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Striving for normality: whole body regeneration through a series of abnormal generations

Ayelet Voskoboynik^*,1, Noa Simon-Blecher^,, Yoav Soen, Baruch Rinkevich, Anthony W. De Tomaso^*, Katherine J. Ishizuka^* and Irving L. Weissman^*

^* Department of Pathology, Stanford University School of Medicine, Stanford, California, USA; Department of Biology, Hopkins Marine Station, Pacific Grove, California, USA;

National Institute of Oceanography, Oceanographic and Limnological Research, Tel-Shikmona, Haifa, Israel;

Faculty of Life Science, Bar Ilan University, Ramat Gan, Israel; and

Department of Biochemistry, Stanford University School of Medicine, Stanford, California, USA

¹Correspondence: Department of Pathology, Stanford University School of Medicine, Stanford, CA 94305, USA. E-mail: ayeletv{at}stanford.edu

Embryogenesis and asexual reproduction are commonly considered to be coordinated developmental processes, which depend on accurate progression through a defined sequence of developmental stages. Here we report a peculiar developmental scenario in a simple chordate, Botryllus schlosseri, wherein a normal colony of individuals (zooids and buds) is regenerated from the vasculature (vascular budding) through a sequence of morphologically abnormal developmental stages. Vascular budding was induced by surgically removing buds and zooids from B. schlosseri colonies, leaving only the vasculature and the tunic that connects them. In vivo imaging and histological sections showed that the timing and morphology of developing structures during vascular budding deviated significantly from other asexual reproduction modes (the regular asexual reproduction mode in this organism and vascular budding in other botryllid species). Subsequent asexual reproduction cycles exhibited gradual regaining of normal developmental patterns, eventually leading to regeneration of a normal colony. The conversion into a normal body form suggests the activation of an alternative pathway of asexual reproduction, which involves gradual regaining of normal positional information. It presents a powerful model for studying the specification of the same body plan by different developmental programs.—Voskoboynik, A., Simon-Blecher, N., Soen, Y., Rinkevich, B., De Tomaso, A. W., Ishizuka, K. J., Weissman, I. L. Striving for normality: whole body regeneration through a series of abnormal generations.

Key Words: vascular budding • blastogenesis • development • tunicate