Department of Life Sciences, School of Agriculture, Meiji University, 1-1-1, Tama-ku, Kawasaki-shi, Kanagawa, 214-8571, Japan.
Life Science Program, Graduate School of Agriculture, Meiji University, 1-1-1, Tama-ku, Kawasaki-shi, Kanagawa, 214-8571, Japan.
Plant J. 2022 Jun;110(5):1370-1381. doi: 10.1111/tpj.15743. Epub 2022 Apr 6.
Inorganic phosphate (Pi) is essential for plant growth. However, Pi is often limiting in soil. Hence, plants have established several mechanisms of response to Pi starvation. One of the important mechanisms is Pi recycling, which includes membrane lipid remodeling and plastid DNA degradation via catabolic enzymes. However, the involvement of other degradation systems in Pi recycling remains unclear. Autophagy, a system for degradation of intracellular components, contributes to recycling of some nutrients, such as nitrogen, carbon, and zinc, under starvation. In the present study, we found that autophagy-deficient mutants depleted Pi early and exhibited severe leaf growth defects under Pi starvation. The main cargo of autophagy induced by early Pi depleted conditions was the endoplasmic reticulum (ER), indicating that ER-phagy, a type of autophagy that selectively degrades the ER, is involved in the response to the early phase of Pi starvation for contribution to Pi recycling. This ER-phagy was suppressed in an INOSITOL-REQUIRING ENZYME 1 double mutant, ire1a ire1b, in which ER stress responses are defective, suggesting that the early Pi starvation induced ER-phagy is induced by ER stress. Furthermore, iron limitation and inhibition of lipid-reactive oxygen species accumulation suppressed the ER-phagy. Interestingly, membrane lipid remodeling, a response to late Pi starvation, was accelerated in the ire1a ire1b under early Pi-depleted conditions. Our findings reveal the existence of two different phases of responses to Pi starvation (i.e. early and late) and indicate that ER stress-mediated ER-phagy is involved in Pi recycling in the early phase to suppress acceleration of the late phase.
无机磷酸盐（Pi）是植物生长所必需的。然而，Pi 在土壤中常常是有限的。因此，植物已经建立了几种应对 Pi 饥饿的机制。其中一个重要的机制是 Pi 再循环，它包括通过分解代谢酶进行膜脂重塑和质体 DNA 降解。然而，其他降解系统在 Pi 再循环中的参与仍不清楚。自噬是一种降解细胞内成分的系统，有助于在饥饿状态下回收一些营养物质，如氮、碳和锌。在本研究中，我们发现自噬缺陷突变体在 Pi 饥饿早期就耗尽了 Pi，并且表现出严重的叶片生长缺陷。自噬诱导的主要货物是内质网（ER），表明 ER 自噬，一种选择性降解 ER 的自噬类型，参与了对 Pi 饥饿早期阶段的反应，有助于 Pi 再循环。这种 ER 自噬在 INOSITOL-REQUIRING ENZYME 1 双突变体 ire1a ire1b 中受到抑制，ire1a ire1b 中 ER 应激反应有缺陷，表明早期 Pi 饥饿诱导的 ER 自噬是由 ER 应激引起的。此外，铁限制和抑制脂质活性氧积累抑制了 ER 自噬。有趣的是，在早期 Pi 耗尽条件下，晚期 Pi 饥饿的膜脂重塑反应加速。我们的研究结果揭示了对 Pi 饥饿的两种不同反应阶段（即早期和晚期）的存在，并表明 ER 应激介导的 ER 自噬参与了早期阶段的 Pi 再循环，以抑制晚期阶段的加速。
