Skip to main content

Multidisciplinary studies of the diversity and evolution in river-weeds

Abstract

The moss-like river-weeds or Podostemaceae offer a special opportunity to study the diversity and evolution of plants that are adapted to extreme environments. This paper reviews multidisciplinary studies on this subject. Based on field work in the four continents, we discovered many species and several genera that are new components of biodiversity, and revealed the Podostemaceae floras of East Asia, Southeast Asia, and Australia. The historical biogeography of the family, i.e., the change in distribution in space and time, is characterized by a few dispersals between continents, followed by diversification within each continent. Local species may be derived from parts of separated populations of parental species, which consequently are paraphyletic. The remarkable morphological adaptations of Podostemaceae include the development of the horizontal axis in plant body, with which the plants adhere to rock surfaces under violent current. The vertical axis is reduced or lost and the horizontal axis develops in the embryo and seedling. We also found saltational organ-level variation, such as presence or absence of shoot, shoot apical meristem, root, and root cap; the form of shoot and root; the mode of root branching and leaf production; and the number of cotyledons. Morphological evolution may not be always adaptive to the habitats, which are rocks periodically submerged across the distribution range. Analyses of shoot regulatory gene expression found that, in contrast to the expression pattern in primitive species with ordinary shoots, which is comparable with Arabidopsis, the unique pattern in derived species may result in ‘fuzzy’ morphology of the shoot and leaf. Finally, problems for future study are pointed out.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Aston HI (1990) Podostemaceae. In: George AS (ed) Flora of Australia, vol 18. Australian Government Publishing Service, Canberra, pp 1–5

    Google Scholar 

  • Borgen L, Jonsell B (ed) (1997) Variation and evolution in arctic and alpine plants. In: Proceedings of VI international symposium of international organization of plant biosystematics. Opera Botanica No. 132

  • Bove CP, Philbrick CT, Novelo RA (2006) A new species of Cipoia (Podostemaceae) from Minas Gerais, Brazil. Syst Bot 31:822–825

    Article  Google Scholar 

  • Cook CDK (1996) Aquatic plant book, 2nd ed. SPB Academic Publishing, The Hague

  • Cook CDK, Rutishauser R (2007) Podostemaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 9. Springer, Berlin, pp 304–344

    Google Scholar 

  • Cusset C (1992) Contribution a l’etude des Podostemaceae: 12. Les genres asiatiques. Bull Mus Natl Hist Nat Paris B Adansonia 14:13–54

    Google Scholar 

  • Cusset C, Cusset G (1988a) Etude sur les Podostemales. 9. Délimitations taxinomiques dans les Tristichaceae. Bull Mus Natl Hist Nat Paris B Adansonia 10:149–177

    Google Scholar 

  • Cusset G, Cusset C (1988b) Etude sur les Podostemales. 10. Structures florales et végétatives des Tristichaceae. Bull Mus Natl Hist Nat Paris B Adansonia 10:179–218

    Google Scholar 

  • Cusset G, Cusset C (1988c) Etude sur les Podostemales. 11. Répartition et évolution des Tristichaceae. Bull Mus Natl Hist Nat Paris B Adansonia 10:223–262

    Google Scholar 

  • Davis CC, Webb CO, Wurdack KJ, Jaramillo CA, Donoghue MJ (2005) Explosive radiation of Malpighiales supports a mid-Cretaceous origin of modern tropical rain forests. Amer Nat 165:E36–E65

    Article  Google Scholar 

  • Esau K (1965) Plant anatomy, 2nd edn. Wiley, New York

    Google Scholar 

  • Friedman WE (2008) Hydatellaceae are water lilies with gymnospermous tendencies. Nature 453:94–97

    CAS  Article  PubMed  Google Scholar 

  • Fujinami R, Imaichi R (2015) Developmental morphology of flattened shoots in Dalzellia ubonensis and Indodalzellia gracilis with implications for the evolution of diversified shoot morphologies in the subfamily Tristichoideae (Podostemaceae). Am J Bot 102:484–859

