Skip to main content
SpringerLink
Log in

Genetic structure of duckweed population of Spirodela, Landoltia and Lemna from Lake Tai, China

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Presenting a basic framework for using MLST to characterize Spirodela, Landoltia and in particular Lemna strains at the species level, and to study population genetics and evolution history of natural duckweed populations.

Abstract

Duckweed is widely used in environmental biotechnology and has recently emerged as a potential feedstock for biofuels due to its high growth rate and starch content. The genetic diversity and composition of a natural duckweed population in genera Spirodela, Landoltia and Lemna from Lake Tai, China, were investigated using probabilistic analysis of multilocus sequence typing (MLST). The 78 strains were categorized into five lineages, among which strains representing L. aequinoctialis and S. polyrhiza were predominant. Among the five lineages, interlineage transfers of markers were infrequent and no recombination was statistically detected. Tajima’s D tests determined that all loci are subject to population bottlenecks, which is likely one of the main reasons for the low genetic diversity observed within the lineages. Interestingly, strains of L. turionifera are found to contain small admixture from L. minor, providing rare evidence of transfer of genetic materials in duckweed. This was discussed with respect to the hypothesis that a cross of these two gave rise to L. japonica. Moreover, the conventional maximum-likelihood phylogenetic analysis clearly recognized all the species in the three genera with high bootstrap supports. In conclusion, this work offers a basic framework for using MLST to characterize Spirodela, Landoltia and in particular Lemna strains at the species level, and to study population genetics and evolution history of natural duckweed populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

atpF–atpH :

Intergenic spacer between ATPase subunit I (atpF) and ATPase subunit III (atpH)

matK :

Maturase K gene

ML:

Maximum likelihood

MLST:

Multilocus sequence typing

rpoB :

RNA polymerase beta subunit gene

ST:

Sequence type

I cong :

Index of congruence

References

  • Appenroth KJ, Borisjuk N, Lam E (2013) Telling duckweed apart: genotyping technologies for the Lemnaceae. Chin J Appl Environ Biol 19:1–10

    Article  CAS  Google Scholar 

  • Bog M, Baumbach H, Schween U, Hellwig F, Landolt E, Appenroth KJ (2010) Genetic structure of the genus Lemna L. (Lemnaceae) as revealed by amplified fragment length polymorphism. Planta 232:609–619

    Article  CAS  PubMed  Google Scholar 

  • Bog M, Schneider P, Hellwig F, Sachse S, Kochieva E, Martyrosian E, Landolt E, Appenroth KJ (2013) Genetic characterization and barcoding of taxa in the genus Wolffia Horkel ex Schleid. (Lemnaceae) as revealed by two plastidic markers and amplified fragment length polymorphism (AFLP). Planta 237:1–13

    Article  CAS  PubMed  Google Scholar 

  • Brain RA, Solomon KR (2007) A protocol for conducting 7-day daily renewal tests with Lemna gibba. Nat Protocols 2:979–987

    Article  CAS  Google Scholar 

  • Cabrera LI, Salazar GA, Chase MW, Mayo SJ, Bogner J, Dávila P (2008) Phylogenetic relationships of aroids and duckweeds (Araceae) inferred from coding and noncoding plastid DNA. Am J Bot 95:1153–1165

    Article  CAS  PubMed  Google Scholar 

  • Chase MW, Fay MF (2009) Barcoding of plants and fungi. Science 325:682–683

    Article  CAS  PubMed  Google Scholar 

  • Chase MW, Salamin N, Wilkinson M, Dunwell JM, Kesanakurthi RP, Haidar N, Savolainen V (2005) Land plants and DNA barcodes: short-term and long-term goals. Philos Trans R Soc Lond B Biol Sci 360:1889–1895

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng JJ, Stomp AM (2009) Growing duckweed to recover nutrients from wastewaters and for production of fuel ethanol and animal feed. Clean Soil Air Water 37:17–26

    Article  CAS  Google Scholar 

  • Chiang TY, Chiang YC, Chen YJ, Chou CH, Havanond S, Hong TN, Huang S (2001) Phylogeography of Kandelia candel in east asiatic mangroves based on nucleotide variation of chloroplast and mitochondrial DNAs. Mol Ecol 10:2697–2710

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772

    Article  CAS  Google Scholar 

  • De Lange L (1975) Gibbosity in the complex Lemna gibba/Lemna minor: literature survey and ecological aspects. Aquat Bot 1:327–332

