Skip to main content
Log in

Polyploid speciation in Zea (Poaceae): cytogenetic insights

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

Abstract

Main conclusion

The analysis of meiotic pairing affinities and genomic formulae in species and hybrids of Zea allowed us to speculate an evolutionary model to recreate the ancient polyploidization of maize and allied species.

Abstract

The meiotic pairing affinities and the genomic formulae analysis in Zea species and hybrids obtained in new and previous crosses, together with the molecular data known in the genus, allowed us to speculate an evolutionary model to attempt to recreate the ancient polyploidization process of Zea species. We propose that x = 5 semispecies are the ancestors of all modern species of the genus. The complex evolutionary process that originated the different taxa could be included hybridization between sympatric diploid ancestral semispecies (2n = 10) and recurrent duplication of the hybrid chromosome number, resulting in distinct auto- and allopolyploids. After the merger and doubling of independent genomes would have undergone cytological and genetical diploidization, implying revolutionary changes in genome organization and genic balance processes. Based on the meiotic behaviour of the 2n = 30 hybrids, that showed homoeology between the A subgenomes of all parental species, we propose that this subgenome A would be pivotal in all the species and would have conserved the rDNA sequences and the pairing regulator locus (PrZ). In the hypothetical model postulated here, the ancestral semispecies with the pivotal subgenome A would have had a wide geographic distribution, co-occurring and hybridizing with the semispecies harbouring B subgenomes, thus enabling sympatric speciation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are provided in this published article or it will be provided from the corresponding author upon a reasonable request.

Abbreviations

Mya:

Million years ago

PrZ:

Pairing regulator locus

References

  • Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birchler JA, Veitia RA (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol 186:54–62

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Veitia RA (2012) Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc Natl Acad Sci USA 109:14746–14753

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Birchler JA, Bhadra U, Bhadra MP, Auger DL (2001) Dosage-dependent gene regulation in multicellular eukaryotes: implications for dosage compensation, aneuploid syndromes, and quantitative traits. Dev Biol 234:275–288

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Riddle NC, Auger DL, Veitia RA (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226

    Article  CAS  PubMed  Google Scholar 

  • Blasio F, Prieto P, Pradillo M, Naranjo T (2022) Genomic and meiotic changes accompanying polyploidization. Plants 11:125. https://doi.org/10.3390/plants11010125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calfee E, Gates D, Lorant A, Perkins MT, Coop G, Ross-Ibarra J (2021) Selective sorting of ancestral introgression in maize and teosinte along an elevational cline. PLoS Genet 17(10):e1009810. https://doi.org/10.1371/journal.pgen.1009810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doebley JF (1990) Molecular systematics of Zea (Gramineae). Maydica 35:143–150

    Google Scholar 

  • Feldman M, Levy AA (2012) Genome evolution due to allopolyploidization in wheat. Genetics 192:763–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Annu Rev Plant Biol 60:433–453

    Article  Google Scholar 

  • Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94:6809–6814

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • González GE, Poggio L (2011) Karyotype of Zea luxurians and Z. mays subsp. mays using FISH/DAPI and analysis of meiotic behavior of hybrids. Genome 54:26–32

    Article  PubMed  Google Scholar 

  • González GE, Poggio L (2015) Genomic affinities revealed by GISH suggests intergenomic restructuring between parental genomes of the paleopolyploid genus Zea. Genome 58:433–439

    Article  PubMed  Google Scholar 

  • González GE, Comas C, Confalonieri VA, Naranjo CA, Poggio L (2006) Genomic affinities between maize and Zea perennis using classical and molecular cytogenetic (GISH-FISH). Chrom Res 14:629–635

    Article  PubMed  Google Scholar 

  • González GE, Fourastié MF, Poggio L (2013) Número y composición de secuencias de los knobs (DAPI-FISH) y su utilidad en la caracterización de accesiones de maíz y teocintle. Rev Fitotec Mex 36:127–135

    Google Scholar 

  • Grant V (1985) The evolutionary process: a critical review of evolutionary theory. Columbia University Press, San Francisco

    Google Scholar 

  • Jenkins G, Rees H (1991) Strategies of bivalent formation in allopolyploid plants. Proc R Soc Biol Sci 243:209–214

    Article  ADS  Google Scholar 

  • Kovarik A, Dadejova M, Lim UK, Chase MW, Clarkson JJ, Knapp S, Leitch AR (2008) Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot 101:815–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82:651–663

    Article  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman M, Sánchez J, Buckler E, Doebley JF (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Molina MC, López CG, Staltari S, Chorzempa SE, Moreno Ferrero V (2013) Cryptic homoeology analysis in species and hybrids of genus Zea. Biol Plant 57:449–456

    Article  CAS  Google Scholar 

  • Moore G, Devos KM, Wang Z, Gale MD (1995) Cereal genome evolution. Grasses, line up and form a circle. Curr Biol 5:737–739

    Article  CAS  PubMed  Google Scholar 

  • Naranjo CA, Molina MC, Poggio L (1990) Evidencias de un número básico x=5 en el género Zea y su importancia en estudios del origen del maíz. Academia Nacional de Ciencias Exactas, Físicas y Naturales de Buenos Aires 5:43–53