    Article  Google Scholar 

  • Fujinami R, Ghogue JP, Imaichi R (2013) Developmental morphology of the controversial ramulus organ of Tristicha trifaria (subfamily Tristichoideae, Podostemaceae): implications for evolution of a unique body plan in Podostemaceae. Int J Plant Sci 174:609–618

    Article  Google Scholar 

  • Gray J (ed) (2004) Programmed cell death in plants. Blackwell, Oxford

    Google Scholar 

  • Gustafsson MHG, Bittrich W, Stevens PF (2002) Phylogeny of Clusiaceae based on rbcL sequences. Int J Plant Sci 163:1045–1054

    CAS  Article  Google Scholar 

  • Haston E, Richardson JE, Stevens PF, Chase MW, Harris DJ (2009) The Linear Angiosperm Phylogeny Group (LAPG) III: a linear sequence of the families in APG III. Bot J Linn Soc 161:128–131

    Article  Google Scholar 

  • Hiyama Y, Tsukamoto I, Imaichi R, Kato M (2002) Developmental anatomy and branching of roots of four Zeylanidium species (Podostemaceae), with implications for evolution of foliose roots. Ann Bot 90:735–744

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Imaichi R, Ichiba T, Kato M (1999) Developmental morphology and anatomy of Malaccotristicha malayana (Podostemaceae). Int J Plant Sci 160:253–259

    Article  Google Scholar 

  • Imaichi R, Maeda R, Suzuki K, Kato M (2004) Developmental morphology of foliose shoots and seedlings of Dalzellia zeylanica (Podostemaceae) with special reference to their meristems. Bot J Linn Soc 144:289–302

    Article  Google Scholar 

  • Imaichi R, Hiyama Y, Kato M (2005) Leaf development in absence of shoot apical meristem in Zeylanidium subulatum (Podostemaceae). Ann Bot 96:51–58

    Article  PubMed  PubMed Central  Google Scholar 

  • Imamura S (1927) Discovery of Podostemonaceae in Japan. Proc Imp Acad Jap 3:616–618

    Google Scholar 

  • Imamura S (1928a) Ueber Cladopus japonicus n. sp., eine Podostemonaceen in Japan. J Jap Bot 5:50–62 (in Japanese with German summary)

    Google Scholar 

  • Imamura S (1928b) Über Cladopus japonicus n. sp., eine Podostemonaceen in Japan. Bot Mag Tokyo 42:379–387 (pl. 5, 6)

    Article  Google Scholar 

  • Jäger-Zürn I (1999) Developmental morphology of the shoot system of Podostemum subulatum (Podostemaceae-Podostemoideae): part V of the series ‘morphology of Podostemaceae’. Beitr Biol Pflanzen 71:281–334

    Google Scholar 

  • Jäger-Zürn I (2007) The shoot apex of Podostemaceae: de novo structure or reduction of the conventional type? Flora 202:383–394

    Article  Google Scholar 

  • Katayama N, Koi S, Kato M (2008) Developmental anatomy of the reproductive shoot in Hydrobryum japonicum (Podostemaceae). J Plant Res 121:417–424

    Article  PubMed  Google Scholar 

  • Katayama N, Koi S, Kato M (2010) Expression of shoot meristemless, wuschel, and asymmetric leaves1 homologs in the shoots of Podostemaceae: implications for the evolution of novel shoot organogenesis. Plant Cell 22:2131–2140

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Katayama N, Kato M, Nishiuchi T, Yamada T (2011) Comparative anatomy of embryogenesis in three species of Podostemaceae and evolution of the loss of embryonic shoot and root meristems. Evol Dev 13:333–342

    Article  PubMed  Google Scholar 

  • Katayama N, Kato M, Yamada T (2013) Origin and development of the cryptic shoot meristem in Zeylanidium lichenoides (Podostemaceae). Amer J Bot 100:635–646

