Integration of Adaptive Changes to Iron Deficiency in Plants
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G Model CPB-30; No. of Pages 12 ARTICLE IN PRESS Current Plant Biology xxx (2016) xxx–xxx Contents lists available at ScienceDirect Current Plant Biology jo urnal homepage: www.elsevier.com/locate/cpb From the proteomic point of view: Integration of adaptive changes to iron deficiency in plants a a,b,∗ Hans-Jörg Mai , Petra Bauer a Institute of Botany, Heinrich Heine University Düsseldorf, Universitätsstraße 1, Building 26.13, 02.36, 40225 Düsseldorf, Germany b CEPLAS Cluster of Excellence on Plant Sciences, Heinrich Heine University Düsseldorf, Düsseldorf, Germany a r t i c l e i n f o a b s t r a c t Article history: Knowledge about the proteomic adaptations to iron deficiency in plants may contribute to find possible Received 10 July 2015 new research targets in order to generate crop plants that are more tolerant to iron deficiency, to increase Received in revised form 22 January 2016 the iron content or to enhance the bioavailability of iron in food plants. We provide this update on adap- Accepted 1 February 2016 tations to iron deficiency from the proteomic standpoint. We have mined the data and compared ten studies on iron deficiency-related proteomic changes in six different Strategy I plant species. We sum- Keywords: marize these results and point out common iron deficiency-induced alterations of important biochemical Arabidopsis pathways based on the data provided by these publications, deliver explanations on the possible benefits Iron Proteome that arise from these adaptations in iron-deficient plants and present a concluding model of these adap- tations. Furthermore, we demonstrate the close interdependence of proteins which were found regulated Post-transcriptional regulation across multiple studies, and we pinpoint proteins with yet unknown function, which may play important roles in iron homeostasis. © 2016 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 3+ 1. Introduction basic steps [6–8]: solubilization of Fe by rhizosphere acidifica- + 3+ 2+ tion by a P-type H -ATPase [9,10], reduction of Fe to Fe by As a micronutrient, iron plays important roles in the biochem- the ferric chelate reductase FRO2 (FERRIC REDUCTION OXIDASE 2) 2+ istry in animals and plants, and iron deficiency belongs to the most [11,12] and uptake of Fe into the root cells by the divalent metal prevalent nutritional disorders in humans [1]. Despite the high transporter IRT1 (IRON-REGULATED TRANSPORTER 1) [13–16]. In soil iron content, iron deficiency also frequently occurs in plants Arabidopsis, expression of these three genes is regulated in an iron- because only a small portion of iron is bioavailable. In the high pH dependent manner by the bHLH transcription factor FIT [17–19]. 3+ environment of calcareous soils Fe is nearly insoluble which ulti- fit knock-out mutants display a severe phenotype of iron starva- mately leads to iron deficiency in plant species that are not adapted tion with reduced growth and chlorosis and they are lethal at the [2]. Although essential for plants and other organisms, iron is poten- seedling stage [17,18]. The iron deficiency response is also accom- tially toxic [2–4] and excess iron may also cause yield loss in crop panied by accumulation of organic acids such as citrate which plants [5]. Therefore iron homeostasis in plants is tightly regulated. serve as chelators for enhancing iron mobilization. Root-to-shoot As a result of iron deficiency, plants adapt and induce or repress organic acid transport is also discussed to provide a carbon source to a number of iron-related gene and protein functions. A primary keep basic mechanisms such as respiration going in iron-deficient response to iron deficiency is that plants stimulate iron acqui- leaves [20]. Phenylpropanoids and riboflavin are synthesized in sition via two distinct strategies. Strategy II used by grasses is iron-deficient roots and, depending on the species, may contribute based on the secretion of phytosiderophores that form complexes to enhanced iron uptake and mobilization [21–29]. Since induced 3+ with Fe . The complexes are transported into the root cells by iron acquisition also facilitates uptake of other transition metals 3+ Fe -phytosiderophore transporters [6]. Iron acquisition in Strat- [30–32], protective mechanisms against heavy metal stress are egy I plants, which are all other studied plants, comprises three switched on [33,34]. Furthermore, iron can be reversibly inter- 2+ 3+ changed between the ferrous (Fe ) and ferric (Fe ) state which enables it to function as a cofactor of oxidoreductases or oxyge- ∗ nases most of which are heme or iron–sulfur proteins [35]. Besides Corresponding author at: Institute of Botany, Heinrich Heine University Düs- iron–sulfur and heme proteins there is a third iron-containing seldorf, Universitätsstraße 1, Building 26.13, 02.36, 40225 Düsseldorf, Germany. class of proteins referred to as mono- and dinuclear non-heme Fax: +49 211 81 12881. E-mail address: [email protected] (P. Bauer). iron proteins [36]. Aside from enzymes that can be found in all http://dx.doi.org/10.1016/j.cpb.2016.02.001 2214-6628/© 2016 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: H.