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      Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1)

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          Abstract

          Phosphate and sulfate are essential macro-elements for plant growth and development, and deficiencies in these mineral elements alter many metabolic functions. Nutritional constraints are not restricted to macro-elements. Essential metals such as zinc and iron have their homeostasis strictly genetically controlled, and deficiency or excess of these micro-elements can generate major physiological disorders, also impacting plant growth and development. Phosphate and sulfate on one hand, and zinc and iron on the other hand, are known to interact. These interactions have been partly described at the molecular and physiological levels, and are reviewed here. Furthermore the two macro-elements phosphate and sulfate not only interact between themselves but also influence zinc and iron nutrition. These intricated nutritional cross-talks are presented. The responses of plants to phosphorus, sulfur, zinc, or iron deficiencies have been widely studied considering each element separately, and some molecular actors of these regulations have been characterized in detail. Although some scarce reports have started to examine the interaction of these mineral elements two by two, a more complex analysis of the interactions and cross-talks between the signaling pathways integrating the homeostasis of these various elements is still lacking. However, a MYB-like transcription factor, PHOSPHATE STARVATION RESPONSE 1, emerges as a common regulator of phosphate, sulfate, zinc, and iron homeostasis, and its role as a potential general integrator for the control of mineral nutrition is discussed.

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          Most cited references151

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          IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth.

          Plants are the principal source of iron in most diets, yet iron availability often limits plant growth. In response to iron deficiency, Arabidopsis roots induce the expression of the divalent cation transporter IRT1. Here, we present genetic evidence that IRT1 is essential for the uptake of iron from the soil. An Arabidopsis knockout mutant in IRT1 is chlorotic and has a severe growth defect in soil, leading to death. This defect is rescued by the exogenous application of iron. The mutant plants do not take up iron and fail to accumulate other divalent cations in low-iron conditions. IRT1-green fluorescent protein fusion, transiently expressed in culture cells, localized to the plasma membrane. We also show, through promoter::beta-glucuronidase analysis and in situ hybridization, that IRT1 is expressed in the external cell layers of the root, specifically in response to iron starvation. These results clearly demonstrate that IRT1 is the major transporter responsible for high-affinity metal uptake under iron deficiency.
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            A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.

            Plants have evolved a number of adaptive responses to cope with growth in conditions of limited phosphate (Pi) supply involving biochemical, metabolic, and developmental changes. We prepared an EMS-mutagenized M(2) population of an Arabidopsis thaliana transgenic line harboring a reporter gene specifically responsive to Pi starvation (AtIPS1::GUS), and screened for mutants altered in Pi starvation regulation. One of the mutants, phr1 (phosphate starvation response 1), displayed reduced response of AtIPS1::GUS to Pi starvation, and also had a broad range of Pi starvation responses impaired, including the responsiveness of various other Pi starvation-induced genes and metabolic responses, such as the increase in anthocyanin accumulation. PHR1 was positionally cloned and shown be related to the PHOSPHORUS STARVATION RESPONSE 1 (PSR1) gene from Chlamydomonas reinhardtii. A GFP::PHR1 protein fusion was localized in the nucleus independently of Pi status, as is the case for PSR1. PHR1 is expressed in Pi sufficient conditions and, in contrast to PSR1, is only weakly responsive to Pi starvation. PHR1, PSR1, and other members of the protein family share a MYB domain and a predicted coiled-coil (CC) domain, defining a subtype within the MYB superfamily, the MYB-CC family. Therefore, PHR1 was found to bind as a dimer to an imperfect palindromic sequence. PHR1-binding sequences are present in the promoter of Pi starvation-responsive structural genes, indicating that this protein acts downstream in the Pi starvation signaling pathway.
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              Plasticity of the Arabidopsis root system under nutrient deficiencies.

              Plant roots show a particularly high variation in their morphological response to different nutrient deficiencies. Although such changes often determine the nutrient efficiency or stress tolerance of plants, it is surprising that a comprehensive and comparative analysis of root morphological responses to different nutrient deficiencies has not yet been conducted. Since one reason for this is an inherent difficulty in obtaining nutrient-deficient conditions in agar culture, we first identified conditions appropriate for producing nutrient-deficient plants on agar plates. Based on a careful selection of agar specifically for each nutrient being considered, we grew Arabidopsis (Arabidopsis thaliana) plants at four levels of deficiency for 12 nutrients and quantified seven root traits. In combination with measurements of biomass and elemental concentrations, we observed that the nutritional status and type of nutrient determined the extent and type of changes in root system architecture (RSA). The independent regulation of individual root traits further pointed to a differential sensitivity of root tissues to nutrient limitations. To capture the variation in RSA under different nutrient supplies, we used principal component analysis and developed a root plasticity chart representing the overall modulations in RSA under a given treatment. This systematic comparison of RSA responses to nutrient deficiencies provides a comprehensive view of the overall changes in root plasticity induced by the deficiency of single nutrients and provides a solid basis for the identification of nutrient-sensitive steps in the root developmental program.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                28 April 2015
                2015
                : 6
                : 290
                Affiliations
                Biochimie et Physiologie Moléculaire des Plantes, Centre National de la Recherche Scientifique – Institut National de la Recherche Agronomique – Université Montpellier 2 Montpellier, France
                Author notes

                Edited by: Leon Kochian, United States Department of Agriculture – Agricultural Research Service, USA

                Reviewed by: Rashid Ali, University of Connecticut, USA; Miguel A. Pineros, United States Department of Agriculture, USA

                *Correspondence: Jean-François Briat, Biochimie et Physiologie Moléculaire des Plantes, Centre National de la Recherche Scientifique – Institut National de la Recherche Agronomique – Université Montpellier 2, SupAgro, Bat 7, 2 Place Viala, 34060 Montpellier Cedex 1, France briat@ 123456supagro.inra.fr

                This article was submitted to Plant Traffic and Transport, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2015.00290
                4411997
                25972885
                a3894786-7e3e-417a-8d7f-23b0566e7152
                Copyright © 2015 Briat, Rouached, Tissot, Gaymard and Dubos.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 December 2014
                : 09 April 2015
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 172, Pages: 16, Words: 0
                Categories
                Plant Science
                Review

                Plant science & Botany
                phr1,mineral homeostasis,phosphate,zinc,iron,sulfate,crosstalks,integration
                Plant science & Botany
                phr1, mineral homeostasis, phosphate, zinc, iron, sulfate, crosstalks, integration

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