    Article  Google Scholar 

  • De Vienne DM, Giraud T, Martin OC (2007) A congruence index for testing topological similarity between trees. Bioinformatics 23(23):3119–3124. doi:10.1093/bioinformatics/btm500

    Article  PubMed  Google Scholar 

  • Fazekas AJ, Burgess KS, Kesanakurti PR, Graham SW, Newmaster SG, Husband BC, Percy DM, Hajibabaei M, Barrett SCH (2008) Multiple multilocus DNA barcodes from the plastid genome discriminate plant species equally well. PLoS ONE 3:e2802

    Article  PubMed Central  PubMed  Google Scholar 

  • Feil EJ (2010) Linkage, selection, and the clonal complex. In: Robinson DA, Falush D, Feil EJ (eds) Bacterial population genetics in infectious disease. John Wiley & Sons, Hoboken, pp 19–35. doi:10.1002/9780470600122.ch2

    Chapter  Google Scholar 

  • Gliddon C, Belhassen E, Gouyon PH (1987) Genetic neighbourhoods in plants with diverse systems of mating and different patterns of growth. Heredity 59:29–32

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hilu KW, Borsch T, Müller K, Soltis DE, Soltis PS, Savolainen V, Chase MW, Powell MP, Alice LA, Evans R, Sauquet H, Neinhuis C, Slotta TAB, Rohwer JG, Campbell CS, Chatrou LW (2003) Angiosperm phylogeny based on matK sequence information. Am J Bot 90:1758–1776

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY (2001) Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Mol Ecol 10:2669–2681

    Article  CAS  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jordan WC, Courtney MW, Neigel JE (1996) Low levels of intraspecific genetic variation at a rapidly evolving chloroplast DNA Locus in North American duckweeds (Lemnaceae). Am J Bot 83:430–439

    Article  CAS  Google Scholar 

  • Kandeler R (1975) Species delimitation in the genus Lemna. Aquat Bot 1:365–376

    Article  Google Scholar 

  • Landolt E (1975) Morphological differentiation and geographical distribution of the Lemna gibba, Lemna minor group. Aquat Bot 1:345–363

    Article  Google Scholar 

  • Landolt E (1986) The family of Lemnaceae: a monographic study, vol 1. Veroffentlichungen des Geobotanischen Institutes Stiftung Rubel, ETH, Zurich

    Google Scholar 

  • Landolt E, Kandeler R (1987) The family of Lemnaceae: a monographic study. Phytochemistry, physiology, application, bibliography. Veröffentlichungen des Geobotanischen Institutes ETH Stiftung Rubel, Zurich

    Google Scholar 

  • Les D, Landolt E, Crawford DJ (1997) Systematics of the Lemnaceae (duckweeds): inferences from micromolecular and morphological data. Plant Syst Evol 204:161–177

    Article  Google Scholar 

  • Les DH, Crawford DJ, Landolt E, Gabel JD, Kimball RT (2002) Phylogeny and systematics of Lemnaceae, the duckweed family. Syst Bot 27:221–240

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lynch M (1984) Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Q Rev Biol 59:257–290

    Article  Google Scholar 

  • Maheshwari S, Gupta S (1967) Induction of flowering in Lemna paucicostata, a short-day plant, by chelating agents and iron. Planta 77:95–98

    Article  CAS  PubMed  Google Scholar 

  • Maiden MC (2006) Multilocus sequence typing of bacteria. Annu Rev Microbiol 60:561–588

    Article  CAS  PubMed  Google Scholar 

  • Marinc-Hrzenjak V, Kristl J, Krajncic B (2008) The effects of jasmonic acid and ethylene-di-o-hydroxyphenylacetic acid on floral induction and induction of turions in Spirodela polyrrhiza (L.) Schleiden. Acta Botanica Croatica 67:131–138

    Google Scholar 

  • Maruyama T, Birky JRC (1996) Effects of periodic selection on gene diversity in organelle genomes and other systems without recombination. Genet 127:449–451

    Google Scholar 

  • Miyawaki T, Matsumoto S, Takahashi W, Tanaka O (2013) Effect of heat-treated noradrenaline on flowering in Lemna. Biosci Biotechnol Biochem 77:1586–1588

