/0169-5347(96)10034-3
[2]	P. J. A. Vervuren, C. W. P. M. Blom and H. de Kroon, “Extreme Flooding Events on the Rhine and the Survival and Distribution of Riparian Plant Species,” Journal of Ecology, Vol. 91, No. 1, 2003, pp. 135-146. doi:10.1046/j.1365-2745.2003.00749.x
[3]	W. H. J. M. van Eck, H. M. van de Steeg, C. W. P. M. Blom and H. de Kroon, “Is Tolerance to Summer Flooding Correlated with Distribution Patterns in River Floodplains? A Comparative Study of 20 Terrestrial Grassland Species,” Oikos, Vol. 107, No. 2, 2004, pp. 393-405. doi:10.1111/j.0030-1299.2004.13083.x
[4]	L. A. C. J. Voesenek, J. H. G. M. Rijnders, A. J. M. Peeters, H. M. van de Steeg and H. de Kroon, “Plant Hormones Regulate Fast Shoot Elongation under Water: From Genes to Communities,” Ecology, Vol. 85, No. 1, 2004, pp. 16-27. doi:10.1890/02-740
[5]	C. G. G. J. van Steenis, “Rheophyte of the World,” Sijthoff and Noordhoff, Alpen aan den Rijn, 1981.
[6]	M. Kato and R. Imaichi, “Leaf Anatomy of Tropical Fern Rheophytes with Its Evolutionary and Ecological Implications,” Canadian Journal of Botany, Vol. 70, No. 1, 1992, pp. 165-174. doi:10.1139/b92-022
[7]	R. Imaichi and M. Kato, “Comparative Leaf Development of Osmunda lancea and O. japonica (Osmundaceae): Heterochronic Origin of Rheophytic Stenophylly,” The Botanical Magazine, Vol. 105, No. 2, 1992, pp. 199-213. doi:10.1007/BF02489415
[8]	R. Imaichi and M. Kato, “Comparative Leaf Morphology of Young Sporophytes of Rheophytic Osmunda lancea and Dryland O. japonica,” Journal of Plant Research, Vol. 106, No. 1, 1993, pp. 37-45. doi:10.1007/BF02344371
[9]	M. Usukura, R. Imaichi and M. Kato, “Leaf Morphology of a Facultative Rheophyte, Farfugium japonicum var. luchuense (Compositae),” Journal of Plant Research, Vol. 107, No. 3, 1994, pp. 263-267. doi:10.1007/BF02344253
[10]	H. Tsukaya, “Leaf Anatomy of a Rheophyte, Dendranthema yoshinaganthum (Asteraceae), and of Hybrids between D. yoshinaganthum and a Closely Related Non- Rheophyte, D. indicum,” Journal of Plant Research, Vol. 115, No. 5, 2002, pp. 329-333. doi:10.1007/s10265-002-0041-y
[11]	Y. Yamada, H. Hayakawa, Y. Minamiya, K. Ito, Z. Shibayama, R. Arakawa and T. Fukuda, “Comparative Morphology and Anatomy of Rheophytic Aster microcephalus (Miq.) Franch. et Sav. var. ripensis Makino (Asteraceae),” Journal of Phytogeography and Taxonomy, Vol. 59, No. 1, 2011, pp. 35-42.
[12]	K. Ohga, M. Muroi, H. Hayakawa, K. Ito, J. Yokoyama, S. Tebayashi, R. Arakawa and T. Fukuda, “Comparative Morphology and Anatomy of Non-Rheophytic and Rheophytic Types of Adenophora triphylla var. japonica (Campanulaceae),” American Journal of Plant Science, Vol. 3, No. 6, 2012, pp. 805-809. doi:10.4236/ajps.2012.36097
[13]	H. Setoguchi and G. Kajimura, “Leaf Morphology of the Rheophyte, Rhododendron indicum f. otakumi (Ericaceae),” Acta Phytotaxomica et Geobotanica, Vol. 55, No. 1, 2004, pp. 45-54.
[14]	R. Ueda, Y. Minamiya, A. Hirata, H. Hayakawa, Y. Muramatsu, M. Saito and T. Fukuda, “Morphological and Anatomical Analyses of Rheophytic Rhododendron ripense Makino (Ericaceae),” Plant Species Biology, Vol. 27, No. 3, 2012, pp. 223-240. doi:10.1111/j.1442-1984.2011.00345.x
[15]	M. W. Chase, D. E. Soltis, R G. Olmstead, D. Morgan, D. H. Les, B. D. Mishler, M. R. Duvall, R. A. Price, H. G. Hills and Y. L. Qiu, “Phylogenetics of Seed Plants: An Analysis of Nucleotide Sequences from the Plastid Gene rbcL,” Annals of the Missouri Botanical Garden, Vol. 80, No. 3, 1993, pp. 528-580. doi:10.2307/2399846
[16]	D. E. Soltis, P. S. Soltis, M. W. Chase, M. E. Mort, D. C. Albach, M. Zanis, V. Savolainen, W. H. Hahn, S. B. Hoot, M. F. Fay, M. Axtell, S. M. Swenson, M. A. Prince, W. J. Kress, K. C. Nixon and J. S. Farris, “Angiosperm Phylogeny Inferred from a Combined Data Set of 18S rDNA, rbcL and atpB Sequences,” Botanical Journal of the Linnean Society, Vol. 133, No. 4, 2000, pp. 381-461.
