Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning - PubMed (original) (raw)

Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning

D Gauchat et al. Proc Natl Acad Sci U S A. 2000.

Abstract

The conservation of developmental functions exerted by Antp-class homeoproteins in protostomes and deuterostomes suggested that homologs with related functions are present in diploblastic animals. Our phylogenetic analyses showed that Antp-class homeodomains belong either to non-Hox or to Hox/paraHox families. Among the 13 non-Hox families, 9 have diploblastic homologs, Msx, Emx, Barx, Evx, Tlx, NK-2, and Prh/Hex, Not, and Dlx, reported here. Among the Hox/paraHox, poriferan sequences were not found, and the cnidarian sequences formed at least five distinct cnox families. Two are significantly related to the paraHox Gsx (cnox-2) and the mox (cnox-5) sequences, whereas three display some relatedness to the Hox paralog groups 1 (cnox-1), 9/10 (cnox-3) and the paraHox cdx (cnox-4). Intermediate Hox/paraHox genes (PG 3 to 8 and lox) did not have clear cnidarian counterparts. In Hydra, cnox-1, cnox-2, and cnox-3 were not found chromosomally linked within a 150-kb range and displayed specific expression patterns in the adult head. During regeneration, cnox-1 was expressed as an early gene whatever the polarity, whereas cnox-2 was up-regulated later during head but not foot regeneration. Finally, cnox-3 expression was reestablished in the adult head once it was fully formed. These results suggest that the Hydra genes related to anterior Hox/paraHox genes are involved at different stages of apical differentiation. However, the positional information defining the oral/aboral axis in Hydra cannot be correlated strictly to that characterizing the anterior-posterior axis in vertebrates or arthropods.

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Figures

Figure 1

Figure 1

Conserved residues at specific positions provide a common signature for all Antp-class HDs and thonon-Hox or the Hox/paraHox HDs (bold). In addition, a family-specific signature is given where identical or equivalent residues between diploblastic and bilaterian sequences are underlined.

Figure 2

Figure 2

Phylogenetic relationships between 200 Antp-class genes inferred by NJ analysis by using Dayhoff's PAM distance matrix. The tree was rooted with a Prd-class sequence. All branch lengths were drawn to scale. Numbers at nodes indicate percentages of 200 bootstrap replicates that support the branch; values under 50% are omitted, except for some significantly important nodes. Support values for each family defined on the right are marked in bold. Sequences from diploblasts are in shaded boxes.

Figure 3

Figure 3

Phylogenetic tree of 57 Hox/paraHox HD sequences inferred by ML analysis where 242,075 of the 677,040 possible quartets of sequences (35.8%) were unresolved, leading to a multifurcating tree with a Log likelihood value of −3,656.89. Numbers above the branches correspond to the quartet puzzling support values; numbers under branches indicate percentages of 1,000 bootstrap replicates for NJ analysis of the same dataset. Ten sequences from non-Hox families (NK2, Msx, Not, and Emx) were used as an outgroup. Shaded boxes as in Fig. 2.

Figure 4

Figure 4

PFGE analysis of Cv genomic DNA predigested with _Cla_I (2), NruI (3), MluI (4), NarI (5), _Pvu_I (6), _Sma_I (7), or undigested (1) and hybridized to cnox-1 Cv, cnox-2 Cv, cnox-3 Hv, and Bar-H1 Cv [initially named cnox-3 Cv (15)] probes.

Figure 5

Figure 5

Expression pattern of the Hv Hox/paraHox genes, cnox-1 (Top), cnox-2 (Middle), and cnox-3 (Bottom) in adult (Left) and regenerating Hydra. Time points after cutting are given; arrowheads and arrows indicate foot- and head-regenerating stumps, respectively. st, budding stage.

Figure 6

Figure 6

Scheme describing a plausible scenario of the evolution of Antp-class genes from diploblastic to bilaterian animals.

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