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Title: The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy

Abstract

Inorganic phosphate (Pi) is often a limiting plant nutrient. In members of the Brassicaceae family, such as Arabidopsis (Arabidopsis thaliana), Pi deprivation reshapes root system architecture to favor topsoil foraging. It does so by inhibiting primary root extension and stimulating lateral root formation. Root growth inhibition from phosphate (Pi) deficiency is triggered by iron-stimulated, apoplastic reactive oxygen species generation and cell wall modifications, which impair cell-to-cell communication and meristem maintenance. These processes require LOW PHOSPHATE RESPONSE1 (LPR1), a cell wall-targeted ferroxidase, and PHOSPHATE DEFICIENCY RESPONSE2 (PDR2), the single endoplasmic reticulum (ER)-resident P5-type ATPase (AtP5A), which is thought to control LPR1 secretion or activity. Autophagy is a conserved process involving the vacuolar degradation of cellular components. While the function of autophagy is well established under nutrient starvation (C, N, or S), it remains to be explored under Pi deprivation. Because AtP5A/PDR2 likely functions in the ER stress response, we analyzed the effect of Pi limitation on autophagy. Our comparative study of mutants defective in the local Pi deficiency response, ER stress response, and autophagy demonstrated that ER stress-dependent autophagy is rapidly activated as part of the developmental root response to Pi limitation and requires the genetic PDR2-LPR1 module. We conclude thatmore » Pi-dependent activation of autophagy in the root apex is a consequence of local Pi sensing and the associated ER stress response, rather than a means for systemic recycling of the macronutrient.« less

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [2];  [1]; ORCiD logo [1]; ORCiD logo [3]
  1. Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany
  2. Biocenter, Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany
  3. Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany, Institute of Biochemistry and Biotechnology, Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany, Department of Plant Sciences, University of California, Davis, California 95616
Publication Date:
Research Org.:
Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1484329
Alternate Identifier(s):
OSTI ID: 1609429
Grant/Contract Number:  
DE–FG0203ER15447; FG02-03ER15447
Resource Type:
Published Article
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Name: Plant Physiology (Bethesda) Journal Volume: 179 Journal Issue: 2; Journal ID: ISSN 0032-0889
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Plant Sciences

Citation Formats

Naumann, Christin, Müller, Jens, Sakhonwasee, Siriwat, Wieghaus, Annika, Hause, Gerd, Heisters, Marcus, Bürstenbinder, Katharina, and Abel, Steffen. The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy. United States: N. p., 2018. Web. https://doi.org/10.1104/pp.18.01379.
Naumann, Christin, Müller, Jens, Sakhonwasee, Siriwat, Wieghaus, Annika, Hause, Gerd, Heisters, Marcus, Bürstenbinder, Katharina, & Abel, Steffen. The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy. United States. https://doi.org/10.1104/pp.18.01379
Naumann, Christin, Müller, Jens, Sakhonwasee, Siriwat, Wieghaus, Annika, Hause, Gerd, Heisters, Marcus, Bürstenbinder, Katharina, and Abel, Steffen. Mon . "The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy". United States. https://doi.org/10.1104/pp.18.01379.
@article{osti_1484329,
title = {The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy},
author = {Naumann, Christin and Müller, Jens and Sakhonwasee, Siriwat and Wieghaus, Annika and Hause, Gerd and Heisters, Marcus and Bürstenbinder, Katharina and Abel, Steffen},
abstractNote = {Inorganic phosphate (Pi) is often a limiting plant nutrient. In members of the Brassicaceae family, such as Arabidopsis (Arabidopsis thaliana), Pi deprivation reshapes root system architecture to favor topsoil foraging. It does so by inhibiting primary root extension and stimulating lateral root formation. Root growth inhibition from phosphate (Pi) deficiency is triggered by iron-stimulated, apoplastic reactive oxygen species generation and cell wall modifications, which impair cell-to-cell communication and meristem maintenance. These processes require LOW PHOSPHATE RESPONSE1 (LPR1), a cell wall-targeted ferroxidase, and PHOSPHATE DEFICIENCY RESPONSE2 (PDR2), the single endoplasmic reticulum (ER)-resident P5-type ATPase (AtP5A), which is thought to control LPR1 secretion or activity. Autophagy is a conserved process involving the vacuolar degradation of cellular components. While the function of autophagy is well established under nutrient starvation (C, N, or S), it remains to be explored under Pi deprivation. Because AtP5A/PDR2 likely functions in the ER stress response, we analyzed the effect of Pi limitation on autophagy. Our comparative study of mutants defective in the local Pi deficiency response, ER stress response, and autophagy demonstrated that ER stress-dependent autophagy is rapidly activated as part of the developmental root response to Pi limitation and requires the genetic PDR2-LPR1 module. We conclude that Pi-dependent activation of autophagy in the root apex is a consequence of local Pi sensing and the associated ER stress response, rather than a means for systemic recycling of the macronutrient.},
doi = {10.1104/pp.18.01379},
journal = {Plant Physiology (Bethesda)},
number = 2,
volume = 179,
place = {United States},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1104/pp.18.01379

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Cited by: 5 works
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Works referencing / citing this record:

Autophagic Machinery of Plant Peroxisomes
journal, September 2019

  • Borek, Sławomir; Stefaniak, Szymon; Śliwiński, Jan
  • International Journal of Molecular Sciences, Vol. 20, Issue 19
  • DOI: 10.3390/ijms20194754