Multiple origins of green coloration in frogs mediated by a novel biliverdin-binding serpin

TABOADA, C.; BRUNETTI, A.E.; LYRA, M. L.; FITAK, R. R.; FAIGON SOVERNA, A.; RON, S.; LAGORIO, MARÍA G.; HADDAD, C.F.B.; LOPES, N. P.; JOHNSEN, S.; FAIVOVICH, J.; CHEMES, LUCÍA B.; BARI, SARA E.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

NATL ACAD SCIENCES

Lugar: Washington DC, USA; Año: 2020 vol. 117 p. 18574 - 18581

0027-8424

Many vertebrates have distinctive blue-green bones and othertissues due to unusually high biliverdin concentrations?a phenomenoncalled chlorosis. Despite its prevalence, the biochemicalbasis, biology, and evolution of chlorosis are poorly understood. Inthis study, we show that the occurrence of high biliverdin in anurans(frogs and toads) has evolved multiple times during theirevolutionary history, and relies on the same mechanism?the presenceof a class of serpin family proteins that bind biliverdin. Usinga diverse combination of techniques, we purified these serpinsfrom several species of nonmodel treefrogs and developed a pipelinethat allowed us to assemble their complete amino acid and nucleotidesequences. The described proteins, hereafter named biliverdinbindingserpins (BBS), have absorption spectra that mimic those ofphytochromes and bacteriophytochromes. Our models showed thatphysiological concentration of BBSs fine-tune the color of the animals,providing the physiological basis for crypsis in green foliage even undernear-infrared light. Additionally, we found that these BBSs aremost similar to human glycoprotein alpha-1-antitrypsin, but with aremarkable functional diversification. Our results present molecularand functional evidence of recurrent evolution of chlorosis, describea biliverdin-binding protein in vertebrates, and introduce a functionfor a member of the serpin superfamily, the largest and most ubiquitousgroup of protease inhibitors.