The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra

Abstract

Cell lineages of cnidarians including Hydra represent the fundamental cell types of metazoans and provides us a unique opportunity to study the evolutionary diversification of cell type in the animal kingdom. Hydra contains epithelial cells as well as a multipotent interstitial cell (I-cell) that gives rise to nematocytes, nerve cells, gland cells, and germ-line cells. We used cDNA microarrays to identify cell type-specific genes by comparing gene expression in normal Hydra with animals lacking the I-cell lineage, so-called epithelial Hydra. We then performed in situ hybridization to localize expression to specific cell types. Eighty-six genes were shown to be expressed in specific cell types of the I-cell lineage. An additional 29 genes were expressed in epithelial cells and were down-regulated in epithelial animals lacking I-cells. Based on the above information, we constructed a database (http://hydra.lab.nig.ac.jp/hydra/), which describes the expression patterns of cell type-specific genes in Hydra. Most genes expressed specifically in either I-cells or epithelial cells have homologues in higher metazoans. By comparison, most nematocyte-specific genes and approximately half of the gland cell- and nerve cell-specific genes are unique to the cnidarian lineage. Because nematocytes, gland cells, and nerve cells appeared along with the emergence of cnidarians, this suggests that lineage-specific genes arose in cnidarians in conjunction with the evolution of new cell types required by the cnidarians.

Fig. 1.

Expression of nematocyte-specific genes using whole-mount in situ hybridization. Whole animals are shown on the left, and high-magnification images showing the expression signal in individual cells are shown on the right. (A) hmp_11623, a previously uncharacterized minicollagen expressed in differentiating nematocytes. (B) hm_02181, a protein disulfide isomerase expressed in differentiating nematocytes. (C) hm_04121, a toxin protein expressed in differentiating isorhizas. (D) hmp_21268, a toxin protein expressed in differentiating nematocytes. (E) hmp_17528, a cnidarian-specific capsule protein expressed in mature holotrichous isorhizas. (F) hmp_08523, a lamin-like protein expressed in all mature nematocytes. (G) hmp_08051, a calcium-binding protein expressed in migrating nematocytes. (H) hmp_07578, a cnidarian-specific protein with unknown function expressed only in stenoteles and desmonemes. All clone names refer to Table 1. S, stenotele; HI, holotrichous isorhiza; I, isorhiza; D, desmoneme; dS, differentiating stenotele; dI, differentiating isorhiza; dD, differentiating desmoneme. (Scale bars, 50 μm.)

Fig. 2.

Expression of gland cell-specific genes using whole-mount in situ hybridization. Whole animals are shown on the left, and high-magnification images showing the expression signal in individual cells are shown on the right. (A) hmp_14705. (B) hm_02146. All clone names refer to Table 2. (Scale bars, 50 μm.)