Autophagy triggered by iron-mediated ER stress is an important stress response to the early phase of Pi starvation in plants

Plant J. 2022 Jun;110(5):1370-1381. doi: 10.1111/tpj.15743. Epub 2022 Apr 6.

Abstract

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.

Keywords: ER-phagy; early Pi starvation; lipid-ROS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autophagy / physiology
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum Stress* / physiology
  • Iron* / metabolism
  • Membrane Lipids / metabolism

Substances

  • Membrane Lipids
  • Iron