Abstract
Alisma L. is a genus of aquatic and wetland plants belonging to family Alismataceae. At present, it is thought to contain ten species. Variation in ploidy level is known in the genus, with diploids, tetraploids and hexaploids recorded. Previous molecular phylogenetic studies of Alisma have generated a robust backbone that reveals important aspects of the evolutionary history of this cosmopolitan genus, yet questions remain unresolved about the formation of the polyploid taxa and the taxonomy of one particularly challenging, widely distributed species complex. Here we directly sequenced, or cloned and sequenced, nuclear DNA (nrITS and phyA) and chloroplast DNA (matK, ndhF, psbA-trnH and rbcL) of multiple samples of six putative species and two varieties, and conducted molecular phylogenetic analyses. Alisma canaliculatum and its two varieties known in East Asia and A. rariflorum endemic to Japan possess closely related but heterogeneous genomes, strongly indicating that the two species were generated from two diploid progenitors, and are possibly siblings of one another. This evolutionary event may have occurred in Japan. Alisma canaliculatum var. canaliculatum is segregated into two types, each of which are geographically slightly differentiated in Japan. We reconstructed a single phylogeny based on the multi-locus data using Homologizer and then applied species delimitation analysis (STACEY). This allowed us to discern A. orientale as apparently endemic to the Southeast Asian Massif and distinct from the widespread A. plantago-aquatica. The former species was most likely formed through parapatric speciation at the southern edge of the distribution of the latter.
Similar content being viewed by others
References
Aston HI (1973) Alismataceae. In: Aston HI (ed) Aquatic plants of Australia. Melbourne University Press, Victoria. 176–186
Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: An example from the Compositae. Mol Phylogenet Evol 1:3–16. https://doi.org/10.1016/1055-7903(92)90030-k
Björkqvist I (1967) Studies in Alisma L. I. Distribution, variation and germination. Opera Bot 17:1–128
Björkqvist I (1968) Studies in Alisma L. II. Chromosome studies, crossing experiments and taxonomy. Opera Bot 19:1–138
Bouckaert RR, Heled J, Kühnert D, Vaughan TG, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537
Chen LY, Chen JM, Gituru RW, Temam TD, Wang QF (2012) Generic phylogeny and historical biogeography of Alismataceae, inferred from multiple DNA sequences. Mol Phylogenet Evol 63:407–416. https://doi.org/10.1016/j.ympev.2012.01.016
Cook CDK (2004) Alismataceae In: Cook CDK (ed) Aquatic and wetland plants of southern Africa. Backhuys Publishers, pp 48–52
Crow GE, Hellquist CB (2000) Alismataceae. In: Crow GE, Hellquist CB (eds) Aquatic and wetland plants of northeastern North America, vol 2. Angiosperms: Monocotyledons. University of Wisconsin Press, Madison, pp 3–11
Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–222. https://doi.org/10.1186/1471-2148-7-214
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88. https://doi.org/10.1371/journal.pbio.0040088
Felsenstein J (1985) Confidence limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Freyman WA, Johnson MG, Rothfels CJ (2022) Homologizer: phylogenetic phasing of gene copies into polyploid subgenomes. bioRxiv 2020.10.22.351486v4
Futuyma DJ (2005) Evolution. Sinauer Associates, Sunderland, Massachusetts
Grubov VI, Matzenko AE, Pachomova MG (2002) Alismataceae. In: Grubov VI (ed) Plants of Central Asia: plant collections from China and Mongolia, vol. 6. Science Publishers, Inc., pp 58–62
Haynes RR (2001) Alismataceae. In: Santisuk T, Larsen K (eds) Flora of Thailand, vol 7. Prachachon, Bangkok, pp 351–358
Haynes RR, Hellquist CB (2000) Alismataceae. In: Flora of North America Editorial Committee (ed) Flora of North America North of Mexico. Oxford University Press, Oxford, Volume 22. pp 7−25
Höhna S, Landis MJ, Heath TA, Boussau B, Lartillot N, Moore BR, Huelsenbeck JP, Ronquist F (2016) RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst Biol 65:726–736. https://doi.org/10.1093/sysbio/syw021
Ito Y, Ohi-Toma T, Murata J, Tanaka N (2010) Hybridization and polyploidy of an aquatic plant, Ruppia (Ruppiaceae), inferred from plastid and nuclear DNA phylogenies. Am J Bot 97:1156–1167. https://doi.org/10.3732/ajb.0900168
Ito Y, Tanaka N, Albach DC, Barfod AS, Oxelman B, Muasya AM (2017) Molecular phylogeny of the cosmopolitan aquatic plant genus Limosella (Scrophulariaceae) with a particular focus on the origin of the Australasian L. curdieana. J Plant Res 130:107–116. https://doi.org/10.1007/s10265-016-0872-6
Ito Y, Tanaka N, Barfod AS, Bogner J, Li J, Yano O, Gale SW (2019) Molecular phylogenetic species delimitation in the aquatic genus Ottelia (Hydrocharitaceae) reveals cryptic diversity within a widespread species. J Plant Res 132:335–344. https://doi.org/10.1007/s10265-019-01109-7
Jacobson A, Hedrèn M (2007) Phylogenetic relationships in Alisma (Alismataceae) based on RAPDs, and sequence data from ITS and trnL. Plant Syst Evol 265:27–44. https://doi.org/10.1007/s00606-006-0514-x
Jones GL (2017) Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J Math Biol 74:447–467. https://doi.org/10.1007/s00285-016-1034-0
Jones GL, Aydin Z, Oxelman B (2015) DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31:991–998. https://doi.org/10.1093/bioinformatics/btu770
