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Abstract Iron (Fe) uptake and translocation in plants are fine-tuned by complex mechanisms that are not yet fully understood. In Arabidopsis thaliana, local regulation of Fe homeostasis at the root level has been extensively studied and is better understood than the systemic shoot-to-root regulation. While the root system is solely a sink tissue that depends on photosynthates translocated from source tissues, the shoot system is a more complex tissue, where sink and source tissues occur synchronously. In this study, and to gain better insight into the Fe deficiency responses in leaves, we overexpressed Zinc/Iron-regulated transporter-like Protein (ZIP5), an Fe/Zn transporter, in phloem-loading cells (proSUC2::AtZIP5) and determined the timing of Fe deficiency responses in sink (young leaves and roots) and source tissues (leaves). Transgenic lines overexpressing ZIP5 in companion cells displayed increased sensitivity to Fe deficiency in root growth assays. Moreover, young leaves and roots (sink tissues) displayed either delayed or dampened transcriptional responses to Fe deficiency compared to wild-type (WT) plants. We also took advantage of the Arabidopsis mutant nas4x-1 to explore Fe transcriptional responses in the opposite scenario, where Fe is retained in the vasculature but in an unavailable and precipitated form. In contrast to proSUC2::AtZIP5 plants, nas4x-1 young leaves and roots displayed a robust and constitutive Fe deficiency response, while mature leaves showed a delayed and dampened Fe deficiency response compared to WT plants. Altogether, our data provide evidence suggesting that Fe sensing within leaves can also occur locally in a leaf-specific manner.
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Loss of OPT3 function decreases phloem copper levels and impairs crosstalk between copper and iron homeostasis and shoot-to-root signaling in Arabidopsis thaliana
Abstract Copper (Cu) and iron (Fe) are essential micronutrients that are toxic when accumulating in excess in cells. Thus, their uptake by roots is tightly regulated. While plants sense and respond to local Cu availability, the systemic regulation of Cu uptake has not been documented in contrast to local and systemic control of Fe uptake. Fe abundance in the phloem has been suggested to act systemically, regulating the expression of Fe uptake genes in roots. Consistently, shoot-to-root Fe signaling is disrupted in Arabidopsis thaliana mutants lacking the phloem companion cell-localized Fe transporter, OLIGOPEPTIDE TRANSPORTER 3 (AtOPT3). We report that AtOPT3 also transports Cu in heterologous systems and contributes to its delivery from sources to sinks in planta. The opt3 mutant contained less Cu in the phloem, was sensitive to Cu deficiency and mounted a transcriptional Cu deficiency response in roots and young leaves. Feeding the opt3 mutant and Cu- or Fe-deficient wild-type seedlings with Cu or Fe via the phloem in leaves downregulated the expression of both Cu- and Fe-deficiency marker genes in roots. These data suggest the existence of shoot-to-root Cu signaling, highlight the complexity of Cu/Fe interactions, and the role of AtOPT3 in fine-tuning root transcriptional responses to the plant Cu and Fe needs.
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- PAR ID:
- 10411610
- Date Published:
- Journal Name:
- The Plant Cell
- ISSN:
- 1040-4651
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Copper and iron are micronutrients but are toxic when they accumulate in cells in excess. Crosstalk between copper and iron homeostasis in Arabidopsis thaliana has been documented and includes iron accumulation under copper deficiency and vice versa. However, molecular components of this crosstalk are not well understood. Iron concentration in the phloem has been suggested to act systemically, negatively regulating iron uptake to the root. Consistently, systemic iron signaling is disrupted in A. thaliana mutants lacking the phloem companion cell-localized iron transporter, AtOPT3, and opt3 mutants hyperaccumulate iron. Here, we report that in addition to iron, AtOPT3 transports copper and mediates copper loading to the phloem for delivery from sources to sinks. As a result of this function, the opt3-3 mutant accumulates less copper in the phloem, roots, developing leaves and embryos compared to wild type, is sensitive to copper deficiency, and mounts transcriptional copper deficiency response. Because copper deficiency has been shown to stimulate iron accumulation, we propose that reduced copper concentration in the phloem of the opt3-3 mutant and its constitutive copper deficiency contribute to iron overaccumulation in its tissues. Our data assign new transport capabilities to AtOPT3 and increase understanding of copper - iron interactions and signaling.more » « less
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Abstract Iron (Fe) and copper (Cu) are essential yet potentially toxic metals with interconnected metabolic pathways; however, the mechanisms underlying Fe–Cu crosstalk remain poorly defined. Here, we show that CITF1 (COPPER DEFICIENCY INDUCED TRANSCRIPTION FACTOR 1), a Cu homeostasis regulator in Arabidopsis thaliana, physically interacts with FIT (FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR), the central Fe homeostasis regulator, forming a nutrient-responsive transcriptional module. Under Cu deficiency, the CITF1–FIT complex accumulates and promotes expression of the Cu uptake genes COPT2 (COPPER TRANSPORTER 2), FRO4 (FERRIC REDUCTION OXIDASE 4), and FRO5 (FERRIC REDUCTION OXIDASE 5). Proteasome-dependent degradation regulates CITF1 and FIT stability, with Cu deficiency delaying their turnover in a CITF1-dependent manner. Under Fe deficiency, CITF1 expression is downregulated, allowing FIT to interact with bHLH38/39/100/101 partners and activate Fe uptake genes, as CITF1 disrupts these interactions. Thus, CITF1 negatively regulates Fe acquisition. Consistent with this, citf1-1 and citf1-2 mutants show reduced sensitivity to Fe deficiency. Under Cu deficiency, the citf1-2 and fit-2 mutants have additive effects and under Fe deficiency, the double mutant shows partial suppression of the fit-2 slow growth phenotype, supporting the positive and negative roles of CITF1 in Cu and Fe homeostasis, respectively. Complete loss of CITF1 function in the homozygous citf1-1 fit-2 double mutant causes embryo lethality, revealing roles for CITF1 and FIT in embryo development. These findings establish CITF1 as a nutrient-responsive regulator of Cu/Fe crosstalk, functioning through interactions with FIT to prioritize Cu or Fe acquisition and balance micronutrient homeostasis.more » « less
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Phosphorus (P) and iron (Fe) deficiency are major limiting factors for plant productivity worldwide. White lupin (Lupinus albus L.) has become a model plant for understanding plant adaptations to P and Fe deficiency, because of its ability to form cluster roots, bottle-brush-like root structures play an important role in the uptake of P and Fe from soil. However, little is known about the signaling pathways involved in sensing and responding to P and Fe deficiency. Sucrose, sent in increased concentrations from the shoot to the root, has been identified as a long-distance signal of both P and Fe deficiency. To unravel the responses to sucrose as a signal, we performed Oxford Nanopore cDNA sequencing of white lupin roots treated with sucrose for 10, 15, or 20 min compared to untreated controls. We identified a set of 17 genes, including 2 bHLH transcription factors, that were up-regulated at all three time points of sucrose treatment. GO (gene ontology) analysis revealed enrichment of auxin and gibberellin responses as early as 10 min after sucrose addition, as well as the emerging of ethylene responses at 20 min of sucrose treatment, indicating a sequential involvement of these hormones in plant responses to sucrose.more » « less
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/plcell/koad053
