Skip to main content
Log in

The molecular population genetics of shoot development in Arabidopsis thaliana

  • Original paper
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Studies in Arabidopsis thaliana have provided us with a wealth of information about the genetic pathways that regulate plant morphogenesis. This developmental genetic treasure trove represents a fantastic resource for researchers interested in the microevolution of development. Several laboratories have begun using molecular population genetic analyses to investigate the evolutionary forces that act upon loci that regulate shoot morphogenesis. Much of this work has focused on coding sequence variation in transcription factors; however, recent studies have explored sequence variation in other types of proteins and in promoter regions. Several genes that regulate shoot development contain signatures of selective sweeps associated with positive selection or harbor putative balanced polymorphisms in coding and noncoding sequences. Other regulatory genes appear to be evolving neutrally, but have accumulated potentially deleterious replacement polymorphisms.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ACL5 :

ACAULIS5

AP :

APETALA

Bla-1:

Blanes/Gerona-1

Cvi-0:

Cape Verde Islands

CAL :

CAULIFLOWER

CLV :

CLAVATA

Col-0:

Columbia

CRY2 :

CRYPTOCHROME2

FLC :

FLOWERING LOCUS C

FRI :

FRIGIDA

FUL :

FRUITFULL

GL1 :

GLABROUS1

Gr-3:

Graz-3

Ler :

Landsberg erecta

LFY :

LEAFY

LRR:

Leucine-rich repeat

LD:

Linkage disequilibrium

PHYA :

PHYTOCHROME A

PI :

PISTILLATA

QTL:

Quantitative trait locus

SEP :

SEPALLATA

πsilent :

Silent site nucleotide diversity

πs :

Synonymous site nucleotide diversity

πa :

Nonsynonymous site nucleotide diversity

TFL1 :

TERMINAL FLOWER1

VRN 1, 2 :

VERNALIZATION 1 and 2

VIN3 :

VERNALIZATION INSENSITIVE3

WUS :

WUSCHEL

References

  • Alonso-Blanco C, Koornneef M (2000) Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci 5:22–29

    Article  PubMed  CAS  Google Scholar 

  • Al-Shehbaz IA, O’Kane SL (2002) Taxonomy and phylogeny of Arabidopsis (Brassicaceae). The Arabidopsis Book 6:1–22.

    Google Scholar 

  • Banfield MJ, Brady RL (2000) The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297:1159–1170

    Article  PubMed  CAS  Google Scholar 

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C, (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    Article  PubMed  CAS  Google Scholar 

  • Blázquez M, Soowal L, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844

    PubMed  CAS  Google Scholar 

  • Botto JF, Alonso-Blanco C, Garzarón I, Sánchez RA, Casal JJ (2003) The Cape Verde Islands allele of cryptochrome 2 enhances cotyledon unfolding in the absence of blue light in Arabidopsis. Plant Physiol 133:1547–1556

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    Article  PubMed  CAS  Google Scholar 

  • Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83

    Article  PubMed  CAS  Google Scholar 

  • Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL (2002) The cost of inbreeding in Arabidopsis. Nature 416:531–534

    Article  PubMed  CAS  Google Scholar 

  • Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci USA 101:15670–15675

    Article  PubMed  CAS  Google Scholar 

  • Cheng YL, Chen XM (2004) Posttranscriptional control of plant development. Curr Opin Plant Biol 7:20–25

    Article  PubMed  CAS  Google Scholar 

  • Clauss MJ, Mitchell-Olds T (2003) Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history. Mol Ecol 12:1287–1299

    Article  PubMed  CAS  Google Scholar 

  • Doebley J, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10:1075–1082

    Article  PubMed  CAS  Google Scholar 

  • El-Assal SE, Alonso-Blanco C, Hanhart CJ, Koornneef M (2004) Pleiotropic effects of the Arabidopsis cryptochrome2 allelic variation underlie fruit trait-related QTL. Plant Biol (Stuttg) 6:370–374

    Article  CAS  Google Scholar 

  • El-Assal SED, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29:435–440

    Article  CAS  Google Scholar 

  • El-Assal SED, Alonso-Blanco C, Peeters AJM, Wagemaker C, Weller JL, Koornneef M (2003) The role of cryptochrome 2 in flowering in Arabidopsis. Plant Physiol 133:1504–1516

    Article  CAS  Google Scholar 

  • Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127:725–734

    PubMed  CAS  Google Scholar 

  • Ford MJ (2002) Applications of selective neutrality tests to molecular ecology. Mol Ecol 11:1245–1262

    Article  PubMed  CAS  Google Scholar 

  • Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132:1107–1114

    Article  PubMed  CAS  Google Scholar 

  • Hauser MT, Harr B, Schlotterer C (2001) Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol Biol Evol 18:1754–1763

