Arabidopsis; SR45; iron; metal homeostasis; serine/arginine-rich 45; splicing; zinc; Arabidopsis mutant; Biological process; Metal distributions; Plant Science
Abstract :
[en] The plant serine/arginine-rich (SR) splicing factor SR45 plays important roles in several biological processes, such as splicing, DNA methylation, innate immunity, glucose regulation, and abscisic acid signaling. A homozygous Arabidopsis sr45-1 null mutant is viable, but exhibits diverse phenotypic alterations, including delayed root development, late flowering, shorter siliques with fewer seeds, narrower leaves and petals, and unusual numbers of floral organs. Here, we report that the sr45-1 mutant presents an unexpected constitutive iron deficiency phenotype characterized by altered metal distribution in the plant. RNA-Sequencing highlighted severe perturbations in metal homeostasis, the phenylpropanoid pathway, oxidative stress responses, and reproductive development. Ionomic quantification and histochemical staining revealed strong iron accumulation in the sr45-1 root tissues accompanied by iron starvation in aerial parts. Mis-splicing of several key iron homeostasis genes, including BTS, bHLH104, PYE, FRD3, and ZIF1, was observed in sr45-1 roots. We showed that some sr45-1 developmental abnormalities can be complemented by exogenous iron supply. Our findings provide new insight into the molecular mechanisms governing the phenotypes of the sr45-1 mutant.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Fanara, Steven ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Schloesser, Marie ; Université de Liège - ULiège > Département des sciences de la vie
Hanikenne, Marc ✱; Université de Liège - ULiège > Département des sciences de la vie > Biologie végétale translationnelle
Motte, Patrick ✱; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
✱ These authors have contributed equally to this work.
Language :
English
Title :
Altered metal distribution in the sr45-1 Arabidopsis mutant causes developmental defects.
Funding was provided by the “Fonds de la Recherche Scientifique‐FNRS” (FRFC‐1.E049.15, PDR‐T.0206.13, CDR‐J.0009.17, PDR‐T0120.18, CDR‐J.0082.21). M.H. was Senior Research Associate of the F.R.S.‐FNRS. S.F. was a doctoral fellow (F.R.I.A.).
Albaqami, M., Laluk, K. & Reddy, A.S.N. (2019) The Arabidopsis splicing regulator SR45 confers salt tolerance in a splice isoform-dependent manner. Plant Molecular Biology, 100, 379–390.
Ali, G.S., Palusa, S.G., Golovkin, M., Prasad, J., Manley, J.L. & Reddy, A.S. (2007) Regulation of plant developmental processes by a novel splicing factor. PLoS One, 2, e471.
Babst, B.A., Gao, F., Acosta-Gamboa, L.M., Karve, A., Schueller, M.J. & Lorence, A. (2019) Three NPF genes in Arabidopsis are necessary for normal nitrogen cycling under low nitrogen stress. Plant Physiology and Biochemistry, 143, 1–10.
Baliardini, C., Meyer, C.L., Salis, P., Saumitou-Laprade, P. & Verbruggen, N. (2015) CATION EXCHANGER1 cosegregates with cadmium tolerance in the metal hyperaccumulator Arabidopsis halleri and plays a role in limiting oxidative stress in Arabidopsis spp. Plant Physiology, 169, 549–559.
Barberon, M., Vermeer, J.E., De Bellis, D., Wang, P., Naseer, S., Andersen, T.G. et al. (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell, 164, 447–459.
Barta, A., Kalyna, M. & Reddy, A.S. (2010) Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell, 22, 2926–2929.
Baxter, I., Hosmani, P.S., Rus, A., Lahner, B., Borevitz, J.O., Muthukumar, B. et al. (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genetics, 5, e1000492.
Bernardes, W.S. & Menossi, M. (2020) Plant 3' regulatory regions from mRNA-encoding genes and their uses to modulate expression. Frontiers in Plant Science, 11, 1252.
Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.
Califice, S., Baurain, D., Hanikenne, M. & Motte, P. (2012) A single ancient origin for prototypical serine/arginine-rich splicing factors. Plant Physiology, 158, 546–560.
