Genetic control over biogenic crystal morphogenesis in zebrafish

Rachael Deis; Tali Lerer-Goldshtein; Olha Baiko; Zohar Eyal; Dolev Brenman-Begin; Moshe Goldsmith; Sylvia Kaufmann; Uwe Heinig; Yonghui Dong; Sofya Lushchekina; Neta Varsano; Tsviya Olender; Meital Kupervaser; Ziv Porat; Smadar Levin-Zaidman; Iddo Pinkas; Rita Mateus; Dvir Gur

doi:10.1038/s41589-024-01722-1

Genetic control over biogenic crystal morphogenesis in zebrafish

Rachael Deis
, Tali Lerer-Goldshtein
, Olha Baiko
, Zohar Eyal
, Dolev Brenman-Begin
, Moshe Goldsmith
, Sylvia Kaufmann
, Uwe Heinig
, Yonghui Dong
, Sofya Lushchekina
, Neta Varsano
, Tsviya Olender
, Meital Kupervaser
, Ziv Porat
, Smadar Levin-Zaidman
, Iddo Pinkas
, Rita Mateus
, Dvir Gur^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

18 Citations (Scopus)

300 Downloads (Pure)

Abstract

Organisms evolve mechanisms that regulate the properties of biogenic crystals to support a wide range of functions, from vision and camouflage to communication and thermal regulation. Yet, the mechanism underlying the formation of diverse intracellular crystals remains enigmatic. Here we unravel the biochemical control over crystal morphogenesis in zebrafish iridophores. We show that the chemical composition of the crystals determines their shape, particularly through the ratio between the nucleobases guanine and hypoxanthine. We reveal that these variations in composition are genetically controlled through tissue-specific expression of specialized paralogs, which exhibit remarkable substrate selectivity. This orchestrated combination grants the organism with the capacity to generate a broad spectrum of crystal morphologies. Overall, our findings suggest a mechanism for the morphological and functional diversity of biogenic crystals and may, thus, inspire the development of genetically designed biomaterials and medical therapeutics. (Figure presented.)

Original language	English
Article number	6368
Pages (from-to)	383-392
Number of pages	10
Journal	Nature Chemical Biology
Volume	21
Issue number	3
Early online date	30 Aug 2024
DOIs	https://doi.org/10.1038/s41589-024-01722-1
Publication status	Published - Mar 2025

Funding

We thank A. Baram for his help with the HPLC measurements and method development. We thank L. Leiserowitz and L. Addadi for helpful discussions on this project. This research was cofunded by the European Union (ERC, CRYSTALCELL, 101077470). Views and opinions expressed are, however, ours and do not necessarily reflect those of the European Union or the European Research Council. Neither the European Union nor the granting authority can be held responsible for them. This research was also supported by a research grant from the Harmstieg New Scientist Fund, the Thomas A. and Georgina T. Russo New Scientist Fund, the Alisa and Peter Savitz Foundation, R. Cohen, M. Levine, A. Schatz, the Lancovici-Fallmann Memorial Fund, established by Ruth and Henry Yancovich, the Ullmann Family Foundation, Mr. and Mrs. Alan Franco, the Horwitz Research Fund and the Barton Award for Young Scientists. S.K. and R.M. acknowledge funding from the Max Planck Society and the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy (EXC-2068-390729961, Cluster of Excellence Physics of Life of TU Dresden). R.D. is a fellow of the Ariane de Rothschild Women Doctoral Program.

All Science Journal Classification (ASJC) codes

Molecular Biology
Cell Biology

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10.1038/s41589-024-01722-1

Cite this

Deis, R., Lerer-Goldshtein, T., Baiko, O., Eyal, Z., Brenman-Begin, D., Goldsmith, M., Kaufmann, S., Heinig, U., Dong, Y., Lushchekina, S., Varsano, N., Olender, T., Kupervaser, M., Porat, Z., Levin-Zaidman, S., Pinkas, I., Mateus, R., & Gur, D. (2025). Genetic control over biogenic crystal morphogenesis in zebrafish. Nature Chemical Biology, 21(3), 383-392. Article 6368. https://doi.org/10.1038/s41589-024-01722-1