    PubMed  CAS  Google Scholar 

  • He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302:1751–1754

    Article  PubMed  CAS  Google Scholar 

  • Hill JP, Lord EM (1989) Floral development in Arabidopsis thaliana—a comparison of the wild-type and the homeotic pistillata mutant. Can J Bot 67:2922–2936

    Google Scholar 

  • Hill T, Day C, Zondlo S, Thackeray A, Irish V (1998) Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125:1711–1721

    PubMed  CAS  Google Scholar 

  • Honma T, Goto K (2000) The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127:2021–2030

    PubMed  CAS  Google Scholar 

  • Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159

    PubMed  CAS  Google Scholar 

  • Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16(Suppl):S1–17

    Article  PubMed  CAS  Google Scholar 

  • Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1933

    Article  PubMed  CAS  Google Scholar 

  • Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347

    Article  PubMed  CAS  Google Scholar 

  • Johnson NA, Porter AH (2001) Toward a new synthesis: population genetics and evolutionary developmental biology. Genetica 112:45–58

    Article  PubMed  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172

    Article  PubMed  CAS  Google Scholar 

  • Kreitman M (2000) Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet 1:539–559

    Article  PubMed  CAS  Google Scholar 

  • Kuittinen H, Salguero D, Aguadé M (2002) Parallel patterns of sequence variation within and between populations at three loci of Arabidopsis thaliana. Mol Biol Evol 19:2030–2034

    PubMed  CAS  Google Scholar 

  • Le Corre V, Roux F, Reboud X (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 19:1261–1271

    PubMed  CAS  Google Scholar 

  • Leyser O, Day S (2003) Mechanisms in plant development. Blackwell Publishing, Oxford

    Google Scholar 

  • Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833

    PubMed  CAS  Google Scholar 

  • Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  PubMed  CAS  Google Scholar 

  • McKay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12:1137–1151

    Article  PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (2000) Memories of winter: vernalization and the competence to flower. Plant Cell Env 23:1145–1153

    Article  Google Scholar 

  • Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc Natl Acad Sci USA 101:3281–3285

    Article  PubMed  CAS  Google Scholar 

  • Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA 100:10102–10107

    Article  PubMed  CAS  Google Scholar 

  • Mockler T, Yang H, Yu X, Parikh D, Cheng Y-c, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100:2140–2145

    Article  PubMed  CAS  Google Scholar 

  • Moore RC, Grant SR, Purugganan MD (2005) Molecular population genetics of redundant floral-regulatory genes in Arabidopsis thaliana. Mol Biol Evol 22:91–103

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Innan H (2002) Molecular population genetics. Curr Opin Plant Biol 5:69–73

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196

    Article  Google Scholar 

  • Olsen KM, Womack A, Garrett AR, Suddith JI, Purugganan MD (2002) Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway. Genetics 160:1641–1650

    PubMed  CAS  Google Scholar 

  • Olsen KM, Halldorsdottir SS, Stinchcombe JR, Weinig C, Schmitt J, Purugganan MD (2004) Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles. Genetics 167:1361–1369

    Article  PubMed  CAS  Google Scholar 

  • Otto SP (2000) Detecting the form of selection from DNA sequence data. Trends Genet 16:526–529

    Article  PubMed  CAS  Google Scholar 

  • Page DR, Grossniklaus U (2002) The art and design of genetic screens: Arabidopsis thaliana. Nat Rev Genet 3:124–136

    Article  PubMed  CAS  Google Scholar 

  • Poduska B, Humphrey T, Redweik A, Grbic V (2003) The synergistic activation of FLOWERING LOCUS C by FRIGIDA and a new flowering gene AERIAL ROSETTE 1 underlies a novel morphology in Arabidopsis. Genetics 163:1457–1465

    PubMed  CAS  Google Scholar 

  • Pruitt RE, Bowman JL, Grossniklaus U (2003) Plant genetics: a decade of integration. Nat Genet 33(Suppl):294–304

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD (1997) The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J Mol Evol 45:392–396

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD (2000) The molecular population genetics of regulatory genes. Mol Ecol 9:1451–1461

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD, Suddith JI (1998) Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: Nonneutral evolution and naturally occurring variation in floral homeotic function. Proc Natl Acad Sci USA 95:8130–8134

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD, Suddith JI (1999) Molecular population genetics of floral homeotic loci: departures from the equilibrium-neutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana. Genetics 151:839–848

    PubMed  CAS  Google Scholar 

  • Purugganan MD, Boyles AL, Suddith JI (2000) Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics 155:855–862

    PubMed  CAS  Google Scholar 

  • Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral identity in Arabidopsis. Development 126:1109–1120

    PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615

    PubMed  CAS  Google Scholar 

  • Riley RM, Jin W, Gibson G (2003) Contrasting selection pressures on components of the Ras-mediated signal transduction pathway in Drosophila. Mol Ecol 12:1315–1323

