A dynamic ubiquitination balance of cell proliferation and endoreduplication regulators determines plant organ size.

Ying Chen, Mattias Vermeersch, Jelle Van Leene, Geert De Jaeger, Yunhai Li, Hannes Vanhaeren

Science advances 2024 Mar 15

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Ubiquitination plays a crucial role throughout plant growth and development. The E3 ligase DA2 has been reported to activate the peptidase DA1 by ubiquitination, hereby limiting cell proliferation. However, the molecular mechanisms that regulate DA2 remain elusive. Here, we demonstrate that DA2 has a very high turnover and auto-ubiquitinates with K48-linkage polyubiquitin chains, which is counteracted by two deubiquitinating enzymes, UBIQUITIN-SPECIFIC PROTEASE 12 (UBP12) and UBP13. Unexpectedly, we found that auto-ubiquitination of DA2 does not influence its stability but determines its E3 ligase activity. We also demonstrate that impairing the protease activity of DA1 abolishes the growth-reducing effect of DA2. Last, we show that synthetic, constitutively activated DA1-ubiquitin fusion proteins overrule this complex balance of ubiquitination and deubiquitination and strongly restrict growth and promote endoreduplication. Our findings highlight a nonproteolytic function of K48-linked polyubiquitination and reveal a mechanism by which DA2 auto-ubiquitination levels, in concert with UBP12 and UBP13, precisely monitor the activity of DA1 and fine-tune plant organ size.

Citation

Ying Chen, Mattias Vermeersch, Jelle Van Leene, Geert De Jaeger, Yunhai Li, Hannes Vanhaeren. A dynamic ubiquitination balance of cell proliferation and endoreduplication regulators determines plant organ size. Science advances. 2024 Mar 15;10(11):eadj2570