Carvalho, R.F., Carvalho, S.D. & Duque, P. (2010) The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiology, 154, 772–783.
Carvalho, R.F., Szakonyi, D., Simpson, C.G., Barbosa, I.C., Brown, J.W., Baena-González, E. et al. (2016) The Arabidopsis SR45 splicing factor, a negative regulator of sugar signaling, modulates SNF1-related protein kinase 1 stability. Plant Cell, 28, 1910–1925.
Castaings, L., Caquot, A., Loubet, S. & Curie, C. (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Scientific Reports, 6, 37222.
Chamala, S., Feng, G., Chavarro, C. & Barbazuk, W.B. (2015) Genome-wide identification of evolutionarily conserved alternative splicing events in flowering plants. Frontiers in Bioengineering and Biotechnology, 3, 33.
Charlier, J.B., Polese, C., Nouet, C., Carnol, M., Bosman, B., Krämer, U. et al. (2015) Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives. Journal of Experimental Botany, 66, 3865–3878.
Chen, S.L., Rooney, T.J., Hu, A.R., Beard, H.S., Garrett, W.M., Mangalath, L.M. et al. (2019) Quantitative proteomics reveals a role for SERINE/ARGININE-Rich 45 in regulating RNA metabolism and modulating transcriptional suppression via the ASAP complex in Arabidopsis thaliana. Frontiers in Plant Science, 10, 1116.
Chen, T., Cui, P., Chen, H., Ali, S., Zhang, S. & Xiong, L. (2013) A KH-domain RNA-binding protein interacts with FIERY2/CTD phosphatase-like 1 and splicing factors and is important for pre-mRNA splicing in Arabidopsis. PLoS Genetics, 9, e1003875.
Chezem, W.R., Memon, A., Li, F.S., Weng, J.K. & Clay, N.K. (2017) SG2-Type R2R3-MYB Transcription Factor MYB15 Controls Defense-Induced Lignification and Basal Immunity in Arabidopsis. Plant Cell, 29, 1907–1926.
Colangelo, E.P. & Guerinot, M.L. (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell, 16, 3400–3412.
Cui, Y., Chen, C.L., Cui, M., Zhou, W.J., Wu, H.L. & Ling, H.Q. (2018) Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis. Molecular Plant, 11, 1166–1183.
Curie, C. & Mari, S. (2017) New routes for plant iron mining. The New Phytologist, 214, 521–525.
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K. & Scheible, W.R. (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology, 139, 5–17.
Dong, C., He, F., Berkowitz, O., Liu, J., Cao, P., Tang, M. et al. (2018) Alternative splicing plays a critical role in maintaining mineral nutrient homeostasis in rice (Oryza sativa). Plant Cell, 30, 2267–2285.
Dučić, T. & Polle, A. (2007) Manganese toxicity in two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca) seedlings as affected by phosphorus supply. Functional Plant Biology, 34, 31–40.
Durrett, T.P., Gassmann, W. & Rogers, E.E. (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology, 144, 197–205.
El-Ashgar, N.M., El-Basioni, A., El-Nahhal, I.M., Zourob, S.M., El-Agez, T.M. & Taya, S.A. (2012) Sol-gel thin films immobilized with bromocresol purple pH-sensitive indicator in presence of surfactants. ISRN Analytical Chemistry, 2012, 1–11.
Fan, S.C., Lin, C.S., Hsu, P.K., Lin, S.H. & Tsay, Y.F. (2009) The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell, 21, 2750–2761.
Fourcroy, P., Sisó-Terraza, P., Sudre, D., Saviron, M., Reyt, G., Gaymard, F. et al. (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. The New Phytologist, 201, 155–167.
Fukao, Y., Ferjani, A., Tomioka, R., Nagasaki, N., Kurata, R., Nishimori, Y. et al. (2011) iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiology, 155, 1893–1907.
García, M.J., Lucena, C., Romera, F.J., Alcántara, E. & Pérez-Vicente, R. (2010) Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. Journal of Experimental Botany, 61, 3885–3899.
