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Int. J. Mol. Sci. 2013, 14(3), 4545-4559; doi:10.3390/ijms14034545
Abstract: It has been suggested that cesium is absorbed from the soil through potassium uptake machineries in plants; however, not much is known about perception mechanism and downstream response. Here, we report that the jasmonate pathway is required in plant response to cesium. Jasmonate biosynthesis mutant aos and jasmonate-insensitive mutant coi1-16 show clear resistance to root growth inhibition caused by cesium. However, the potassium and cesium contents in these mutants are comparable to wild-type plants, indicating that jasmonate biosynthesis and signaling are not involved in cesium uptake, but involved in cesium perception. Cesium induces expression of a high-affinity potassium transporter gene HAK5 and reduces potassium content in the plant body, suggesting a competitive nature of potassium and cesium uptake in plants. It has also been found that cesium-induced HAK5 expression is antagonized by exogenous application of methyl-jasmonate. Taken together, it has been indicated that cesium inhibits plant growth via induction of the jasmonate pathway and likely modifies potassium uptake machineries.
Cesium (Cs+) is a Group I alkali metal, which exists naturally at very low concentrations in the soil. Cs+ has no known beneficial function in plants; however, it can, at high concentrations, cause toxicity, observed as growth inhibition (reviewed in ). Thus far, Cs+ uptake and response in plants have not been thoroughly studied. However, the accident at the Fukushima nuclear power plant following the disaster in 2011 in Japan highlighted the importance of understanding the mechanism of cesium uptake in plants to improve phytoremediation efficiency for radiocesium. Radiocesium, 134Cs and 137Cs, produced from anthropogenic sources are of environmental and health concerns, since they are rapidly incorporated into the food chain, emit β and γ radiation and have relatively long half-lives (reviewed in ). The potential of plants to decontaminate radiocesium from soil was also focused after the accident in Chernobyl [2,3]. Earlier studies have suggested that Cs+ may be absorbed by plants in a competitive fashion with potassium (K+), which belongs to the same alkali metal group and shares similar chemical properties with Cs+. The first report that plants accumulate Cs+ through the same uptake mechanism as K+ was published as early as 1941 , and many other studies reinforced this view (reviewed in ). A theoretical modeling predicted that voltage-insensitive cation channels (VICCs) predominantly mediate Cs+ uptake under the K+ sufficient conditions and K+ uptake permeases (KUPs) significantly contribute under the K+ deficient conditions . In Arabidopsis thaliana, some members of cyclic nucleotide gated channels (CNGCs), which belong to VICCs, such as CNGC1, CNGC2, CNGC4 and CNGC10, were predicted to form K+ channels and, thus, suggested as being involved in Cs+ uptake, also [5–8].
The first K+ channel identified in plants is KAT1 from Arabidopsis, which functions at high K+ concentrations as a voltage-dependent, low-affinity inward rectifying channel . The major K+ channel functioning in the roots of Arabidopsis under the K+ sufficient conditions is assumed to be AKT1 . However, the contribution of these channels to Cs+ uptake is small or negligible [9,11]. In response to K+ deficiency, expression of high-affinity K+ transporters, members of the KUP family, are induced, such as high affinity K+ transporter5 (HAK5) and KUP3[12,13]. HAK5 has been reported to be involved in Cs+ uptake in planta, consequently resulting in higher Cs+ accumulation under the K+ deficient conditions . Another K+ transporter, KUP9, from Arabidopsis was also shown to transport Cs+ when expressed in a K+ transport-deficient mutant of Escherichia coli.
There have been a few reports pointing out interaction between K+ deficiency response and phytohormone signaling. Expression of ethylene biosynthesis genes and ethylene production are reported to be induced in response to K+ deficiency and, subsequently, activate reactive oxygen species production . Expression of jasmonate (JA) biosynthesis genes is also induced in response to K+ deficiency and confers tolerance to insects [16–18]. Cytokinins, by contrast, decrease under the K+ deficient conditions and allow downstream response for adaptation to take place . Auxin-related mutants were found to be impaired in K+ deficiency-induced lateral root growth . If Cs+ were to cause similar effects as K+ deficiency in plants, it is possible that Cs+ response is regulated through phytohormone pathways.
