Abstract
Homeobox genes are compared between genomes in an attempt to understand the evolution of animal development. The ability of the protist, Dictyostelium discoideum, to shift between uni- and multicellularity makes this group ideal for studying the genetic changes that may have occurred during this transition. We present here the first genome-wide classification and comparative genomic analysis of the 14 homeobox genes present in D. discoideum. Based on the structural alignment of the homeodomains, they can be broadly divided into TALE and non-TALE classes. When individual homeobox genes were compared with members of known class or family, we could further classify them into 3 groups, namely, TALE, OTHER and NOVEL classes, but no HOX family was found. The 5 members of TALE class could be further divided into PBX, PKNOX, IRX and CUP families; 4 homeobox genes classified as NOVEL did not show any similarity to any known homeobox genes; while the remaining 5 were classified as OTHERS as they did show certain degree of similarity to few known homeobox genes. No unique RNA expression pattern during development of D. discoideum emerged for members of an individual group. Putative promoter analysis revealed binding sites for few homeobox transcription factors among many probable factors.
Similar content being viewed by others
References
Bailey TL and Elkan C 1994 Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2 28–36
Bailey TL and Gribskov M 1998 Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14 48–54
Baldauf SL and Palmer JD 1993 Animals and fungi are each other’s closest relatives: congruent evidence from multiple proteins. Proc. Natl. Acad. Sci. USA 90 11558–11562
Bapteste E, Brinkmann H, Lee JA, Moore DV, Sensen CW, Gordon P, Duruflé L, Gaasterland T, et al. 2002 The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba and Mastigamoeba. Proc. Natl. Acad. Sci. USA 99 1414–1419
Bertolino E, Reimund B, Wildt-Perinic D and Clerc RG 1995 A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif. J. Biol. Chem. 270 31178–31188
Booth HAF and Holland PWH 2007 Annotation nomenclature and evolution of four novel homeobox genes expressed in the human germ line. Gene 387 7–14
Bürglin TR 1997 Analysis of TALE superclass homeobox genes (MEIS PBC KNOX Iroquois TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res. 25 4173–4180
Bürglin TR 1998 The PBC domain contains a MEINOX domain: coevolution of Hox and TALE homeobox genes? Dev. Genes Evol. 208 113–116
Bürglin TR 2003 The homeobox genes of Encephalitozoon cuniculi (Microsporidia) reveal a putative mating-type locus. Dev. Genes Evol. 213 50–52
Chisholm RL, Gaudet P, Just EM, Pilcher KE, Fey P, Merchant SN and Kibbe WA 2006 dictyBase the model organism database for Dictyostelium discoideum. Nucleic Acids Res. 34 D423–D427
Coates JC, Grimson MJ, Williams RSB, Bergman W, Blanton RL and Harwood AJ 2002 Loss of the beta-catenin homologue aardvark causes ectopic stalk formation in Dictyostelium. Mech. Dev. 116 117–127
Cole C, Barber JD and Barton GJ 2008 The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36 W197–W201
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, et al. 2008 Phylogeny fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36 W465–W469
Derelle R, Lopez P, Le Guyader H and Manuel M 2007 Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol. Dev. 9 212–219
Fonseca NA, Vieira CP, Holland PWH and Vieira J 2008 Protein evolution of ANTP and PRD homeobox genes. BMC Evol. Biol. 8 200
Galardi-Castilla M, Fernandez-Aguado I, Suarez T and Sastre L 2013 Mef2A a homologue of animal Mef2 transcription factors regulates cell differentiation in Dictyostelium discoideum. BMC Dev. Biol. 13 12
Gallo GJ, Prentice H and Kingston RE 1993 Heat shock factor is required for growth at normal temperatures in the fission yeast Schizosaccharomyces pombe. Mol. Cell. Biol. 13 749–761
Garcia-Fernàndez J 2005 The genesis and evolution of homeobox gene clusters. Nat. Rev. Genet. 6 881–892
Gehring WJ 1994 A history of the homeobox; in Guidebook to the homeobox genes (ed) D Duboule (New York: Oxford Univ Press)
Gervasi F, D’Agnano I, Vossio S, Zupi G, Sacchi A and Lombardi D 1996 nm23 influences proliferation and differentiation of PC12 cells in response to nerve growth factor. Cell Growth Differ. 7 1689–1695
Gosain A, Lohia R, Shrivastava A and Saran S 2012 Identification and characterization of peptide: N-glycanase from Dictyostelium discoideum. BMC Biochem. 13 9
Grimson MJ, Coates JC, Reynolds JP, Shipman M, Blanton RL and Harwood AJ 2000 Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism. Nature 408 727–731