    Google Scholar 

  • Poggio L, González GE (2018) Cytological diploidization of paleopolyploid genus Zea: divergence between homoeologous chromosomes or activity of pairing regulator genes? PLoS ONE 13(1):e0189644. https://doi.org/10.1371/journal.pone.0189644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poggio L, Molina MC, Naranjo CA (1990) Cytogenetic studies in the genus Zea: colchicine-induced multivalents. Theor Appl Genet 79:461–464

    Article  CAS  PubMed  Google Scholar 

  • Poggio L, Confalonieri VA, Comas C, González GE, Naranjo CA (1999) Genomic affinities among Zea luxurians, Zea perennis and Zea diploperennis: meiotic behaviour in the F1 and genomic in situ hybridization (GISH). Genome 42:993–1000

    Article  Google Scholar 

  • Poggio L, González GE, Confalonieri VA, Comas C, Naranjo CA (2005) The genome organization and diversification of maize and its allied species revisited: evidences from classical and FISH-GISH cytogenetics analysis. Cytogenet Genome Res 109:259–267

    Article  CAS  PubMed  Google Scholar 

  • Renny-Byfield S, Kovarik A, Kelly LJ et al (2013) Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. Plant J 74:829–839

    Article  CAS  PubMed  Google Scholar 

  • Renny-Byfield S, Rodgers-Melnick E, Ross-Ibarra J (2017) Gene fractionation and function in the ancient subgenomes of maize. Mol Biol Evol 34:1825–1832

    Article  CAS  PubMed  Google Scholar 

  • Ross-Ibarra J, Tenaillon M, Gaut BS (2009) Historical divergence and gene flow in the genus Zea. Genetics 181:1399–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnable JC, Freeling M (2011) Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize. PLoS ONE 6(3):e17855. https://doi.org/10.1371/journal.pone.0017855

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci USA 108:4069–4074

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Soares NR, Mollinari M, Oliveira GK, Pereira GS, Vieira MLC (2021) Meiosis in polyploids and implications for genetic mapping: a review. Genes 12:1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trend Ecol Evol 14:48–352

    Article  Google Scholar 

  • Soltis DE, Soltis PS, Rieseberg LH (1993) Molecular data and the dynamic nature of polyploidy. Crit Rev Plant Sci 12:243–273

    Article  CAS  Google Scholar 

  • Stebbins GL (1971) Chromosomal evolution in higher plants. Edward Arnold Ltd., London

    Google Scholar 

  • Swigoñová Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) On the tetraploid origin of the maize genome. Comp Funct Genomics 5:281–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Sybenga J (1975) Meiotic configurations. Springer, Berlin, Heidelberg, New York

    Book  Google Scholar 

  • Sybenga J (1996) Chromosome pairing affinity and quadrivalent formation in polyploids. Do segmental allopolyploids exist? Genome 39:1176–1184

    Article  CAS  PubMed  Google Scholar 

  • Sybenga J (1999) What makes homologous chromosomes find each other in meiosis? A review and a hypothesis. Chromosoma 108:209–219

    Article  CAS  PubMed  Google Scholar 

  • Sybenga J, Schabbink E, van Eden J, de Jong JH (1994) Pachytene pairing and metaphase I configurations in a tetraploid somatic Lycopersicon esculentum × L. peruvianum hybrid. Genome 37:54–60

    Article  CAS  PubMed  Google Scholar 

  • Tenaillon MI, Burban E, Huynh S et al (2023) Crop domestication as a step toward reproductive isolation. Am J Bot 110:e16173

    Article  PubMed  Google Scholar 

  • Tito C, Poggio L, Naranjo CA (1991) Cytogenetics studies in the genus Zea: DNA content and heterochromatin in species and hybrids. Theor Appl Genet 83:58–64

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Beissinger TM, Lorant A, Ross-Ibarra C, Ross-Ibarra J, Hufford MB (2017) The interplay of demography and selection during maize domestication and expansion. Genome Biol 18:215

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang N, Wang Y, Liu X et al (2023) Two teosintes made modern maize. Science 382:eadg8940

    Article  CAS  PubMed  Google Scholar 

  • Zafar Iqbal M, Cheng M, Zhao Y et al (2018) Mysterious meiotic behavior of autopolyploid and allopolyploid maize. Comp Cytogen 12(2):247–265

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Comisión Nacional de Investigaciones Científicas y Técnicas-CONICET (PIP 2115CO) and Universidad de Buenos Aires (UBACYT-20020170100614BA).

Author information

Authors and Affiliations

Authors

Contributions

GG and LP conceived and designed research, conducted experiments, analyzed data and wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Graciela Esther González.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest associated with the article.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Communicated by Dorothea Bartels.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González, G.E., Poggio, L. Polyploid speciation in Zea (Poaceae): cytogenetic insights. Planta 259, 67 (2024). https://doi.org/10.1007/s00425-024-04345-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-024-04345-x

Keywords

Navigation