-J. Mai, P. Bauer, From the proteomic point of view: Integration of adaptive changes to iron deficiency in plants, Curr. Plant Biol. (2016), http://dx.doi.org/10.1016/j.cpb.2016.02.001 G Model CPB-30; No. of Pages 12 ARTICLE IN PRESS 2 H.-J. Mai, P. Bauer / Current Plant Biology xxx (2016) xxx–xxx kingdoms, plant-specific iron–sulfur or heme proteins are involved N metabolism as well as riboflavin biosynthesis. The metabolic in the synthesis of many compounds such as phenylpropanoids profiling showed that riboflavin, FAD and riboflavin sulfates were [37], oxylipins [38], gibberellins [39] or brassinosteroids [40,41] present in yellow root zones [61]. In M. truncatula, adaptations and many other primary and secondary metabolites. Iron is also to iron deficiency include protein metabolism, N metabolism, needed by enzymes involved in nutrient assimilation such as glycolysis, TCA cycle, secondary metabolism and stress [63]. P. dul- nitrate and nitrite reductase or sulfite reductase that require heme, cis × P. persica roots show changes in redox homeostasis, ascorbic siroheme and [4Fe–4S] cluster cofactors [42–44]. Given the mul- acid synthesis, pathogen response, protein folding, glycolysis, fer- titude of processes that directly or indirectly depend on iron, mentation, electron transport and secondary metabolism [64]. In expression of a multitude of genes and proteins acting in different Arabidopsis roots, TCA cycle, glycolysis, amino acid metabolism metabolic and regulatory pathways is adapted as plants encounter and minor CHO metabolism were observed most regulated [55]. iron deficiency. In shoots of iron-deficient Arabidopsis plants, regulated protein Large scale transcriptomic analysis based on DNA microar- functions are rather related to protein processing, folding, sorting rays or RNA shotgun sequencing (RNA-Seq) are tools to gain and degradation and glutathione metabolism [68]. In the iTRAQ- overview of the plant’s global responses to physiological stim- based analyses, the most prominent changes in roots upon iron uli. Gene expression responses could be divided into clusters of deficiency have been observed for proteins involved in S-adenosyl co-expressed genes [19], and indeed separate transcription factor methionine (SAM) and nicotianamine (NA) synthesis. Furthermore, cascades are known to regulate these clusters [45–54]. How- proteins involved in the phenylpropanoid pathway were found up- ever, due to post-transcriptional regulation, protein stability and regulated upon iron deficiency [22]. Additionally, RNA and mRNA turnover and post-translational modifications, protein expression processing proteins are up-regulated [22]. In the phosphoproteome often does not correlate with transcript levels and this has also been [66] RNA processing and ribosomal proteins are enriched in iron- shown for Arabidopsis thaliana with regard to iron homeostasis deficient roots. Both indicates that post-transcriptional processing [22,55]. Indeed, AHA2 and FRO2 activity [10,11] as well as IRT1 sub- and translation may be altered upon iron deficiency in roots. cellular location and turnover are post-translationally controlled Taken together, the most commonly regulated functional cate- [56–59]. Also the activity of transcription factors is controlled at gories among the plant species investigated in the ten compared the protein level [60]. Therefore investigation of the proteome is studies are C and N metabolism, glycolysis and TCA cycle. Although very crucial to uncover the components for plant iron adaptation. these previously conducted proteomic studies display results with For this review we used the data of 10 previously published com- a very low to no overlap in single proteins regulated under dif- parative proteomic studies. These studies were performed with six ferent iron conditions there are still clearly recognizable parallels different plant species, namely Beta vulgaris [61], Cucumis sativus concerning the regulated functional categories with which the [62], Medicago truncatula [63], Prunus dulcis × Prunus persica [64], respectively regulated proteins are associated. For more informa- Solanum lycopersicum [65] and A. thaliana [22,55,66–68]. In order tion on