    CAS  Article  Google Scholar 

  • Katayama N, Kato M, Imaichi R (2016) Habitat specificity enhances genetic differentiation in two species of aquatic Podostemaceae in Japan. Am J Bot 103. doi:10.3732/ajb.1500385

  • Kato M (2004) Taxonomic study of Podostemaceae of Thailand 1. Hydrobryum and related genera with crustaceous roots (subfamily Podostemoideae). Acta Phytotax Geobot 55:133–165

    Google Scholar 

  • Kato M (2006) Taxonomic study of Podostemaceae of Thailand 2. Subfamily Podostemoideae with ribbon-like roots and subfamily Tristichoideae. Acta Phytotax Geobot 57:1–54

    Google Scholar 

  • Kato M (2008) A taxonomic study of Podostemaceae of Japan. Bull Natl Mus Nat Sci ser B (Bot) 34:63–73

    Google Scholar 

  • Kato M (2011) Taxonomic enumeration of Podostemaceae of Cambodia and Vietnam. Bull Natl Mus Nat Sci ser B (Bot) 37:1–8

    Google Scholar 

  • Kato M (2013) The illustrated book of plant systematics in color: Podostemaceae of the world. Hokuryukan, Tokyo

    Google Scholar 

  • Kato M, Fukuoka F (2002) Two new species of Diplobryum (Podostemaceae, Podostemoideae) from Laos. Acta Phytotax Geobot 53:115–120

    Google Scholar 

  • Kato M, Koi S (2009) Taxonomic studies of Podostemaceae of Thailand. 3. Six new and a rediscovered species. Gard Bull Singapore 61:55–72

    Google Scholar 

  • Kato M, Kita Y, Koi S (2003) Molecular phylogeny, taxonomy and biogeography of Malaccotristicha australis comb. nov. (syn. Tristicha australis) (Podostemaceae). Aust Syst Bot 16:177–183

    CAS  Article  Google Scholar 

  • Kato M, Koi S, Kita Y (2004) A new foliose-rooted genus of Podostemaceae (subfamily Podostemoideae) from Thailand with note on root evolution. Acta Phytotax Geobot 55:65–73

    Google Scholar 

  • Khanduri P, Tandon R, Uniyal PL, Bhat V, Pandey AK (2015) Comparative morphology and molecular systematics of Indian Podostemaceae. Plant Syst Evol 301:861–882

    Article  Google Scholar 

  • Kita Y, Kato M (2001) Infrafamilial phylogenetic relationships of the aquatic angiosperm family Podostemaceae inferred from matK sequence data. Plant Biol 3:156–163

    CAS  Article  Google Scholar 

  • Kita Y, Kato M (2004a) Molecular phylogeny of Cladopus and Hydrobryum (Podostemaceae, Podostemoideae) with implications for their biogeography in East Asia. Syst Bot 29:921–932

    Article  Google Scholar 

  • Kita Y, Kato M (2004b) Phylogenetic relationships between disjunctly occurring groups of Tristicha trifaria (Podostemaceae). J Biogeogr 31:1605–1612

    Article  Google Scholar 

  • Kita Y, Kato M (2005) Seedling developmental anatomy of an undescribed Malaccotristicha species (Podostemaceae, subfamily Tristichoideae) with implications for body plan evolution. Plant Syst Evol 254:221–232

    Article  Google Scholar 

  • Koi S, Katayama N (2013) Gene expression analysis of aquatic angiosperms Podostemaceae to gain insight into the evolution of their enigmatic morphology. In: De Smet I (ed) Plant organogenesis: methods and protocols. Methods in molecular biology, vol 959. Springer Science + Business Media, New York, pp 83‒95

  • Koi S, Kato M (2003) Comparative developmental anatomy of the root in three species of Cladopus (Podostemaceae). Ann Bot 91:927–937

    Article  PubMed  PubMed Central  Google Scholar 

  • Koi S, Kato M (2007) Developmental morphology of shoot in Weddellina squamulosa (Podostemaceae) and implications for shoot evolution in the Podostemaceae. Ann Bot 99:1121–1130

