Polyploidy and Paralogous Chromosome Regions


Polyploidisations, that is, genome doublings, have taken place on numerous occasions during the evolution of animals and plants. The resulting duplicated chromosome regions can be recognised by their similar repertoires of gene families. Duplicated genes or regions within a genome are referred to as paralogous, and each set of related chromosome regions comprise a paralogon. In the ancestor of vertebrates, before the origin of the gnathostomes (jawed vertebrates), two tetraploidisations took place, abbreviated 2R for two rounds of tetraploidisation. A third tetraploidisation, 3R, happened before the radiation of the true bony fishes, the teleosts. Paralogues resulting from tetraploidisations are called ohnologues in honour of Susumu Ohno, who proposed the vertebrate tetraploidisations. Paralogous genes can undergo either subfunctionalisation (become more specialised) or neofunctionalisation (evolve novel functions). The vertebrate tetraploidisations seem to have paved the way for many gnathostome innovations such as jaws, limbs, an advanced nervous system and a complex adaptive immune system.

Key Concepts:

  • Polyploidisations have happened on numerous occasions in plant evolution and several times in vertebrate evolution.

  • A paralogon is a set of related chromosome regions resulting from duplications, usually tetraploidizations.

  • Paralogous genes can undergo either subfunctionalisation (become more specialised), neofunctionalisation (evolve novel functions) or loss.

  • The tetraploidisations in vertebrate evolution are thought to have facilitated evolution of new functions and structures.

  • After tetraploidisations, rearrangements scramble the chromosome regions, thereby obscuring the relationships.

  • The tetraploidisations do not only generate copies of single genes. Since all genes are duplicated, whole networks of genes or pathways are duplicated, such as the phototransduction pathway.

  • The total number of genes are doubled after a tetraploidisation event. However, the number of genes is later reduced due to different mutations such as deletions.

Keywords: paralogue; orthologue; Ohnologue; gene duplication; genome duplication; polyploidy; polyploidisation; tetraploidy; tetraploidisation

Figure 1.

Proposed evolutionary history for the chromosomal regions containing the five gene families neurotrophin Trk receptors (NTRK), Src homology 2 domain containing (SHC), tropomodulin (TMOD), hyaluronan and proteoglycan link protein (HAPLN) and chondroitin sulfate proteoglycans aggrecan, versican, neurocan and brevican (CAN). A single ancestral chromosomal region was quadrupled in the basal vertebrate tetraploidisations. Subsequently, one local duplication took place whereupon a few paralogues were lost, leading to the present situation in the human genome. The number below each box shows the chromosomal position in Mb. Note that the gene order has been reshuffled to highlight similarities between the duplicated chromosomes. The number to the side of each line shows the chromosome number. The double dash indicates the breakpoint for a translocation involving chromosomes 9 and 5. Based on data from Hallböök et al..

Figure 2.

Proposed evolutionary history of the chromosomal regions containing voltage‐gated sodium channel (SCN) alpha genes and some of the adjacent gene families. A single ancestral chromosomal region was quadrupled in the basal vertebrate tetraploidisations. A third tetraploidisation took place in the teleost fish lineage. Local gene duplications have taken place both before and after the tetraploidisations. Some paralogues have been lost. The present gene repertoire is shown for human and zebrafish. Each gene's name or subtype is shown in its box. TGF, transforming growth factor; IGFBP, insulin‐like growth factor binding protein; NPY, neuropeptide Y; and PYY, peptide YY. Each Hox cluster contains a large number of genes. The number below each box shows the chromosomal position in Mb. Note that the gene order has been reshuffled to highlight similarities between the duplicated chromosomes. The number to the side of each line shows the chromosome number. The double dash indicates the breakpoint for a translocation from human chromosome 7 to chromosome 3. In the zebrafish, four breakages and translocations have taken place. Drawn from data in Widmark et al. and Sundström et al..



Aburomia R, Khaner O and Sidow A (2003) Functional evolution in the ancestral lineage of vertebrates or when genomic complexity was wagging its morphological tail. Journal of Structural and Functional Genomics 3: 45–52.

Amores A, Catchen J, Ferrara A, Fontenot Q and Postlethwait JH (2011) Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188: 799–808.

Ayala FJ (1999) Molecular clock mirages. BioEssays 21: 71–75.

Catchen JM, Conery JS and Postlethwait JH (2008) Inferring ancestral gene order. Methods in Molecular Biology 452: 365–383.

Coulier F, Popovici C, Villet R and Birnbaum D (2000) MetaHox gene clusters. Journal of Experimental Zoology 288: 345–351.

Crow KD, Smith CD, Cheng JF, Wagner GP and Amemiya CT (2012) An independent genome duplication inferred from Hox paralogs in the American paddlefish – A representative basal ray‐finned fish and important comparative reference. Genome Biology and Evolution 4: 937–953.

David L, Blum S, Feldman MW, Lavi U and Hillel J (2003) Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Molecular Biology and Evolution 20: 1425–1434.

Dehal P and Boore J (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology 3: e314.

Edwards JH (1991) The Oxford Grid. Annals of Human Genetics 55: 17–31.

Evans BJ, Kelley DB, Tinsley RC, Melnick DJ and Cannatella DC (2004) A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Molecular Phylogenetics and Evolution 33: 197–213.

Freeling M and Thomas BC (2006) Gene‐balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Research 16: 805–814.

Gallardo MH, González CA and Cebrián I (2006) Molecular cytogenetics and allotetraploidy in the red vizcacha rat, Tympanoctomys barrerae (Rodentia, Octodontidae). Genomics 88: 214–221.