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg NA, Nordborg M (2002) Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nature Rev Genet 3:380–390

    Article  CAS  Google Scholar 

  • Schmid KJ, Ramos-Onsins S, Ringys-Beckstein H, Weisshaar B, Mitchell-Olds T (2005) A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism. Genetics 169:1601–1615

    Article  PubMed  CAS  Google Scholar 

  • Serino G, Deng XW (2003) The COP9 signalosome: regulating plant development through the control of proteolysis. Annu Rev Plant Biol 54:165–182

    Article  PubMed  CAS  Google Scholar 

  • Sharma VK, Carles C, Fletcher JC (2003) Maintenance of stem cell populations in plants. Proc Natl Acad Sci USA 100:11823–11829

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758

    Article  PubMed  CAS  Google Scholar 

  • Shepard KA, Purugganan MD (2003) Molecular population genetics of the Arabidopsis CLAVATA2 region: the genomic scale of variation and selection in a selfing species. Genetics 163:1083–1095

    PubMed  CAS  Google Scholar 

  • Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138:1163–1173

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Steimer A, Schob H, Grossniklaus U (2004) Epigenetic control of plant development: new layers of complexity. Curr Opin Plant Biol 7:11–19

    Article  PubMed  CAS  Google Scholar 

  • Stern DL (2000) Perspective: Evolutionary developmental biology and the problem of variation. Evolution 54:1079–1091

    PubMed  CAS  Google Scholar 

  • Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101:4712–4717

    Article  PubMed  CAS  Google Scholar 

  • Suh S-S, Choi K-R, Lee I (2003) Revisiting phase transition during flowering in Arabidopsis. Plant Cell Physiol 44:836–843

    Article  PubMed  CAS  Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004a) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10

    Article  CAS  Google Scholar 

  • Sung SB, Amasino RM (2004b) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tilly JJ, Allen DW, Jack T (1998) The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 125:1647–1657

    PubMed  CAS  Google Scholar 

  • Veit B (2004) Determination of cell fate in apical meristems. Curr Opin Plant Biol 7:57–64

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859

    Article  PubMed  CAS  Google Scholar 

  • Weinig C, Dorn LA, Kane NC, German ZM, Hahdorsdottir SS, Ungerer MC, Toyonaga Y, Mackay TFC, Purugganan MD, Schmitt J (2003) Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165:321–329

    PubMed  CAS  Google Scholar 

  • Werner JD, Borevitz JO, Warthmann N, Trainer GT, Ecker JR, Chory J, Weigel D (2005) Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proc Natl Acad Sci USA 102:2460–2465

    Article  PubMed  CAS  Google Scholar 

  • William DA, Su YH, Smith MR, Lu M, Baldwin DA, Wagner D (2004) Genomic identification of direct target genes of LEAFY. Proc Natl Acad Sci USA 101:1775–1780

    Article  PubMed  CAS  Google Scholar 

  • Wray GA (2003) Transcriptional regulation and the evolution of development. Int J Devel Biol 47:675–684

    CAS  Google Scholar 

  • Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20:1377–1419

    Article  PubMed  CAS  Google Scholar 

  • Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506–519

    Article  PubMed  CAS  Google Scholar 

  • Yang YZ, Jack T (2004) Defining subdomains of the K domain important for protein–protein interactions of plant MADS proteins. Plant Mol Biol 55:45–59

    Article  PubMed  CAS  Google Scholar 

  • Yang YZ, Fanning L, Jack T (2003a) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J 33:47–59

    Article  Google Scholar 

  • Yang YZ, Xiang HJ, Jack T (2003b) pistillata-5, an Arabidopsis B class mutant with strong defects in petal but not in stamen development. Plant J 33:177–188

    Article  CAS  Google Scholar 

  • Yoshida K, Kamiya T, Kawabe A, Miyashita NT (2003) DNA polymorphism at the ACAULIS5 locus of the wild plant Arabidopsis thaliana. Genes Genet Syst 78:11–21

    Article  PubMed  CAS  Google Scholar 

  • Zik M, Irish VF (2003) Flower development: initiation, differentiation, and diversification. Annu Rev Cell Dev Biol 19:119–140

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

I am grateful to Tom Jack for sharing results prior to publication and to Hilary Callahan, Ken Olsen, Michael Purugganan, members of my laboratory, and an anonymous reviewer for helpful comments on drafts of this manuscript. Research in my laboratory is supported by the D.D.E. fund at Barnard College.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kristen A. Shepard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shepard, K.A. The molecular population genetics of shoot development in Arabidopsis thaliana . Genetica 129, 19–36 (2007). https://doi.org/10.1007/s10709-006-0030-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-006-0030-5

Keywords

Navigation