    Article  PubMed  PubMed Central  Google Scholar 

  • Koi S, Kato M (2010a) Developmental anatomy of seedling of Indodalzellia gracilis (Podostemaceae). Plant Biol 12:794–799

    CAS  Article  PubMed  Google Scholar 

  • Koi S, Kato M (2010b) Developmental morphology of shoot and seedling and phylogenetic relationship of Diplobryum koyamae (Podostemaceae). Am J Bot 97:373–387

    CAS  Article  PubMed  Google Scholar 

  • Koi S, Kato M (2012) A taxonomic study of Podostemaceae subfamily Podostemoideae of Laos with phylogenetic analyses of Cladopus, Paracladopus and Polypleurum. Kew Bull 67:331–365

    Article  Google Scholar 

  • Koi S, Kato M (2015a) The taxonomy of Podostemaceae subfamily Tristichoideae in Laos, with descriptions of seven new species. Acta Phytotax Geobot 66:61–79

    Google Scholar 

  • Koi S, Kato M (2015b) Additions to Podostemaceae subfamily Podostemoideae of Laos. Acta Phytotax Geobot 66:173–179

    Google Scholar 

  • Koi S, Imaichi R, Kato M (2005) Endogenous leaf initiation in the apical-meristemless shoot of Cladopus queenslandicus (Podostemaceae) and implications for evolution of shoot morphology. Int J Plant Sci 166:199–206

    Article  Google Scholar 

  • Koi S, Tsukamoto I, Inagawa R, Kubo N, Fujinami R, Imaichi R, Kato M (2006) Comparative anatomy of root meristem and root cap in some species of Podostemaceae and the evolution of root dorsiventrality. Amer J Bot 93:682–692

    Article  Google Scholar 

  • Koi S, Kita Y, Kato M (2008) Paracladopus chanthaburiensis, a new species of Podostemaceae from Thailand, with notes on its morphology, phylogeny and distribution. Taxon 57:201–210

    Google Scholar 

  • Koi S, Rutishauser R, Kato M (2009) Phylogenetic relationship and morphology of Dalzellia gracilis (Podostemaceae, subfamily Tristichoideae) with proposal of a new genus. Int J Plant Sci 170:237–246

    CAS  Article  Google Scholar 

  • Koi S, Kita Y, Hirayama Y, Rutishauser R, Huber KA, Kato M (2012a) Molecular phylogenetic analysis of Podostemaceae: implications for taxonomy of major groups. Bot J Linn Soc 169:461–492

    Article  Google Scholar 

  • Koi S, Werukamkul P, Amporpan L, Kato M (2012b) Seedling development of Hanseniella, Hydrobryum and Thawatchaia (Podostemaceae) and implications on body plan evolution in the Hydrobryum clade. Plant Syst Evol 298:1755–1766

    Article  Google Scholar 

  • Koi S, Ikeda H, Rutishauser R, Kato M (2015) Historical biogeography of river-weeds (Podostemaceae). Aquat Bot 127:62–69

    Article  Google Scholar 

  • Korotkova N, Schneider JV, Quandt D, Worberg A, Zizka G, Borsch T (2009) Phylogeny of the eudicot order Malpighiales: analysis of a recalcitrant clade with sequences of the petD group II intron. Plant Syst Evol 282:201–228

    Article  Google Scholar 

  • Landolt E, Jäger-Zürn I, Schnell RAA (eds) (1988) Extreme adaptations in angiospermous hydrophytes. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Lansdown RV (2012) The conservation of aquatic and wetland plants in the Indo-Burma region. In: Allen DJ, Smith KG, Darwall WRT (eds) The status and distribution of freshwater biodiversity in Indo-Burma, Chap 7, pp 114‒133. https://cmsdata.iucn.org/downloads/ib_chapter_7__the_conservation_of_aquatic_and_wetland_plants_in_the_indo_burma_region.pdf

  • Lieberman BS, Eldredge N (1996) Trilobite biogeography in the Middle Devonian: geological processes and analytical methods. Paleobiology 22:66–79

