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Title: Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling

Journal Article · · Nature Communications

Abstract Iron deficiency hampers photosynthesis and is associated with chlorosis. We recently showed that iron deficiency-induced chlorosis depends on phosphorus availability. How plants integrate these cues to control chlorophyll accumulation is unknown. Here, we show that iron limitation downregulates photosynthesis genes in a phosphorus-dependent manner. Using transcriptomics and genome-wide association analysis, we identify two genes, PHT4;4 encoding a chloroplastic ascorbate transporter and bZIP58 , encoding a nuclear transcription factor, which prevent the downregulation of photosynthesis genes leading to the stay-green phenotype under iron-phosphorus deficiency. Joint limitation of these nutrients induces ascorbate accumulation by activating expression of an ascorbate biosynthesis gene, VTC4 , which requires bZIP58. Furthermore, we demonstrate that chloroplastic ascorbate transport prevents the downregulation of photosynthesis genes under iron-phosphorus combined deficiency through modulation of ROS homeostasis. Our study uncovers a ROS-mediated chloroplastic retrograde signaling pathway to adapt photosynthesis to nutrient availability.

Research Organization:
Carnegie Inst. of Washington, Washington, DC (United States); Donald Danforth Plant Science Center, St. Louis, MO (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0008769; SC0018277; SC0020366
OSTI ID:
1835175
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 12; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (55)

At ROP 6 is involved in reactive oxygen species signaling in response to iron‐deficiency stress in Arabidopsis thaliana journal October 2018
Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots journal June 2003
Iron Nutrition of Plants in Calcareous Soils book January 1982
1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana journal July 2016
Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions journal July 2016
EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis journal July 2021
Iron-Dependent Callose Deposition Adjusts Root Meristem Maintenance to Phosphate Availability journal April 2015
Iron deprivation-induced reactive oxygen species generation leads to non-autolytic PCD in Brassica napus leaves journal July 2013
Ancient and essential: the assembly of iron–sulfur clusters in plants journal April 2011
Iron nutrition, biomass production, and plant product quality journal January 2015
Effect of Iron Deficiency Induced Changes on Photosynthetic Pigments, Ribulose-1,5-Bisphosphate Carboxylase, and Photosystem Activities in Field Grown Grapevine (Vitis Vinifera L. cv. Pinot Noir) Leaves journal March 2001
Function and biogenesis of iron–sulphur proteins journal August 2009
AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis journal January 2015
BoxPlotR: a web tool for generation of box plots journal January 2014
HISAT: a fast spliced aligner with low memory requirements journal March 2015
Measurement of reduced, oxidized and total ascorbate content in plants journal April 2007
The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat: Effect of drought and UV on pea and wheat journal December 2001
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal December 1998
SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis journal September 2014
Iron deficiency of soybean in the North Central U.S. and associated soil properties journal February 2004
Leaf chlorophyll content and its relation to the intracellular localization of iron journal January 1982
Diagnosis and correction of iron deficiency in field crops ‐ an overview journal January 1982
Function of iron in chloroplasts journal March 1986
Signal transduction by reactive oxygen species journal July 2011
Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis journal June 2007
Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine journal February 2009
Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency journal June 2013
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update journal May 2018
Active Iron in Plant Leaves journal June 1979
Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions: Figure 1. journal June 2006
The Effect of Iron on the Primary Root Elongation of Arabidopsis during Phosphate Deficiency     journal May 2008
Differential Regulation of the Expression of Two High-Affinity Sulfate Transporters, SULTR1.1 and SULTR1.2, in Arabidopsis     journal April 2008
VTC4 Is a Bifunctional Enzyme That Affects Myoinositol and Ascorbate Biosynthesis in Plants journal April 2009
Identification of the Endodermal Vacuole as the Iron Storage Compartment in the Arabidopsis Embryo journal September 2009
Plasticity of the Arabidopsis Root System under Nutrient Deficiencies journal July 2013
The Impacts of Phosphorus Deficiency on the Photosynthetic Electron Transport Chain journal March 2018
Investigations of the Role of Iron in Chlorophyll Metabolism. II. Effect of Iron Deficiency on Chlorophyll Synthesis journal November 1963
JUNGBRUNNEN1 , a Reactive Oxygen Species–Responsive NAC Transcription Factor, Regulates Longevity in Arabidopsis journal February 2012
Vacuolar Nicotianamine Has Critical and Distinct Roles under Iron Deficiency and for Zinc Sequestration in Arabidopsis journal February 2012
GWAPP: A Web Application for Genome-Wide Association Mapping in Arabidopsis journal December 2012
The Chloroplast Function Database: a large-scale collection of Arabidopsis Ds/Spm - or T-DNA-tagged homozygous lines for nuclear-encoded chloroplast proteins, and their systematic phenotype analysis journal February 2010
Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters journal March 2008
Iron Uptake, Translocation, and Regulation in Higher Plants journal June 2012
ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control journal June 1998
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo journal June 2008
Systematic discovery of novel eukaryotic transcriptional regulators using sequence homology independent prediction journal June 2017
Ascorbic acid modulation by ABI4 transcriptional repression of VTC2 in the salt tolerance of Arabidopsis journal February 2021
Suppression of Reactive Oxygen Species Accumulation in Chloroplasts Prevents Leaf Damage but Not Growth Arrest in Salt-Stressed Tobacco Plants journal July 2016
The ethylene response factor AtERF4 negatively regulates the iron deficiency response in Arabidopsis thaliana journal October 2017
The presence of ferric and ferrous iron in the nonheme iron store of resident macrophages in different tissues and organs: histochemical demonstrations by the perfusion-Perls and -Turnbull methods in the rat journal January 2005
Nonheme-iron histochemistry for light and electron microscopy: a historical, theoretical and technical review journal January 2007
ROS-talk – how the apoplast, the chloroplast, and the nucleus get the message through journal January 2012
The Involvement of OsPHO1;1 in the Regulation of Iron Transport Through Integration of Phosphate and Zinc Deficiency Signaling journal April 2016
Iron Deficiency Induces a Partial Inhibition of the Photosynthetic Electron Transport and a High Sensitivity to Light in the Diatom Phaeodactylum tricornutum journal August 2016
Redox-regulated transcription in plants: Emerging concepts journal January 2017