Geldner, N. (2013) The endodermis. Annual Review of Plant Biology, 64, 531–558.
Glaring, M.A., Zygadlo, A., Thorneycroft, D., Schulz, A., Smith, S.M., Blennow, A. et al. (2007) An extra-plastidial alpha-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. Journal of Experimental Botany, 58, 3949–3960.
Golovkin, M. & Reddy, A.S. (1999) An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1-70K protein. The Journal of Biological Chemistry, 274, 36428–36438.
Green, L.S. & Rogers, E.E. (2004) FRD3 controls iron localization in Arabidopsis. Plant Physiology, 136, 2523–2531.
Guo, W., Nazim, H., Liang, Z. & Yang, D. (2016) Magnesium deficiency in plants: An urgent problem. The Crop Journal, 4, 83–91.
Hanikenne, M., Esteves, S.M., Fanara, S. & Rouached, H. (2021) Coordinated homeostasis of essential mineral nutrients: a focus on iron. Journal of Experimental Botany, 72, 2136–2153.
Hanikenne, M., Talke, I.N., Haydon, M.J., Lanz, C., Nolte, A., Motte, P. et al. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature, 453, 391–395.
Haydon, M.J., Kawachi, M., Wirtz, M., Hillmer, S., Hell, R. & Krämer, U. (2012) Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell, 24, 724–737.
Hindt, M.N., Akmakjian, G.Z., Pivarski, K.L., Punshon, T., Baxter, I., Salt, D.E. et al. (2017) BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana. Metallomics, 9, 876–890.
Ivanov, R., Brumbarova, T. & Bauer, P. (2012) Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Molecular Plant, 5, 27–42.
Jain, A., Wilson, G.T. & Connolly, E.L. (2014) The diverse roles of FRO family metalloreductases in iron and copper homeostasis. Frontiers in Plant Science, 5, 100.
Jakoby, M., Wang, H.Y., Reidt, W., Weisshaar, B. & Bauer, P. (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Letters, 577, 528–534.
Jeong, S. (2017) SR Proteins: binders, regulators, and connectors of RNA. Molecules and Cells, 40, 1–9.
Kailasam, S., Wang, Y., Lo, J.C., Chang, H.F. & Yeh, K.C. (2018) S-Nitrosoglutathione works downstream of nitric oxide to mediate iron-deficiency signaling in Arabidopsis. The Plant Journal, 94, 157–168.
Kamiya, T., Borghi, M., Wang, P., Danku, J.M., Kalmbach, L., Hosmani, P.S. et al. (2015) The MYB36 transcription factor orchestrates Casparian strip formation. Proceedings of the National Academy of Sciences of the United States of America, 112, 10533–10538.
Kawachi, M., Kobae, Y., Mori, H., Tomioka, R., Lee, Y. & Maeshima, M. (2009) A mutant strain Arabidopsis thaliana that lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant & Cell Physiology, 50, 1156–1170.
Kobayashi, T., Nagasaka, S., Senoura, T., Itai, R.N., Nakanishi, H. & Nishizawa, N.K. (2013) Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. Nature Communications, 4, 2792.
Laloum, T., Martín, G. & Duque, P. (2018) Alternative splicing control of abiotic stress responses. Trends in Plant Science, 23, 140–150.
Lan, P., Li, W., Lin, W.D., Santi, S. & Schmidt, W. (2013) Mapping gene activity of Arabidopsis root hairs. Genome Biology, 14, R67.
Le, C.T., Brumbarova, T., Ivanov, R., Stoof, C., Weber, E., Mohrbacher, J. et al. (2016) ZINC FINGER OF ARABIDOPSIS THALIANA12 (ZAT12) interacts with FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT) linking iron deficiency and oxidative stress responses. Plant Physiology, 170, 540–557.
Lei, Y., Korpelainen, H. & Li, C. (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere, 68, 686–694.
Li, J., Zhang, M., Sun, J., Mao, X., Wang, J., Liu, H. et al. (2020) Heavy metal stress-associated proteins in rice and Arabidopsis: genome-wide identification, phylogenetics, duplication, and expression profiles analysis. Frontiers in Genetics, 11, 477.
