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Late Somatic Gene 2 disrupts parental spheroids cooperatively with Volvox hatching enzyme A in Volvox

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Abstract

Main conclusion

We identified LSG2 as a novel lytic enzyme that accumulates in the parental extracellular matrix and disrupts parental spheroids cooperatively with VheA secreted by juveniles in Volvox.

Spatiotemporally restricted degradation of extracellular matrix (ECM) is essential for development and survival in multicellular organisms. In an asexual life cycle of green algae Volvox, juveniles are released from parental spheroids through holes made by restricted degradation of parental ECM at the proper timing. Lytic enzyme(s) should specifically degrade parental ECM upon Volvox hatching, but little is known about the mechanisms of spatiotemporally restricted parental degradation. Here, we identified a glycoprotein encoded by the Late Somatic Gene 2 (LSG2) as a novel lytic enzyme that accumulates in parental ECM during the prehatching stages. The dual action of LSG2 and Volvox hatching enzyme A (VheA), a serine protease secreted by juveniles, causes the degradation of ECM sheets at all stages and destroys even daughter spheroids, while VheA alone disrupts spheroids only in the prehatching stage when LSG2 is accumulated, suggesting that the combination of LSG2 and VheA is sufficient to cause the degradation of ECM sheet. In the prehatching stage, parental spheroids became susceptible to the proteolysis by a mixture of bacterial proteases applied externally, which could be facilitated by LSG2. These results suggest that LSG2 disrupts parental ECM cooperatively with VheA by modifying the parental ECM to make it fragile, and that the appropriate activity of these enzymes is crucial for the parent-specific ECM degradation at the proper timing.

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Abbreviations

ECM:

Extracellular matrix

LSG2:

Late somatic gene 2

MMP:

Matrix metalloproteinase

SVM:

Standard Volvox medium

VheA:

Volvox hatching enzyme A

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Acknowledgments

We thank all the members of the Section of Biology, College of Liberal Arts and Sciences, Kitasato University, for helpful discussions and valuable technical support; Ms. Etsuko Nagata, Department of Biochemistry, Kitasato University School of Medicine, for mass spectrometric analysis; Drs. Hiroko Toyooka and Hisayoshi Nozaki, Department of Biological Science, The University of Tokyo, and Dr. Hideaki Shiraishi, Graduate School of Biostudies, Kyoto University, for providing the Volvox strains; Robert E. Brandt, Founder, CEO, and CME, of MedEd Japan, for editing the manuscript. This research was supported by the Section of Biology, College of Liberal Arts and Sciences, Kitasato University, Kitasato University Research Grant for Young Researchers, and the Sasakawa Scientific Research Grant from The Japan Science Society.

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Correspondence to Mayuko Nishimura.

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Nishimura, M., Nagashio, R., Sato, Y. et al. Late Somatic Gene 2 disrupts parental spheroids cooperatively with Volvox hatching enzyme A in Volvox . Planta 245, 183–192 (2017). https://doi.org/10.1007/s00425-016-2599-y

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