Gallardo MH, Kausel G, Jiménez A et al. (2004) Whole‐genome duplications in South American desert rodents (Octodontidae). Biological Journal of the Linnean Society 82: 443–451.

Hallböök F, Wilson K, Thorndyke M and Olinski RP (2006) Formation and evolution of the chordate neurotrophin and Trk receptor genes. Brain, Behavior and Evolution 68: 133–144.

Holland LZ (2009) Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nature Reviews Neuroscience 10: 736–746.

Holland PWH (1999) Gene duplication: past, present and future. Seminars in Cell and Developmental Biology 10: 541–547.

Jaillon O, Aury JM, Brunet F et al. (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto‐karyotype. Nature 431: 946–957.

Jiao Y, Leebens‐Mack J, Ayyampalayam S et al. (2012) A genome triplication associated with early diversification of the core eudicots. Genome Biology 13: R3.

Jiao Y, Wickett NJ, Ayyampalayam S et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100.

Kawashima T, Kawashima S, Tanaka C et al. (2009) Domain shuffling and the evolution of vertebrates. Genome Research 19: 1393–1403.

Larhammar D and Risinger C (1994) Molecular genetic aspects of tetraploidy in the common carp, Cyprinus carpio. Molecular Phylogenetics and Evolution 3: 59–68.

Le Comber SC and Smith C (2004) Polyploidy in fishes: patterns and processes. Biological Journal of the Linnean Society 82: 431–442.

Ludwig L, Belfiore NM, Pitra C, Svirsky V and Jenneckens I (2001) Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics 158: 1203–1215.

Lundin LG (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16: 1–19.

Lundin LG (1999) Gene duplications in early metazoan evolution. Seminars in Cell and Developmental Biology 10: 523–530.

Lundin LG, Larhammar D and Hallböök F (2003) Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates. Journal of Structural and Functional Genomics 3: 53–63.

Lynch M and Conery JS (2003) The evolutionary demography of duplicate genes. Journal of Structural and Functional Genomics 3: 35–44.

Messing J, Bharti AK, Karlowski WM et al. (2004) Sequence composition and genome organization of maize. Proceedings of the National Academy of Sciences of the USA 101: 14349–14354.

Nadeau JH and Sankoff D (1997) Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics 147: 1259–1266.

Nakatani Y, Takeda H, Kohara Y and Morishita S (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Research 17: 1254–1265.

Ohno S (1970) Evolution by Gene Duplication. New York: Springer.

Olinski RP, Lundin L‐G and Hallböök F (2006) Conserved synteny between the Ciona genome and human paralogons identifies large duplication events in the molecular evolution of the insulin‐relaxin gene family. Molecular Biology and Evolution 23: 10–22.

Otto SP and Whitton J (2000) Polyploid incidence and evolution. Annual Review of Genetics 34: 401–437.

Pont C, Murat F, Confolent C, Balzergue S and Salse J (2011) RNA‐seq in grain unveils fate of neo‐ and paleopolyploidization events in bread wheat (Triticum aestivum L). Genome Biology 12: R119.

Popovici C, Leveugle M, Birnbaum D and Coulier F (2001) Coparalogy: physical and functional clusterings in the human genome. Biochemical and Biophysical Research Communications 288: 362–370.

Postlethwait JH, Yan YL, Gates M et al. (1998) Vertebrate genome evolution and the zebrafish gene map. Nature Genetics 18: 345–349.

Putnam NH, Butts T, Ferrier DE et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064–1071.

Shiina T, Dijkstra JM, Shimizu S et al. (2005) Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics 56: 878–893.

Shimeld SM and Holland PWH (2000) Vertebrate innovations. Proceedings of the National Academy of Sciences of the USA 97: 4449–4452.

Shu DG, Morris SC, Han J et al. (2003) Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature 421: 526–529.

Sundström G, Larsson TA and Larhammar D (2008) Phylogenetic and chromosomal analyses of multiple gene families syntenic with vertebrate Hox clusters. BMC Evolutionary Biology 8: 254.

Tordai H, Nagy A, Farkas K, Banyai L and Patthy L (2005) Modules, multidomain proteins and organismic complexity. FEBS Journal 272: 5064–5078.

Van de Peer Y, Fawcett JA, Proost S, Sterck L and Vandepoele K (2009) The flowering world: a tale of duplications. Trends in Plant Science 14: 680–688.

Venter JC, Adams MD, Myers EW et al. (2001) The sequence of the human genome. Science 291: 1304–1351.

Widmark J, Sundström G, Ocampo Daza D and Larhammar D (2011) Differential evolution of voltage‐gated sodium channels in tetrapods and teleost fishes. Molecular Biology and EvolutionVolume: 28: 859–871.

Wolfe KH (2001) Yesterday's polyploids and the mystery of diploidization. Nature Reviews Genetics 2: 333–341.

Zhong YF, Butts T and Holland PW (2008) HomeoDB: a database of homeobox gene diversity. Evolution and Development 10: 516–518.

Further Reading

Cañestro C (2012) Two rounds of whole‐genome duplication: evidence and impact on the evolution of vertebrate innovations. In: Soltis PS and Soltis DE (eds) Polyploidy and Genome Evolution, pp. 309–339. Berlin, Heidelberg: Springer‐Verlag.

Henkel CV, Burgerhout E, de Wijze DL et al. (2012) Primitive duplicate Hox clusters in the European eel's genome. PLoS One 7: e32231.

Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131: 452–462.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Lundin, Lars‐Gustav, Larhammar, Dan, and Hallböök, Finn(Mar 2013) Polyploidy and Paralogous Chromosome Regions. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0005072.pub3]