Li, S., Yamada, M., Han, X., Ohler, U. & Benfey, P.N. (2016) High-resolution expression map of the Arabidopsis root reveals alternative splicing and lincRNA regulation. Developmental Cell, 39, 508–522.
Li, W., Lin, W.D., Ray, P., Lan, P. & Schmidt, W. (2013) Genome-wide detection of condition-sensitive alternative splicing in Arabidopsis roots. Plant Physiology, 162, 1750–1763.
Lichtenthaler, H.K. & Buschmann, C. (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry, 1, F4.3.1–F4.3.8.
Lingam, S., Mohrbacher, J., Brumbarova, T., Potuschak, T., Fink-Straube, C., Blondet, E. et al. (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell, 23, 1815–1829.
Liu, M., Liu, X.X., He, X.L., Liu, L.J., Wu, H., Tang, C.X. et al. (2017) Ethylene and nitric oxide interact to regulate the magnesium deficiency-induced root hair development in Arabidopsis. The New Phytologist, 213, 1242–1256.
Liu, M., Zhang, H., Fang, X., Zhang, Y. & Jin, C. (2018) Auxin acts downstream of ethylene and nitric oxide to regulate magnesium deficiency-induced root hair development in Arabidopsis thaliana. Plant & Cell Physiology, 59, 1452–1465.
Liu, W., Sun, Q., Wang, K., Du, Q. & Li, W.X. (2017) Nitrogen limitation adaptation (NLA) is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1.7 in Arabidopsis. The New Phytologist, 214, 734–744.
Long, T.A., Tsukagoshi, H., Busch, W., Lahner, B., Salt, D.E. & Benfey, P.N. (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell, 22, 2219–2236.
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
Manley, J.L. & Krainer, A.R. (2010) A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins). Genes & Development, 24, 1073–1074.
Marschner, H. & Marschner, P. (2012) Marschner's mineral nutrition of higher plants, 3rd edition. London; Waltham, MA: Academic Press.
Meyer, K., Koester, T. & Staiger, D. (2015) Pre-mRNA splicing in plants: in vivo functions of RNA-binding proteins implicated in the splicing process. Biomolecules, 5, 1717–1740.
Millaleo, R., Reyes-Díaz, M., Alberdi, M., Ivanov, A.G., Krol, M. & Hüner, N.P. (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. Journal of Experimental Botany, 64, 343–354.
Mladenka, P., Macáková, K., Zatloukalová, L., Reháková, Z., Singh, B.K., Prasad, A.K. et al. (2010) In vitro interactions of coumarins with iron. Biochimie, 92, 1108–1114.
Morrissey, J., Baxter, I.R., Lee, J., Li, L., Lahner, B., Grotz, N. et al. (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell, 21, 3326–3338.
Nouet, C., Charlier, J.B., Carnol, M., Bosman, B., Farnir, F., Motte, P. et al. (2015) Functional analysis of the three HMA4 copies of the metal hyperaccumulator Arabidopsis halleri. Journal of Experimental Botany, 66, 5783–5795.
Nouet, C., Motte, P. & Hanikenne, M. (2011) Chloroplastic and mitochondrial metal homeostasis. Trends in Plant Science, 16, 395–404.
Palmer, C.M., Hindt, M.N., Schmidt, H., Clemens, S. & Guerinot, M.L. (2013) MYB10 and MYB72 are required for growth under iron-limiting conditions. PLoS Genetics, 9, e1003953.
Palusa, S.G., Ali, G.S. & Reddy, A.S. (2007) Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. The Plant Journal, 49, 1091–1107.
Palusa, S.G. & Reddy, A.S. (2010) Extensive coupling of alternative splicing of pre-mRNAs of serine/arginine (SR) genes with nonsense-mediated decay. The New Phytologist, 185, 83–89.
