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. 2023 Aug;245(1):1-8.
doi: 10.1086/730536. Epub 2024 May 15.

Cymric, a Maternal and Zygotic HTK-16-Like SHARK Family Tyrosine Kinase Gene, Is Disrupted in Molgula occulta, a Tailless Ascidian

Kazuhiro W Makabe, Hannah I Jensen, Alexander C A Fodor, Jennifer Hsu, William R Jeffery, Noriyuki Satoh, Billie J Swalla

Cymric, a Maternal and Zygotic HTK-16-Like SHARK Family Tyrosine Kinase Gene, Is Disrupted in Molgula occulta, a Tailless Ascidian

Kazuhiro W Makabe et al. Biol Bull. 2023 Aug.

Abstract

AbstractWe describe the cloning and expression of a nonreceptor tyrosine kinase, cymric (Uro-1), a HTK-16-like (HydraTyrosineKinase-16) gene, identified in a subtractive screen for maternal ascidian cDNAs in Molgula oculata, an ascidian species with a tadpole larva. The cymric gene encodes a 4-kb mRNA expressed in gonads, eggs, and embryos in the tailed M. oculata but is not detected in eggs or embryos of the closely related tailless species Molgula occulta. There is a large insertion in cymric in the M. occulta genome, as shown by transcriptome and genome analyses, resulting in it becoming a pseudogene. The cymric amino acid sequence encodes a nonreceptor tyrosine kinase with an N-terminal region containing two SH2 domains and five ankyrin repeats, similar to the HTK-16-like gene found in other ascidians. Thus, the ascidian cymric genes are members of the SHARK (Src-homology ankyrin-repeat containing tyrosine kinase) family of nonreceptor tyrosine kinases, which are found throughout invertebrates and missing from vertebrates. We show that cymric is lacking the tyrosine kinase domain in the tailless M. occulta, although the truncated mRNA is still expressed in transcriptome data. This maternal and zygotic HTK-16-like tyrosine kinase is another described pseudogene from M. occulta and appears not to be necessary for adult development.

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Figures

Figure 1.
Figure 1.
Photographs of A. Molgula oculata and B. Molgula occulta larvae. M. oculata is a tailed ascidian larva with arrows pointing to notochord and muscle cells in the tail, and a pigmented sensory organ (the otolith) in the head. In contrast, M. occulta is tailless, lacking a sensory otolith, notochord, and muscle cells (Swalla and Jeffery 1990; Berrill, 1931).
Figure 2.
Figure 2.
A. A schematic diagram of the putative M. oculata cymric protein. The amino and carboxy termini are labeled, the locations of SH2 domains are in pink, ankyrin repeats are in blue, and the tyrosine kinase catalytic domain is in green. Below the protein diagram are the corresponding exons from M. oculata in blue and M. occulta in red that encode the cymric protein. Shown below is the position of cDNA clone (probe A) used for identifying the cymric amino acid sequence and as probes for in situ hybridizations. B. Intron and exon organization of M. oculata and M. occulta SHARK tyrosine kinase transcripts compared to the M. oculata and M. occulta genomes. The M. occulta genome is missing the last 5 exons transcribed from the M. oculata genome (exons 10–14) and has an extra exon at the 5’ end of the transcript (not shown). The M. occulta cymric transcript is truncated missing the tyrosine kinase domain.
Figure 3.
Figure 3.
Alignment of SHARK tyrosine kinases including ascidian (M. oculata, M. occulta, M. occidentalis, and C. intestinalis (XP_002121112.2)) cymric, H. vulgaris HTK16 (NP_00129668.1) (Chan et al., 1994), A. queenslandica (sponge) SHARK (BAA81720) (Suga et al. 1999), D. melanogaster SHARK (NP_524743.2) (Ferrante et al., 1995), S. purpuratus SHARK (XP_001180232.2), and A. californica SHARK (XP_005102068.1) tyrosine kinases. The amino acid positions are numbered at the beginning and end of each row. The gaps in the alignment are indicated by dashes. The SH2 domains are in pink, the ankyrin repeats are blue, and the tyrosine kinase domain is green. There is very high sequence similarity across metazoans, suggesting that cymric was present in the metazoan common ancestor and has been very conserved.
Figure 4.
Figure 4.
Distribution of cymric transcripts throughout the tailed Molgula oculata development as determined by in situ hybridization. A. Oocyte at first ooplasmic segregation with animal pole up and vegetal pole down, the cymric transcript is expressed in the vegetal pole. B. 8-cell with animal pole up and vegetal pole down. Cymric expression accumulates in the blastomeres on the vegetal and posterior poles. C. 16-cell embryo in a vegetal view. Cymric transcripts are sequestered into the 4 tail muscle cells at the posterior of the embryo. D. A vegetal view of a gastrula showing cymric accumulation in all the larval tail muscle cells. E. Neurula with the animal pole up, the vegetal pole down, the anterior left and posterior right; cymric transcripts still remain expressed in the tail muscle cells. G. Tailbud stage with animal pole up, vegetal down, anterior left, and posterior right. Cymric expression is no longer detectable in the larva.
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