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Ordered expression pattern of Hox and ParaHox genes along the alimentary canal in the ascidian juvenile

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Abstract

The Hox and ParaHox genes of bilateria share a similar expression pattern along the body axis and are known to be associated with anterior-posterior patterning. In vertebrates, the Hox genes are also expressed in presomitic mesoderm and gut endoderm and the ParaHox genes show a restricted expression pattern in the gut-related derivatives. Regional expression patterns in the embryonic central nervous system of the basal chordates amphioxus and ascidian have been reported; however, little is known about their endodermal expression in the alimentary canal. We focus on the Hox and ParaHox genes in the ascidian Ciona intestinalis and investigate the gene expression patterns in the juvenile, which shows morphological regionality in the alimentary canal. Gene expression analyses by using whole-mount in situ hybridization reveal that all Hox genes have a regional expression pattern along the alimentary canal. Expression of Hox1 to Hox4 is restricted to the posterior region of pharyngeal derivatives. Hox5 to Hox13 show an ordered expression pattern correlated with each Hox gene number along the postpharyngeal digestive tract. This expression pattern along the anterior-posterior axis has also been observed in Ciona ParaHox genes. Our observations suggest that ascidian Hox and ParaHox clusters are dispersed; however, the ordered expression patterns along the alimentary canal appear to be conserved among chordates.

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Acknowledgments

We thank Professors Nori Satoh and Kazuko Hirayama for providing the Ciona cDNA clones and juvenile specimens. We also thank Takatsugu Takiguchi and Takuya Nomura for their help in the in situ hybridizations of the Ciona juveniles and larvae.

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Authors and Affiliations

  1. The Graduate School of Advanced Integration Science, Chiba University, Yayoi-cho 1-33, Inage-ku, Chiba, 263-8522, Japan

    Satoshi Nakayama, Kunihiro Satou, Wataru Orito & Michio Ogasawara

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  1. Satoshi Nakayama
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  2. Kunihiro Satou
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  3. Wataru Orito
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  4. Michio Ogasawara
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Correspondence to Michio Ogasawara.

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Supplementary Fig. 1

Expression of larval CNS-positive Hox genes in the neural complex of the Ciona juvenile. a Expression of Hox1 is observed in the middle to posterior part of the cerebral ganglion. b Expression of Hox3 is also observed in the middle to posterior part of the cerebral ganglion, extending posterior to the neuron. c–e Strict expression patterns of Hox5 (c), Hox10 (d) and Hox12 (e) are not observed in the juvenile neural complex (cf ciliated funnel, cg cerebral ganglion, ng neural gland). Bar 20 μm. (GIF 210 kb)

High resolution image (TIF 11275 kb)

Supplementary Fig. 2

Expression of larval CNS-positive Hox genes in the trunk region of Ciona larvae. The expression of Hox1 is observed in the visceral ganglion, anterior nerve cord and posterior pharyngeal endoderm (a, c). Expression of Hox3 is mainly observed in the visceral ganglion; however strict expression is observed in the posterior pharyngeal endoderm (b, d). The dashed line indicates the edge of the posterior pharyngeal endoderm. The dotted line indicates the region of the prospective stomach (n notochord, nc nerve cord, pe pharyngeal endoderm, ps prospective stomach, vg visceral ganglion). Bar 50 μm (a, b), 20 μm (c, d). (GIF 190 kb)

High resolution image (TIF 11457 kb)

Supplementary Fig. 3

Schematic drawing of Hox gene expression in Fig. 1. Expression domains are indicated in blue. Expression level is indicated by color intensity (abbreviations as in Fig. 1). (GIF 112 kb)

High resolution image (TIF 5907 kb)

Supplementary Fig. 4

Schematic drawing of Hox gene expression in Fig. 3. Expression domains are indicated by colors: brown endostyle, purple esophagus, blue retropharyngeal band, green right epicardium, orange left of left epicardium, red right of left epicardium (abbreviations as in Fig. 1). (GIF 116 kb)

High resolution image (TIF 5036 kb)

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Nakayama, S., Satou, K., Orito, W. et al. Ordered expression pattern of Hox and ParaHox genes along the alimentary canal in the ascidian juvenile. Cell Tissue Res 365, 65–75 (2016). https://doi.org/10.1007/s00441-016-2360-7

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