Adachi, Y.; Nagai, H.; Fujichika, T.; Takahashi, A.; Miura, M.; Nakajima, Y.

Diapause is a survival strategy in which growth and aging are temporarily suspended, enabling animals to withstand unfavorable environments. Various insects, including the fruit fly Drosophila, enter reproductive diapause, or dormancy, in response to cold temperatures and/or short-day lengths. During reproductive diapause, ovarian development halts, and non-reproductive organs also undergo remodeling at both morphological and metabolic levels: however, the mechanisms underlying this remodeling and its physiological impact remain largely unclear. Here, we show that the Drosophila adult midgut undergoes extensive remodeling in diapause, marked by a sustained growth arrest due to the cell cycle arrest of intestinal stem cells (ISCs), reverting to normal upon returning to recovery conditions. During dormancy, BubR1 and Mad2, key regulators of mitosis, are highly expressed and localized in the cytoplasm of ISCs rather than at the kinetochore, and both BubR1 and Mad2 are essential for diapause-specific midgut remodeling. Furthermore, disruption of midgut growth arrest during diapause reduces the resistance to starvation in adult flies. Therefore, our findings identify a novel role for BubR1 and Mad2 in ISCs, promoting proper midgut remodeling during dormancy, and highlight the importance of this process for survival under adverse environments.