    Google Scholar 

  • Mathew CJ, Satheesh VK (1997) Taxonomy and distribution of the Podostemaceae in Kerala, India. Aquat Bot 57:243–274

    Article  Google Scholar 

  • Mohan Ram HY, Sehgal A (1997) In vitro studies on developmental morphology of Indian Podostemaceae. Aquat Bot 57:97–132

    Article  Google Scholar 

  • Moline P, Thiv M, Ameka GK, Ghogue J-P, Pfeifer E, Rutishauser R (2007) Comparative morphology and molecular systematics of African Podostemaceae-Podostemoideae, with emphasis on Dicraeanthus and Ledermanniella from Cameroon. Int J Plant Sci 168:159–180

    CAS  Article  Google Scholar 

  • Nei M (2013) Mutation-driven evolution. Oxford University Press, Oxford

    Google Scholar 

  • Ota M, Imaichi R, Kato M (2001) Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae). Am J Bot 88:382–390

    CAS  Article  PubMed  Google Scholar 

  • Philbrick CT (1984) Aspects of floral biology, breeding system, and seed and seedling biology in Podostemum ceratophyllum (Podostemaceae). Syst Bot 9:166–174

    Article  Google Scholar 

  • Philbrick CT, Novelo RA, Irgang BE (2004) Two new genera of Podostemaceae from the state of Minas Gerais, Brazil. Syst Bot 29:109–117

    Article  Google Scholar 

  • Philbrick CT, Bove CP, Stevens HI (2010) Endemism in Neotropical Podostemaceae. Ann Missouri Bot Gard 97:425–456

    Article  Google Scholar 

  • Piazza P, Jasinski S, Tsiantis M (2005) Evolution of leaf developmental mechanisms. New Phytol 167:693–710

    CAS  Article  PubMed  Google Scholar 

  • Ruhfel BR, Bittrich V, Bove CP, Gustafsson MHG, Philbrick CT, Rutishauser R, Xi Z, Davis CC (2011) Phylogeny of the clusioid clade (Malpighiales): evidence from the plastid and mitochondrial genomes. Am J Bot 98:306–325

    Article  PubMed  Google Scholar 

  • Rutishauser R (1995) Developmental patterns of leaves in Podostemaceae compared with more typical flowering plants: saltational evolution and fuzzy morphology. Can J Bot 73:1305–1317

    Article  Google Scholar 

  • Rutishauser R (1997) Structural and developmental diversity in Podostemaceae (river-weeds). Aquat Bot 57:29–70

    Article  Google Scholar 

  • Rutishauser R, Huber KA (1991) The developmental morphology of Indotristicha ramosissima (Podostemaceae, Tristichoideae). Plant Syst Evol 178:195–223

    Google Scholar 

  • Rutishauser R, Pfeifer E, Grob V, Bernhard A (2007) Podostemaceae of African and Madagascar: keys to genera and species, including genera descriptions, illustrations to all species known, synonyms, and literature list. http://.systbot.uzh.ch/podostemaceae

  • Saitou N (2009) From selectionism to neutralism: paradigm shift of evolutionary studies. NTT Publishing, Tokyo (in Japanese)

    Google Scholar 

  • Savolainen V, Fay MF, Albach DC, Backlund A, van der Bank M, Cameron KM, Johnson SA, Lledó MD, Pintaud J-C, Powell M, Sheahan MC, Soltis DE, Soltis PS, Weston P, Whitten WM, Wurdack KJ, Chase MW (2000) Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull 55:257–309

    Article  Google Scholar 

  • Sculthorpe CD (1967) The biology of aquatic vascular plants. Edward Arnold, London (reprinted 1985 by Koeltz Scientific Books, Königstein)

  • Sehgal A, Khurana JP, Sethi M, Ara H (2011) Occurrence of unique three-celled megagametophyte and single fertilization in an aquatic angiosperm–Dalzellia zeylanica (Podostemaceae–Tristichoideae). Sexual Plant Repr 24:199–210