[17]	V. Savolainen and M. W. Chase, “A Decade of Progress in Plant Molecular Phylogenetics,” Trends in Genetics, Vol. 19, No. 12, 2003, pp. 717-724. doi:10.1016/j.tig.2003.10.003
[18]	P. S. Soltis and D. S. Soltis, “The Origin and Diversification of Angiosperms,” American Journal of Botany, Vol. 91, No. 10, 2004, pp. 1614-1626. doi:10.3732/ajb.91.10.1614
[19]	S. Akiyama, H. Ohba and S. Tabuchi, “Violaceae,” In: K. Iwatsuki, T. Tamazaki, D. E. Boufford and H. Ohba, Eds., Flora of Japan Vol. IIc., Kodansha, Tokyo, 1993, pp. 161-190.
[20]	M, Igari, “Wild Violets of Japan,” Yama-to-Keikoku-sha, Tokyo, 1996.
[21]	H. Tsukaya, “The Leaf Index: Heteroblasty, Natural Variation, and the Genetic Control of Polar Process of Leaf Expansion,” Plant and Cell Physiology, Vol. 43, No. 4, 2002, pp. 372-378. doi:10.1093/pcp/pcf051
[22]	T. Yamanaka and K. Takezaki, “Distribution and Ecology of Rhododendron ripense Makino, with Reference to the Vegetation and Flora on Rocky River-Bank,” Journal of Japanese Botany, Vol. 34, 1959, pp. 215-224.
[23]	N. Nomura, H. Setoguchi and T. Takaso, “Functional Consequences of Stenophylly for Leaf Productivity: Comparison of the Anatomy and Physiology of a Rheophyte, Farfugium japonicum var. luchuence, and a Related Non- Rheophyte, F. japonicum (Asteraceae),” Journal of Plant Research, Vol. 119, No. 6, 2006, pp. 645-656. doi:10.1007/s10265-006-0024-5
[24]	R. Imaichi and M. Kato, “Speciation and Morphological Evolution in Rheophytes,” In: K. Iwatsuki and P. H. Raven, Eds., Evolution and Diversification of Landplants, Springer-Verlag, Tokyo, 1997, pp. 309-318. doi:10.1007/978-4-431-65918-1_15
[25]	ü. Niinemets, “Components of Leaf Dry Mass per Area— Thickness and Density—Alter Leaf Photosynthetic Capacity in Reverse Directions in Woody Plants,” New Phytolgist, Vol. 144, No. 1, 1999, pp. 35-47. doi:10.1046/j.1469-8137.1999.00466.x
[26]	ü. Niinemets, “Global-Scale Climatic Controls of leaf Dry Mass per Area, Density and Thickness in Trees and Shrubs,” Ecology, Vol. 82, No. 2, 2001, pp. 453-469. doi:10.1890/0012-9658(2001)082[0453:GSCCOL]2.0.CO;2
[27]	K. Raschke, “Stomatal Action,” Annual Review of Plant Physiology, Vol. 26, No. 1, 1975, pp. 309-340. doi:10.1146/annurev.pp.26.060175.001521
[28]	P. G. Schoch, C. Zinsou and M. Sibi, “Dependence of the Stomatal Index on Environmental Factors Differentiation in Leaves of Vigna sinensis L. 1. Effect of Light Intensity,” Journal of Experimental Botany, Vol. 31, No. 5, 1980, pp. 1211-1216. doi:10.1093/jxb/31.5.1211
[29]	E. E. Brent and O. Ram, “Analyses of Assumptions and Errors in the Calculation of Stomatal Conductance from Sap Flux Measurements,” Tree Physiology, Vol. 20, No. 9, 2000. pp. 579-589. doi:10.1093/treephys/20.9.579
[30]	P. G. Jarvis, “The Interpretation of Variations in Leaf Water Potential and Stomatal Conductance Found in Canopies in the Field,” Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, Vol. 273, No. 927, 1976, pp. 93-610. doi:10.1098/rstb.1976.0035
[31]	B. E. Ewers, R. Oren, K. H. Johnsen and J. J. Landsberg, “Estimating Maximum Mean Canopy Stomatal Conductance for Use in Models,” Canadian Journal of Forest Research, Vol. 31, No. 2, 2001, pp. 198-207.
[32]	D. F. Cole and A. K. Dobrenz, “Stomata Density of Alfalfa (Medicago sativa L.),” Crop science, Vol. 10, No. 1, 1970, pp. 61-63. doi:10.2135/cropsci1970.0011183X001000010024x
[33]	D. Teare, C. J. Peterson and A. G. Law, “Size and Frequency of Leaf Stomata in Cultivars of Triticum aestivum and Other Triticum Species,” Crop Science, Vol. 11, No. 4, 1971, pp. 496-498. doi:10.2135/cropsci1971.0011183X001100040010x
[34]	J. Ciha and W. A. Brown, “Stomatal Size and Frequency in Soybean,” Crop Science, Vol. 15, No. 3, 1975, pp. 309-313. doi:10.2135/cropsci1975.0011183X001500030008x
[35]	N. Yamada, T. Suzuki and M. Okamoto, “A New Rheophilous Variety, Viola grypoceras var. ripensis, from Central and Western Honshu, Japan,” Bulletin of the Osaka Museum of Natural History, Vol. 50, 1996, pp. 1- 8.