Research articleSuppression of Fe deficiency gene expression by jasmonate
Highlights
► Jasmonate suppression of IRT1 and FRO2 gene expression but not of their inducibility in response to Fe deficiency. ► Jasmonate inhibition of IRT1 and FRO2 gene expression independent of the functional regulator FIT. ► Jasmonate action not related to systemic Fe sufficiency signalling to down-regulate Fe deficiency responses in the root.
Introduction
Plant roots are nearly constantly exposed to nutrient salts in their environment. Yet, the uptake profiles for nutrients vary diurnally and in response to various physiological and developmental stimuli. Regulation of nutrient uptake is necessary not only to ensure minimum uptake of the essential nutrients but also to avoid excessive uptake followed by potentially toxic effects. Plants sense the availability of nutrients in their local environment and their physiological diurnal and developmental needs for these nutrients [1].
Uptake of Fe can be used as a model system to study the role of plant internal signals related to nutrient regulation to investigate the underlying regulatory mechanisms. The Fe status of a wild type plant is reflected by the expression levels of marker genes. For example, increased expression of IRT1 and FRO2 in the root compared to a control condition indicates Fe deficiency [2], [3], [4]. Mutant studies showed that these two genes encode structural core components for Fe acquisition from the soil following the Fe reduction-based strategy I. FRO2 encodes the root plasmamembrane-bound ferric chelate reductase [3], while IRT1 codes for the divalent metal transporter for Fe uptake [5], [6], [7]. FRO2 and IRT1 were often found co-regulated [8]. Their expression is controlled by a bHLH transcription factor named FIT [9]. In the absence of a functional FIT protein the expression of FRO2 and IRT1 is far lower than in wild type and if not supplemented with Fe fit mutants develop a lethal leaf chlorosis [10], [11], [12]. Ethylene and nitric oxide positively affect expression of IRT1 and FRO2 suggesting that these two signals increase the sensitivity of plants for Fe uptake [13], [14], [15], [16]. Cytokinins on the other hand cause a down-regulation of the two genes [17]. Hormonal influence on Fe acquisition gene expression may serve to coordinate physiology and stress responses with necessary adaptations for altered root growth and uptake of Fe [18], [19], [20], [21]. Systemic signals controlling Fe uptake have been physiologically identified but their nature is not known. For instance, grafting of constitutive mutant Fe-deficient shoots to wild type roots can override any local Fe sufficiency sensing in the root and promote constitutive induction of Fe acquisition responses [22], [23]. On the other hand, Fe-sufficient shoots may block Fe uptake in Fe-deficient parts of split roots [4], [8], [18], [19].
Jasmonates are oxylipin-based plant hormones originating from poly-unsaturated fatty acids that act in response to developmental or environmental stimuli [24]. Environmental cues for activating the jasmonate signalling pathway include wounding, insect attack or UV light and as such jasmonate belongs to the so-called stress hormones. Jasmonate has an interesting property in that it is a systemically acting mobile plant hormone [25]. Progress has been made in identifying the jasmonate signalling pathway by thorough analysis of JA resistant and insensitive mutants [26]. Jasmonates are perceived intracellularly by a jasmonate receptor belonging to the F-box protein family that upon binding to the plant hormone targets a repressor of the jasmonate response pathway for degradation [27], [28], [29]. The activated jasmonate form most efficiently bound by the jasmonate receptor was found to be an Ile-conjugated derivative of jasmonic acid (JA-Ile, namely (+)-7-iso-JA-Ile) [30], [31]. Isoleucine conjugation to jasmonate is catalyzed by an enzyme encoded by the JAR1 gene [32], [33].
Here, we tested whether the plant hormone jasmonate had any effect on the regulation of Fe uptake responses, and whether jasmonate might be a candidate for a systemic signal involved in Fe deficiency regulation.
Section snippets
Gene expression analysis of Fe deficiency genes in response to jasmonate treatment
In search for mobile plant signalling compounds that influence the regulation of Fe acquisition and may represent candidates as systemic signals we tested the effect of jasmonate on the regulation of the IRT1 promoter using transgenic pIRT1::GUS plants [7]. We exposed two week-old Arabidopsis seedlings for 3 days to + or − Fe in the presence of 0 or 100 μM jasmonate, respectively. We found that in the absence of jasmonate GUS activity was induced four times in the root upon − Fe treatment (
Discussion
Here, we demonstrated that the mobile plant hormone jasmonate affected Fe deficiency gene expression. FRO2 and IRT1 were negatively regulated by jasmonate in a manner that was dependent on jasmonate-Ile signalling. Negative regulation of FRO2 and IRT1 by jasmonate did not require the FIT protein which is a central regulator of Fe deficiency responses although the FIT gene was partially found repressed by jasmonate. The role of jasmonate was not found to be related to systemic signalling of Fe
Plant material
The Arabidopsis thaliana accession used was Col-0. fit-3 loss of function mutant (hereafter named fit mutant) was verified due to the strong leaf chlorosis [9], [11]. The jar1-1 and coi1-1 mutants were obtained from the European Arabidopsis Stock Center, and the phenotype was verified by an in vitro jasmonate response root growth assay [32]. pIRT1::GUS plants were obtained from C. Curie [7].
Plant growth conditions
Arabidopsis seeds were surface-sterilized with 6% NaOCl, 0.1% Triton-X for 10 min, and washed 5 times
Acknowledgements
Funding by the Deutsche Forschungsgemeinschaft is greatly acknowledged. We thank Angelika Anna for assistance in plant growth.
References (45)
- et al.
Root uptake regulation: a central process for NPS homeostasis in plants
Curr. Opin. Plant Biol.
(2009) - et al.
FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis
Plant. Physiol. Biochem.
(2007) - et al.
FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana
FEBS Lett.
(2004) - et al.
Ethylene involvement in the regulation of the H(+)-ATPase CsHA1 gene and of the new isolated ferric reductase CsFRO1 and iron transporter CsIRT1 genes in cucumber plants
Plant. Physiol. Biochem.
(2007) Plants under attack: systemic signals in defence
Curr. Opin. Plant Biol.
(2009)The power of mutants for investigating jasmonate biosynthesis and signaling
Phytochemistry
(2009)- et al.
Top hits in contemporary JAZ: an update on jasmonate signaling
Phytochemistry
(2009) - et al.
ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana
FEBS Lett.
(1997) Regulation of gene expression by jasmonate hormones
Phytochemistry
(2009)- et al.
A novel iron-regulated metal transporter from plants identified by functional expression in yeast
Proc. Natl. Acad. Sci. U S A
(1996)
A ferric-chelate reductase for iron uptake from soils
Nature
Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana
Planta
Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects
Plant. Mol. Biol.
The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana
Plant J.
IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth
Plant Cell
Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals
Plant Physiol.
The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response
Plant Cell
AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants
Cell Res.
Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis
J. Exp. Bot.
Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots
Plant J.
Ethylene could influence ferric reductase, iron transporter, and H+-ATPase gene expression by affecting FER (or FER-like) gene activity
J. Exp. Bot.
Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway
Plant J.
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