    Article  Google Scholar 

  • Seno J, Hattori M (2013) The northernmost locality of Cladopus japonicus Imamura (Podostemaceae). J Jap Bot 88:61–63

    Google Scholar 

  • Sharma BD, Karthikeya D, Shetty BV (1974) Indotristicha tirunelveliana Sharma, Karthik. & Shetty—a new species of Podostemaceae from South India. Bull Bot Surv India 16:157–161

    Google Scholar 

  • Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Price LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461

    Article  Google Scholar 

  • Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS, Bell CD, Latvis M, Crawley S, Black C, Diouf D, Xi Z, Rushworth CA, Gitzendanner MA, Sytsma KJ, Qiu Y-L, Hilu KW, Davis CC, Sanderson MJ, Beaman RS, Olmstead RG, Judd WS, Donoghue MJ, Soltis PS (2011) Angiosperm phylogeny: 17 genes, 640 taxa. Am J Bot 98:704–730

    Article  PubMed  Google Scholar 

  • Steeves TA, Sussex IM (1989) Patterns in plant development, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Stuessy TF, Crawford DJ, Marticorena C (1990) Patterns of phylogeny in the endemic vascular flora of the Juan Fernandez Islands, Chile. Syst Bot 15:338–346

    Article  Google Scholar 

  • Suzuki K, Kita Y, Kato M (2002) Comparative developmental anatomy of seedlings in nine species of Podostemaceae (subfamily Podostemoideae). Ann Bot 89:755–765

    Article  PubMed  PubMed Central  Google Scholar 

  • Thiv M, Ghogue J-P, Grob V, Huber K, Pfeifer E, Rutishauser R (2009) How to get off the mismatch at the generic rank in African Podostemaceae? Plant Syst Evol 283:57–77

    CAS  Article  Google Scholar 

  • Tokuoka T, Tobe H (2006) Phylogenetic analyses of Malpighiales using plastid and unclear DNA sequences, with particular reference to the embryology of Euphorbiaceae sens. str. J Plant Res 119:599–616

    CAS  Article  PubMed  Google Scholar 

  • Werukamkul P, Amporpan L, Koi S, Kato M (2012) Taxonomic study of Podostemaceae in Loei Province, northeastern Thailand. Acta Phytotax Geobot 63:11–28

    Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution, and conservation, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Willis JC (1902) Studies in the morphology and ecology of the Podostemaceae of Ceylon and India. Ann R Bot Gard Peradeniya 1:268–465 (pl. IV‒XXXVIII)

    Google Scholar 

  • Willis JC (1914) On the lack of adaptation in the Tristichaceae and Podostemaceae. Proc R Soc Lond B 87:532–550

    Article  Google Scholar 

  • Wurdack KJ, Davis CC (2009) Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Am J Bot 90:1151–1570

    Google Scholar 

  • Xi Z, Ruhfel BR, Schaefer H, Amorim AM, Sugumaran M, Wurdack KJ, Endress PK, Matthews ML, Stevens PF, Mathews S, Davis CC (2012) Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales. Proc Natl Acad Sci USA 109:17519–17524

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

I thank many colleagues in Japan and abroad for collaboration on the studies of Podostemaceae, in particular, S. Koi, N. Katayama, and Y. Hirayama, my coworkers in field and lab. This paper is a product of those collaborative studies. Thanks are also due to N. Katayama, S. Koi and H. Okada for their useful comments on the manuscript, to N. Katayama for her help with drawing Fig. 6, and D. E. Boufford for his linguistic check of the manuscript. This study was supported by JSPS KAKENHI Grant Number 25291091.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masahiro Kato.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kato, M. Multidisciplinary studies of the diversity and evolution in river-weeds. J Plant Res 129, 397–410 (2016). https://doi.org/10.1007/s10265-016-0801-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-016-0801-8

Keywords

  • Biogeography
  • Fuzzy morphology
  • Gene expression
  • Phylogeny
  • Podostemaceae
  • Saltational evolution