Comparative expression profiling reveals a role of the root apoplast in local phosphate response.
BACKGROUND
Plant adaptation to limited phosphate availability comprises a wide range of responses to conserve and remobilize internal phosphate sources and to enhance phosphate acquisition. Vigorous restructuring of root system architecture provides a developmental strategy for topsoil exploration and phosphate scavenging. Changes in external phosphate availability are locally sensed at root tips and adjust root growth by modulating cell expansion and cell division. The functionally interacting Arabidopsis genes, LOW PHOSPHATE RESPONSE 1 and 2 (LPR1/LPR2) and PHOSPHATE DEFICIENCY RESPONSE 2 (PDR2), are key components of root phosphate sensing. We recently demonstrated that the LOW PHOSPHATE RESPONSE 1 - PHOSPHATE DEFICIENCY RESPONSE 2 (LPR1-PDR2) module mediates apoplastic deposition of ferric iron (Fe(3+)) in the growing root tip during phosphate limitation. Iron deposition coincides with sites of reactive oxygen species generation and triggers cell wall thickening and callose accumulation, which interfere with cell-to-cell communication and inhibit root growth.


RESULTS
We took advantage of the opposite phosphate-conditional root phenotype of the phosphate deficiency response 2 mutant (hypersensitive) and low phosphate response 1 and 2 double mutant (insensitive) to investigate the phosphate dependent regulation of gene and protein expression in roots using genome-wide transcriptome and proteome analysis. We observed an overrepresentation of genes and proteins that are involved in the regulation of iron homeostasis, cell wall remodeling and reactive oxygen species formation, and we highlight a number of candidate genes with a potential function in root adaptation to limited phosphate availability. Our experiments reveal that FERRIC REDUCTASE DEFECTIVE 3 mediated, apoplastic iron redistribution, but not intracellular iron uptake and iron storage, triggers phosphate-dependent root growth modulation. We further highlight expressional changes of several cell wall-modifying enzymes and provide evidence for adjustment of the pectin network at sites of iron accumulation in the root.


CONCLUSIONS
Our study reveals new aspects of the elaborate interplay between phosphate starvation responses and changes in iron homeostasis. The results emphasize the importance of apoplastic iron redistribution to mediate phosphate-dependent root growth adjustment and suggest an important role for citrate in phosphate-dependent apoplastic iron transport. We further demonstrate that root growth modulation correlates with an altered expression of cell wall modifying enzymes and changes in the pectin network of the phosphate-deprived root tip, supporting the hypothesis that pectins are involved in iron binding and/or phosphate mobilization.
Proteome Analytics Research Group, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany.
Wolfgang
W
Hoehenwarter
Department of Stress and Developmental Biology, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany.
Susann
S
Mönchgesang
Department of Stress and Developmental Biology, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany.
Steffen
S
Neumann
Proteome Analytics Research Group, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany.
Petra
P
Majovsky
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany.|Institute of Biochemistry and Biotechnology, Martin Luther University Halle-Wittenberg, D-06120, Halle (Saale), Germany.|Department of Plant Sciences, University of California-Davis, Davis, CA, 95616, USA.
Steffen
S
Abel
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany. Jens.Mueller@ipb-halle.de.
Jens
J
Müller
D000222:Adaptation, Physiological / Q000235:genetics; D000251:Adenosine Triphosphatases / Q000235:genetics / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D001692:Biological Transport / Q000235:genetics; D002473:Cell Wall / Q000235:genetics* / Q000378:metabolism; D002853:Chromatography, Liquid; D020869:Gene Expression Profiling / Q000379:methods*; D018506:Gene Expression Regulation, Plant; D007501:Iron / Q000378:metabolism; D013058:Mass Spectrometry; D009154:Mutation; D020411:Oligonucleotide Array Sequence Analysis; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010368:Pectins / Q000378:metabolism; D010710:Phosphates / Q000378:metabolism*; D018517:Plant Roots / Q000235:genetics* / Q000378:metabolism; D020543:Proteome / Q000235:genetics / Q000378:metabolism; D040901:Proteomics / Q000379:methods; D017382:Reactive Oxygen Species / Q000378:metabolism; D012987:Soil / Q000737:chemistry
D029681:Arabidopsis Proteins; D010710:Phosphates; D020543:Proteome; D017382:Reactive Oxygen Species; D012987:Soil; D010368:Pectins; D007501:Iron; C543910:LPR1 protein, Arabidopsis; D010088:Oxidoreductases; D000251:Adenosine Triphosphatases; C543909:PDR2 protein, Arabidopsis
Arabidopsis thaliana; Cell wall; Iron transport; Pectin; Phosphate deficiency; Proteomics; Root growth; Transcriptomics