Guindon S and Gascuel O 2003 A simple fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 696–704
Guindon S, Lethiec F, Duroux P and Gascuel O 2005 PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33 W557–W559
Han Z and Firtel RA 1998 The homeobox-containing gene Wariai regulates anterior-posterior patterning and cell-type homeostasis in Dictyostelium. Development 125 313–325
Harrison SC and Aggarwal AK 1990 DNA recognition by proteins with the helix-turn-helix motif. Annu. Rev. Biochem. 59 933–969
Harwood AJ, Plyte SE, Woodgett J, Strutt H and Kay RR 1995 Glycogen synthase kinase 3 regulates cell fate in Dictyostelium. Cell 80 139–148
Holland PWH, Booth HAF and Bruford EA 2007 Classification and nomenclature of all human homeobox genes. BMC Biol. 5 47
Hsu S, Huang F, Wang L, Banerjee S, Winawer S and Friedman E 1994 The role of nm23 in transforming growth factor beta 1-mediated adherence and growth arrest. Cell Growth Differ. 5 909–917
Iyer LM, Anantharaman V, Wolf MY and Aravind L 2008 Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int. J. Parasitol. 38 1–31
Kawakami K, Sato S, Ozaki H and Ikeda K 2000 Six family genes–structure and function as transcription factors and their roles in development. Bioessays 22 616–626
Kelley LA and Sternberg MJE 2009 Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4 363–371
Kim JS, Seo JH, Yim HS and Kang SO 2011 Homeoprotein Hbx4 represses the expression of the adhesion molecule DdCAD-1 governing cytokinesis and development. FEBS Lett. 585 1864–1872
Kissinger CR, Liu BS, Martin-Blanco E, Kornberg TB and Pabo CO 1990 Crystal structure of an engrailed homeodomain-DNA complex at 2 8 A resolution: a framework for understanding homeodomain-DNA interactions. Cell 63 579–590
Kuma K, Nikoh N, Iwabe N and Miyata T 1995 Phylogenetic position of Dictyostelium inferred from multiple protein data sets. J. Mol. Evol. 41 238–246
Letunic I, Doerks T and Bork P 2011 SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40 D302–D305
Mukherjee K, Brocchieri L and Bürglin TR 2009 A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol. Biol. Evol. 26 2775–2794
Philippe H, Germot A and Moreira D 2000 The new phylogeny of eukaryotes. Curr. Opin. Genet. Dev. 10 596–601
Postel EH, Berberich SJ, Flint SJ and Ferrone CA 1993 Human c-myc transcription factor PuF identified as nm23-H2 nucleoside diphosphate kinase, a candidate suppressor of tumor metastasis. Science 261 478–480
Rot G, Parikh A, Curk T, Kuspa A, Shaulsky G and Zupan B 2009 dictyExpress: a Dictyostelium discoideum gene expression database with an explorative data analysis web-based interface. BMC Bioinformatics 10 265
Roy SW, Fedorov A and Gilbert W 2003 Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc. Natl. Acad. Sci. USA 100 7158–7162
Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC and Finnerty JR 2006 The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone Nematostella vectensis. Genome Biol. 7 R64
Sillo A, Bloomfield G, Balest A, Balbo A, Pergolizzi B, Peracino B, Skelton J, Ivens A, et al. 2008 Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9 291
Steenkamp ET, Wright J and Baldauf SL 2006 The protistan origins of animals and fungi. Mol. Biol. Evol. 23 93–106
Takatori N, Butts T, Candiani S, Pestarino M, Ferrier DEK, Saiga H and Holland PWH 2008 Comprehensive survey and classification of homeobox genes in the genome of amphioxus Branchiostoma floridae. Dev. Genes Evol. 218 579–590
Tamura K, Stecher G, Peterson D, Filipski A and Kumar S 2013 MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30 2725–2729
Wingender E, Dietze P, Karas H and Knüppel R 1996 TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res. 24 238–241
Zhong Y and Holland PWH 2011 The dynamics of vertebrate homeobox gene evolution: gain and loss of genes in mouse and human lineages. BMC Evol. Biol. 11 169
Acknowledgements
SS acknowledges the DST PURSE grant to her, and HM acknowledges UGC for fellowship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: Durgadas P Kasbekar
[Mishra H and Saran S 2015 Classification and expression analyses of homeobox genes from Dictyostelium discoideum. J. Biosci. 40 1–15] DOI 10.1007/s12038-015-9519-3
Supplementary materials pertaining to this article are available on the Journal of Biosciences Website at http://www.ias.ac.in/jbiosci/jun2015/supp/Mishra.pdf
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 1.90 MB)
Rights and permissions
About this article
Cite this article
Mishra, H., Saran, S. Classification and expression analyses of homeobox genes from Dictyostelium discoideum . J Biosci 40, 241–255 (2015). https://doi.org/10.1007/s12038-015-9519-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-015-9519-3