Distinct and redundant expression and transcriptional diversity of MEIS gene paralogs during chicken development

Abstract

Members of the Meis family of TALE homeobox transcription factors are involved in many processes of vertebrate development and morphogenesis, showing extremely complex transcriptional and spatiotemporal expression patterns. In this work, we performed a comprehensive study of chicken Meis genes using multiple approaches. First, we assessed whether the chicken genome contains a Meis3 ortholog or harbors only two Meis genes; we gathered several lines of evidence pointing to a specific loss of the Meis3 ortholog in an early ancestor of birds. Next, we studied the transcriptional diversity generated from chicken Meis genes through alternative splicing during development. Finally, we performed a detailed analysis of chick Meis1/ 2 expression patterns during early embryogenesis and organogenesis. We show that the expression of both Meis genes begins at the gastrulation stage in the three embryonic layers, presenting highly dynamic patterns with overlapping as well as distinct expression domains throughout development. Developmental Dynamics 240:1475-1492, 2011. V C 2011 Wiley-Liss, Inc.Key words: TALE family; alternative splicing; ectoderm; mesoderm; endoderm; central nervous system; sensory organs; visceral development; gut Accepted 17 January 2011 Developmental DynamicsABBREVIATIONS A atrium aip anterior intestinal portal as alternative splicing av allantoic vesicle ba branchial arches bd bile duct C conotruncus cl cloaca cnp caudal neural plate co coelom cp cardiac primordium D diencephalon da dorsal aorta dh dorsal horn dm dermomyotome dp dorsal pancreas du duodenum ect ectoderm ep ephiphysis end endoderm Eo-PmC extraocular pre-muscle cluster FB forebrain fg foregut fp floor plate Hn Hensen node HB hindbrain Hyp hypothalamus inf infundibulum isth isthmus l lens ltl larynx-trachea-lug bud lpm lateral plate mesoderm lp lens placode lv liver lb lung bud MB midbrain Mes mesencephalon mes mesoderm mg mid-gut mn mesonephric system mp mandibular process MRB mesencephalic-rhombencephalic boundary nep nephrotome nf neural fold np neural plate nr neural retina nt notochord oc otic cup oe oesophagus of optic furrow omv omphalomensenteric vena os optic stalk ot otocyst ov optic vesicle p prosomere p1 prosomere 1 p2 prosomere 2 p3 prosomere 3 pc pericardial cavity pe pigmented epithelium pf primitive fold pg primitive groove ph pharynx pm precardiac mesoderm POA preoptic area pp prechordal plate ps primitive streak psm primitive streak mesoderm PT pretectum Rh rhombencephalon rh rhombomere RhA1 rhombomere A1 rnp rostral neural plate Rp Rathke's pouch rp roof plate SC spinal cord scl sclerotome sm somatic mesoderm smp somatopleure som somite SP secondary prosencephalon sp segmental plate spm splanchnic mesoderm spp splanchnopleure st stomach sub.p subcephalic pocket sv sinus venosus tb tail bud td thyro-glossal duct Tel telencephalon TH thalamus Tv telencephalic vesicle V.n trigeminal ganglion V ventricle WGS whole genome shotgun zli zona limitans intrathalamica

Comparison of Pretectal Genoarchitectonic Pattern between Quail and Chicken Embryos

“…According to the genoarchitectonic data from Schlosser and Ahrens, (2004), the distinction between p1, p2, p3, and midbrain in Xenopus is established at stages 24–27, whereas Tcf712 ( Tcf4 ) is clearly expressed only in the diencephalon until at least stages 33–34 (Figure 1 in Morona et al, 2010). Meis2 expression in the alar mesencephalon, stopping rostrally at the DMB boundary, was described in chicken from stage HH9/10 onward (Ferran et al, 2007; Sánchez-Guardado et al, 2011). In the present study, we identified at Q27/HH28 some Meis2 -positive cells in the pe and su strata from the CoP, which progressively increased in number.…”

A Non-Mammalian Type Opsin 5 Functions Dually in the Photoreceptive and Non-Photoreceptive Organs of Birds

“…Two Meis family members have been identified in the chicken genome [16]. Although the antibody used in this study cannot discriminate between the two Meis proteins, Meis2 is known to be expressed by a subpopulation of γ-aminobutyric acid (GABA) ergic amacrine cells in vertebrate mature retina, including near-hatched chick retina [17].…”

Contrasting 5' and 3' Evolutionary Histories and Frequent Evolutionary Convergence in Meis/hth Gene Structures

“…However, we found four Meis genes in the lophotrochozoan H. robusta ; in addition, two paralogs have been described in two distantly related spiders (Prpic et al 2003; Pechmann and Prpic 2009), Cupiennius salei and Acanthoscurria geniculata , for which full genome sequences are not yet available. Among vertebrates, Meis complement ranged from two paralogs in birds (Sánchez-Guardado et al 2011) to five in zebrafish (dating to the extra round of WGD that occurred at the base of teleosts), with three genes in most tetrapods. Phylogenetic analysis using Bayesian inference strongly supports the orthology of all identified genes (supplementary fig.…”

“…Combining the different sources of data, most exon boundaries could be determined unambiguously (supplementary table S1). Introns and exons were named following the vertebrate nomenclature (exons 12 and 13 were named 12a and 12b [Sánchez-Guardado et al 2011] and insect-specific exons between ancestral exons 7 and 8 were not counted [supplementary fig. S1]).…”

“…1 A ), but the Meis1B isoform does not, leading to an alternative C-terminus, encoded by the downstream exon 12b, and to higher transcriptional activator capacities than both Meis1A - and the Meis -related pknox1 gene, especially in response to protein kinase A (PKA) and TrichostatinA (TSA) (Maeda et al 2001; Huang et al 2005). Alternative splicing (AS) of exons homologous to 12a, as well as other AS events, have been reported for the Meis2 and Meis3 genes in vertebrates (Oulad-Abdelghani et al 1997; Yang et al 2000; Williams et al 2005; Shim et al 2007; Hyman-Walsh et al 2010; Sánchez-Guardado et al 2011). …”