Petridis, A., Döll, S., Nichelmann, L., Bilger, W. & Mock, H.P. (2016) Arabidopsis thaliana G2-LIKE FLAVONOID REGULATOR and BRASSINOSTEROID ENHANCED EXPRESSION1 are low-temperature regulators of flavonoid accumulation. The New Phytologist, 211, 912–925.
Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
Pirone, C., Gurrieri, L., Gaiba, I., Adamiano, A., Valle, F., Trost, P. et al. (2017) The analysis of the different functions of starch-phosphorylating enzymes during the development of Arabidopsis thaliana plants discloses an unexpected role for the cytosolic isoform GWD2. Physiologia Plantarum, 160, 447–457.
Rajniak, J., Giehl, R.F.H., Chang, E., Murgia, I., von Wirén, N. & Sattely, E.S. (2018) Biosynthesis of redox-active metabolites in response to iron deficiency in plants. Nature Chemical Biology, 14, 442–450.
Ravet, K., Touraine, B., Boucherez, J., Briat, J.F., Gaymard, F. & Cellier, F. (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. The Plant Journal, 57, 400–412.
Remy, E., Cabrito, T.R., Batista, R.A., Hussein, M.A., Teixeira, M.C., Athanasiadis, A. et al. (2014) Intron retention in the 5'UTR of the novel ZIF2 transporter enhances translation to promote zinc tolerance in Arabidopsis. PLoS Genetics, 10, e1004375.
Reyt, G., Boudouf, S., Boucherez, J., Gaymard, F. & Briat, J.F. (2015) Iron- and ferritin-dependent reactive oxygen species distribution: impact on Arabidopsis root system architecture. Molecular Plant, 8, 439–453.
Robinson, N.J., Procter, C.M., Connolly, E.L. & Guerinot, M.L. (1999) A ferric-chelate reductase for iron uptake from soils. Nature, 397, 694–697.
Rodríguez-Celma, J., Connorton, J.M., Kruse, I., Green, R.T., Franceschetti, M., Chen, Y.T. et al. (2019) Arabidopsis BRUTUS-LIKE E3 ligases negatively regulate iron uptake by targeting transcription factor FIT for recycling. Proceedings of the National Academy of Sciences of the United States of America, 116, 17584–17591.
Römheld, V. & Marschner, H. (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiology, 80, 175–180.
Roschzttardtz, H., Conéjéro, G., Curie, C. & Mari, S. (2009) Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiology, 151, 1329–1338.
Roschzttardtz, H., Seguela-Arnaud, M., Briat, J.F., Vert, G. & Curie, C. (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell, 23, 2725–2737.
Sancenón, V., Puig, S., Mira, H., Thiele, D.J. & Peñarrubia, L. (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Molecular Biology, 51, 577–587.
Santi, S. & Schmidt, W. (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. The New Phytologist, 183, 1072–1084.
Scheepers, M., Spielmann, J., Boulanger, M., Carnol, M., Bosman, B., De Pauw, E. et al. (2020) Intertwined metal homeostasis, oxidative and biotic stress responses in the Arabidopsis frd3 mutant. The Plant Journal, 102, 34–52.
Schmidt, H., Günther, C., Weber, M., Spörlein, C., Loscher, S., Böttcher, C. et al. (2014) Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLoS One, 9, e102444.
Schvartzman, M.S., Corso, M., Fataftah, N., Scheepers, M., Nouet, C., Bosman, B. et al. (2018) Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri. The New Phytologist, 218, 269–282.
Selote, D., Samira, R., Matthiadis, A., Gillikin, J.W. & Long, T.A. (2015) Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiology, 167, 273–286.
Shang, X., Cao, Y. & Ma, L. (2017) Alternative splicing in plant genes: a means of regulating the environmental fitness of plants. International Journal of Molecular Sciences, 18., 1–18.
Shanmugam, V., Lo, J.C., Wu, C.L., Wang, S.L., Lai, C.C., Connolly, E.L. et al. (2011) Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana - the role in zinc tolerance. The New Phytologist, 190, 125–137.
Sinclair, S.A., Senger, T., Talke, I.N., Cobbett, C.S., Haydon, M.J. & Krämer, U. (2018) Systemic upregulation of MTP2- and HMA2-mediated Zn partitioning to the shoot supplements local Zn deficiency responses. Plant Cell, 30, 2463–2479.