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title = "Genetic control over biogenic crystal morphogenesis in zebrafish",

abstract = "Organisms evolve mechanisms that regulate the properties of biogenic crystals to support a wide range of functions, from vision and camouflage to communication and thermal regulation. Yet, the mechanism underlying the formation of diverse intracellular crystals remains enigmatic. Here we unravel the biochemical control over crystal morphogenesis in zebrafish iridophores. We show that the chemical composition of the crystals determines their shape, particularly through the ratio between the nucleobases guanine and hypoxanthine. We reveal that these variations in composition are genetically controlled through tissue-specific expression of specialized paralogs, which exhibit remarkable substrate selectivity. This orchestrated combination grants the organism with the capacity to generate a broad spectrum of crystal morphologies. Overall, our findings suggest a mechanism for the morphological and functional diversity of biogenic crystals and may, thus, inspire the development of genetically designed biomaterials and medical therapeutics. (Figure presented.)",

author = "Rachael Deis and Tali Lerer-Goldshtein and Olha Baiko and Zohar Eyal and Dolev Brenman-Begin and Moshe Goldsmith and Sylvia Kaufmann and Uwe Heinig and Yonghui Dong and Sofya Lushchekina and Neta Varsano and Tsviya Olender and Meital Kupervaser and Ziv Porat and Smadar Levin-Zaidman and Iddo Pinkas and Rita Mateus and Dvir Gur",

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Deis, R, Lerer-Goldshtein, T, Baiko, O, Eyal, Z , Brenman-Begin, D , Goldsmith, M, Kaufmann, S, Heinig, U, Dong, Y, Lushchekina, S , Varsano, N , Olender, T , Kupervaser, M , Porat, Z , Levin-Zaidman, S , Pinkas, I, Mateus, R & Gur, D 2025, 'Genetic control over biogenic crystal morphogenesis in zebrafish', Nature Chemical Biology, vol. 21, no. 3, 6368, pp. 383-392. https://doi.org/10.1038/s41589-024-01722-1

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AU - Deis, Rachael

AU - Lerer-Goldshtein, Tali

AU - Baiko, Olha

AU - Eyal, Zohar

AU - Brenman-Begin, Dolev

AU - Goldsmith, Moshe

AU - Kaufmann, Sylvia

AU - Heinig, Uwe

AU - Dong, Yonghui

AU - Lushchekina, Sofya

AU - Varsano, Neta

AU - Olender, Tsviya

AU - Kupervaser, Meital

AU - Porat, Ziv

AU - Levin-Zaidman, Smadar

AU - Pinkas, Iddo

AU - Mateus, Rita

AU - Gur, Dvir

PY - 2025/3

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N2 - Organisms evolve mechanisms that regulate the properties of biogenic crystals to support a wide range of functions, from vision and camouflage to communication and thermal regulation. Yet, the mechanism underlying the formation of diverse intracellular crystals remains enigmatic. Here we unravel the biochemical control over crystal morphogenesis in zebrafish iridophores. We show that the chemical composition of the crystals determines their shape, particularly through the ratio between the nucleobases guanine and hypoxanthine. We reveal that these variations in composition are genetically controlled through tissue-specific expression of specialized paralogs, which exhibit remarkable substrate selectivity. This orchestrated combination grants the organism with the capacity to generate a broad spectrum of crystal morphologies. Overall, our findings suggest a mechanism for the morphological and functional diversity of biogenic crystals and may, thus, inspire the development of genetically designed biomaterials and medical therapeutics. (Figure presented.)

AB - Organisms evolve mechanisms that regulate the properties of biogenic crystals to support a wide range of functions, from vision and camouflage to communication and thermal regulation. Yet, the mechanism underlying the formation of diverse intracellular crystals remains enigmatic. Here we unravel the biochemical control over crystal morphogenesis in zebrafish iridophores. We show that the chemical composition of the crystals determines their shape, particularly through the ratio between the nucleobases guanine and hypoxanthine. We reveal that these variations in composition are genetically controlled through tissue-specific expression of specialized paralogs, which exhibit remarkable substrate selectivity. This orchestrated combination grants the organism with the capacity to generate a broad spectrum of crystal morphologies. Overall, our findings suggest a mechanism for the morphological and functional diversity of biogenic crystals and may, thus, inspire the development of genetically designed biomaterials and medical therapeutics. (Figure presented.)

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Genetic control over biogenic crystal morphogenesis in zebrafish

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