Juzepczuk SV (1934) Alismataceae In: Komarov VL (ed) Flora of USSR vol. 1. Leningrad, pp 218–222 (English edition published in 1986)
Kadono Y (2020) Alismataceae. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan, vol IVa. Kodansha Ltd., Tokyo, pp 24–26
Kadono Y, Hamashima S (1988) A new variety of Alisma canaliculatum found in Japan. J Jpn Bot 63:411–412
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Les DH, Tippery NP (2013) In time and with water … the systematics of alismatid monocotyledons. In: Wilkin P, Mayo SJ (eds) Early events in monocot evolution. Cambridge University Press, pp 118–164
Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in Alismatidae, II—Evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22:443–463
Linneaus C (1753) Alisma. In: Linneaus C (ed) Species Plantarum vol. 1, pp. 342–343
Little DP, Barrington DS (2003) Major evolutionary events in the origin and diversification of the fern genus Polystichum (Dryopteridaceae). Am J Bot 90:508–514. https://doi.org/10.3732/ajb.90.3.508
Love A, Love D (1980) Chromosome number reports LXIX. Taxon 29:707–709
Love A, Love D (1981) Chromosome number reports LXXII. Taxon 30:699–701
Makino T (1940) An illustrated flora of Nippon, with the cultivated and naturalized plants. Hokuryukan, Tokyo (in Japanese)
Nylander JAA (2002) MrModeltest v.1.0. Program distributed by the author. Department of Systematic Zoology, Uppsala University, Uppsala. Available at: http://www.ebc.uu.se/systzoo/staff/nylander.html
Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481. https://doi.org/10.1093/sysbio/43.4.467
Oxelman B, Backlund M, Bremer B (1999) Relationships of the Buddlejaceae s. l. inferred from chloroplast rbcL and ndhF sequences. Syst Bot 24:164–182
Probatova NS, Sokolovskaya AP (1986) Chromosome numbers of the vascular plants from the far east of the USSR. Bot Zhurn SSSR 71:1572–1575
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rambaut A, Suchard MA, Xie W, Drummond AJ (2014) Tracer. Ver 1.6. http://beast.bio.ed.ac.uk/Tracer
Rambaut A (2009) FigTree ver. 1.3.1: Tree Figure Drawing Tool. Retrieved from http://tree.bio.ed.ac.uk/software/fgtree/
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Ross TG, Barrett CF, Soto Gomez M, Lam VKY, Henriquez CL, Les DH, Davis JI, Cuenca A, Petersen G, Seberg O, Thadeo M, Givnish TJ, Conran J, Stevenson DW, Graham SW (2016) Plastid phylogenomics and molecular evolution of Alismatales. Cladistics 32:160–178. https://doi.org/10.1111/cla.12133
Samuelsson G (1931) Die Arten der Gattung Alisma L. Ark Bot 24A:1–46
Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am J Bot 84:1120–1136
Sato J (1942) Illustration of Manchurian water-plants. Kanto-gun (in Japanese)
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771. https://doi.org/10.1080/10635150802429642
Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b. Sinauer, Sunderland, Massachusetts, USA
Tanaka N (2015) Alismataceae. In: Ohashi H, Kadota Y, Murata J, Yonekura K (eds) Wild flowers of Japan, vol 1. Heibonsha Ltd, Tokyo, pp 115–117 (in Japanese)
Tribble CM, Freyman WA, Landis MJ, Lim JY, Barido-Sottani J, Kopperud BT, Höhna S, May MR (2022) RevGadgets: An R package for visualizing Bayesian phylogenetic analyses from RevBayes. Methods Ecol Evol 13:314–323. https://doi.org/10.1111/2041-210X.13750
Uchiyama H (1989) Karyomorphological studies on some taxa of the Helobiae. J Sci Hiroshima Univ Ser b Div 2(22):271–352
Wang ZQ, Sun XZ, Wang HQ (1987) Cytotaxonomic studies on Alisma L. from Hubei. Acta Phytotax Sin 25:254–263
Wang QF, Guo YH, Haynes RR, Hellquist CB (2010) Alismataceae. In: Wu C-Y, Raven PH, Hong D-Y (eds) Flora of China, vol 23. Science Press. Beijing & Missouri Botanical Garden Press, St. Louis, pp 84–89
Wolf PG, Soltis PS, Soltis DE (1994) Phylogenetic relationships of Dennstaedtioid ferns: evidence from rbcL sequences. Mol Phylogenet Evol 3:383–392
Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724. https://doi.org/10.1093/oxfordjournals.molbev.a025811
Acknowledgements
The authors thank A. Bobrov (IBIW) and E. Cameron (AK) for their hospitality during YI’s research visits; Nob. Tanaka (TNS), A. Naiki (Okinawa), T. Sugawara (MAK), S. Mifsud (Malta), and Z. Wu (KIB) for their kind help in YI’s field survey; S. Tagane (FU), T. Kuhara (Niigata), S. Chiba (Nagano), and S. Matsumoto (Hyogo), for providing a material of Alisma; H. Ono (Shimane), and C. Enju (Tsukuba), T. Godo (Toyama), T. Ohara (Toyama), and M. Nakata (Toyama) for supporting collection of materials of Alisma; C. Ishii (Tsukuba) for help with DNA sequencing and S. Gale (KFBG) for improving an earlier draft of the manuscript. This study was partly supported by the international cooperative project “Biological Inventory with special attention to Myanmar: Investigations of the origin of southern elements of Japanese flora and fauna” as the integrated research initiated by the National Museum of Nature and Science, Japan based on MoU between the Forest Department, and the Ministry of Natural Resources and Environmental Conservation, Myanmar.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ito, Y., Tanaka, N. Phylogeny of Alisma (Alismataceae) revisited: implications for polyploid evolution and species delimitation. J Plant Res 136, 613–629 (2023). https://doi.org/10.1007/s10265-023-01477-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-023-01477-1