Singh, S.K. & Reddy, V.R. (2017) Potassium starvation limits soybean growth more than the photosynthetic processes across CO2 levels. Frontiers in Plant Science, 8, 991.
Sivitz, A.B., Hermand, V., Curie, C. & Vert, G. (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS One, 7, e44843.
Siwinska, J., Siatkowska, K., Olry, A., Grosjean, J., Hehn, A., Bourgaud, F. et al. (2018) Scopoletin 8-hydroxylase: a novel enzyme involved in coumarin biosynthesis and iron-deficiency responses in Arabidopsis. Journal of Experimental Botany, 69, 1735–1748.
Song, W.Y., Choi, K.S., Kim, D.Y., Geisler, M., Park, J., Vincenzetti, V. et al. (2010) Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell, 22, 2237–2252.
Spielmann, J., Ahmadi, H., Scheepers, M., Weber, M., Nitsche, S., Carnol, M. et al. (2020) The two copies of the zinc and cadmium ZIP6 transporter of Arabidopsis halleri have distinct effects on cadmium tolerance. Plant, Cell & Environment, 43, 2143–2157.
Stacey, M.G., Patel, A., McClain, W.E., Mathieu, M., Remley, M., Rogers, E.E. et al. (2008) The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiology, 146, 589–601.
Talke, I.N., Hanikenne, M. & Krämer, U. (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiology, 142, 148–167.
Tehseen, M., Cairns, N., Sherson, S. & Cobbett, C.S. (2010) Metallochaperone-like genes in Arabidopsis thaliana. Metallomics, 2, 556–564.
Thomine, S. & Vert, G. (2013) Iron transport in plants: better be safe than sorry. Current Opinion in Plant Biology, 16, 322–327.
Tsai, H.H., Rodríguez-Celma, J., Lan, P., Wu, Y.C., Vélez-Bermúdez, I.C. & Schmidt, W. (2018) Scopoletin 8-hydroxylase-mediated fraxetin production is crucial for iron mobilization. Plant Physiology, 177, 194–207.
Verbruggen, N. & Hermans, C. (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant and Soil, 368, 87–99.
Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F. et al. (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell, 14, 1223–1233.
Wang, N., Cui, Y., Liu, Y., Fan, H., Du, J., Huang, Z. et al. (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Molecular Plant, 6, 503–513.
Wintermans, J.F. & de Mots, A. (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochimica et Biophysica Acta, 109, 448–453.
Xing, D., Wang, Y., Hamilton, M., Ben-Hur, A. & Reddy, A.S. (2015) Transcriptome-wide identification of RNA targets of Arabidopsis SERINE/ARGININE-RICH45 uncovers the unexpected roles of this RNA binding protein in RNA processing. Plant Cell, 27, 3294–3308.
Yang, T.J., Lin, W.D. & Schmidt, W. (2010) Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiology, 152, 2130–2141.
Yi, Y. & Guerinot, M.L. (1996) Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. The Plant Journal, 10, 835–844.
Yuan, Y., Wu, H., Wang, N., Li, J., Zhao, W., Du, J. et al. (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Research, 18, 385–397.
Zhang, W., Du, B., Liu, D. & Qi, X. (2014) Splicing factor SR34b mutation reduces cadmium tolerance in Arabidopsis by regulating iron-regulated transporter 1 gene. Biochemical and Biophysical Research Communications, 455, 312–317.
Zhang, X.N. & Mount, S.M. (2009) Two alternatively spliced isoforms of the Arabidopsis SR45 protein have distinct roles during normal plant development. Plant Physiology, 150, 1450–1458.
Zhang, X.N., Shi, Y., Powers, J.J., Gowda, N.B., Zhang, C., Ibrahim, H.M.M. et al. (2017) Transcriptome analyses reveal SR45 to be a neutral splicing regulator and a suppressor of innate immunity in Arabidopsis thaliana. BMC Genomics, 18, 772.