    Article  CAS  PubMed  Google Scholar 

  • Naumann B, Eberius M, Appenroth KJ (2007) Growth rate based dose-response relationships and EC-values of ten heavy metals using the duckweed growth inhibition test (ISO 20079) with Lemna minor L. clone St. J Plant Physiol 164:1656–1664

    Article  CAS  PubMed  Google Scholar 

  • Orive ME (2001) Somatic mutations in organisms with complex life histories. Theor Popul Biol 59:235–249

    Article  CAS  PubMed  Google Scholar 

  • Pennisi E (2007) Wanted: a barcode for plants. Science 318:190–191

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genet 155:945–959

    CAS  Google Scholar 

  • Purves WK (1961) Dark reactions in the flowering of Lemna perpusilla 6746. Planta 56:684–690

    Article  Google Scholar 

  • Reid MS, Bieleski RL (1970) Response of Spirodela oligorrhiza to phosphorus deficiency. Plant Physiol 46:609–613

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Santamaría L (2002) Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecologica 23:137–154

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541

    Article  CAS  Google Scholar 

  • Seth PN, Venkataraman R, Maheshwari SC (1970) Studies on the growth and flowering of a short-day plant, Wolffia microscopica. Planta 90:349–359

    Article  CAS  PubMed  Google Scholar 

  • Shimakawa A, Shiraya T, Ishizuka Y, Wada KC, Mitsui T, Takeno K (2012) Salicylic acid is involved in the regulation of starvation stress-induced flowering in Lemna paucicostata. J Plant Physiol 169:987–991

    Article  CAS  PubMed  Google Scholar 

  • Silvertown J (2008) The evolutionary maintenance of sexual reproduction: evidence from the ecological distribution of asexual reproduction in clonal plants. Int J Plant Sci 169:157–168

    Article  Google Scholar 

  • Stomp AM (2005) The duckweeds: a valuable plant for biomanufacturing. Biotechnol Annu Rev 11:69–99

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genet 105:437–460

    CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vasseur L, Aarssen LW, Bennett T (1993) Allozymic variation in local apomictic populations of Lemna minor (Lemnaceae). Am J Bot 80:974–979

    Article  CAS  Google Scholar 

  • Wang W, Messing J (2011) High-throughput sequencing of three Lemnoideae (duckweeds) chloroplast genomes from total DNA. PLoS ONE 6:e24670

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang R, Ai B, Gao BQ, Yu S, Li YY, Chen XY (2009) Spatial genetic structure and restricted gene flow in a functionally dioecious fig, Ficus pumila L. var. pumila (Moraceae). Popul Ecol 51:307–315

    Article  Google Scholar 

  • Wang W, Wu Y, Yan Y, Ermakova M, Kerstetter R, Messing J (2010) DNA barcoding of the Lemnaceae, a family of aquatic monocots. BMC Plant Biol 10:205

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wernersson R, Pedersen AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3537–3539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu J, Cui W, Cheng JJ, Stomp AM (2011) Production of high-starch duckweed and its conversion to bioethanol. Biosyst Eng 110:67–72

    Article  Google Scholar 

  • Xu J, Zhao H, Stomp AM, Cheng JJ (2012) The production of duckweed as a source of biofuels. Biofuels 3:589–601

    Article  CAS  Google Scholar 

  • Xue H, Xiao Y, Jin Y, Li X, Fang Y, Zhao H, Zhao Y, Guan J (2012) Genetic diversity and geographic differentiation analysis of duckweed using inter-simple sequence repeat markers. Mol Biol Rep 39:547–554

    Article  CAS  PubMed  Google Scholar 

  • Yuan JX, Pan J, Wang BS, Zhang DM (2011) Genetic differentiation of Wolffia globosa in China. J Syst Evol 49:509–517

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the anonymous reviewers for their critical reading of the manuscript. This research was funded by a Key Project of Shenzhen Emerging Industries to JM (No. JC201104210118A).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen, 518055, China

    Jie Tang, Fei Zhang & Jiong Ma

  2. School of Water Resources and Environment, China University of Geosciences, Beijing, 100083, China

    Weihua Cui

Authors
  1. Jie Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weihua Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiong Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiong Ma.

Additional information

J. Tang and F. Zhang contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tang, J., Zhang, F., Cui, W. et al. Genetic structure of duckweed population of Spirodela, Landoltia and Lemna from Lake Tai, China. Planta 239, 1299–1307 (2014). https://doi.org/10.1007/s00425-014-2053-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2053-y

Keywords

Search

Navigation