In this study, JA biosynthesis and signaling were demonstrated to be required in plant response to Cs+. JAs are a class of phytohormone that are involved in various physiological processes, such as growth inhibition, fertility, senescence and defense against biotic and abiotic stresses . JAs are biosynthesized from linolenic acid through a series of steps, including allene oxide synthase (AOS) , and recognized by a receptor complex which is composed of an E3 ubiquitin ligase, SCF (SKP1, CDC53p/CUL1 F-box protein) complex. An active form of JAs, the jasmonyl-isoleucine conjugate (JA–Ile), directly binds to the F-box protein in the receptor complex, CORONATINE INSENSITIVE1 (COI1), and SCFCOI1 targets the negative regulators for proteolysis to activate downstream JA signaling in Arabidopsis[23–27]. Therefore, mutations in COI1 can render the plants insensitive to JAs [28,29].
Here, we investigated the relationship between JA biosynthesis/signaling and Cs+ response in Arabidopsis in order to understand the fundamental mechanism of plant response to Cs+. Our studies revealed the induction of JA biosynthesis/signaling and consequent growth inhibition in response to Cs+. However, JA signaling was not apparently involved in Cs+ uptake under the K+ sufficient conditions. Meanwhile, induction of HAK5 was demonstrated in response to Cs+, suggesting the involvement of K+ uptake machineries in Cs+ uptake. The possibility of JA signaling casting an antagonistic effect on HAK5 expression was also implied. In this report, plant response to Cs+ is dissected.
2.1. JA-Related Mutants Are Less Responsive to Cs+-Induced Growth Inhibition
In order to understand the mechanism of Cs+ response in plants, phytohormone-related mutants in Arabidopsis thaliana were tested on 0.5 mM KCl with or without 0.3 mM CsCl. This condition was chosen as a “stringent condition” for monitoring strong Cs+ resistance phenotype. In this condition, growth of Col-0 plants (wild-type) was severely retarded by the addition of CsCl (Figure 1A). However, a JA biosynthesis mutant aos[30,31] and a JA-insensitive mutant coi1-16  showed significantly less response to Cs+-induced root growth retardation (p < 0.001, Figure 1). A mutant, which produces less bioactive JA-Ile and shows mild JA-insensitive phenotype, jasmonate resistant1 (jar1-1) , also showed less response to Cs+ in terms of root growth inhibition (p < 0.001, Table S1). Among them, the stronger phenotype of aos corresponds with the fact that the aos mutant is a knockout line . The coi1-16 and jar1-1 mutants are known to be “leaky” [29,33], and this might be why their resistance to Cs+ was also compromised. Also, other phytohormone-related mutants were found to be less responsive to Cs+, such as an auxin-insensitive mutant, auxin resistant1 (aux1-7)  (p < 0.001), and, to a lesser extent (p < 0.01), a trans-zeatin-type cytokinin biosynthesis quadruple mutant, isopentenyltransferase1,3,5,7 (ipt1,3,5,7)  and a cytokinin-insensitive double mutant histidine kinase2;3 (ahk2;3)  (Table S1). An ethylene-insensitive mutant, ethylene insensitive2, (ein2-1) , but not ethylene response sensor1 (ers1-1) , was marginally less responsive to Cs+ (p < 0.05, Table S1). A GA-related DELLA double mutant, repressor of ga;gibberellic acid insensitive (rga-24;gai-t6) , showed increased growth % in response to Cs+ compared to its wild-type, Ler (p < 0.001, Table S1). This could be due to the absence of growth inhibitor proteins in the mutant , enabling the resistance to Cs+-induced growth inhibition, but further analysis is required for confirmation. The relationship between Cs+ response and JA signaling was further investigated.
2.2. Resistance of JA-Related Mutants to Cs+ Was Not Due to Less Uptake of Cs+
JA-related mutants were found to be less responsive to Cs+-induced growth inhibition compared to wild-type. One explanation could be that JA-related mutants might be impaired in Cs+ uptake. To test this possibility, K+ and Cs+ contents were measured in wild-type, aos and coi1-16 treated with or without 0.3 mM CsCl under the K+ sufficient condition (1.75 mM KCl) for seven days. Reduced K+ contents were observed upon Cs+ treatment (p < 0.05, Figure 2A). However, there was no statistically significant difference observed between wild-type and mutants for both K+ and Cs+ contents, regardless of Cs+ treatment (Figure 2). This suggests that the JA pathway is not involved in the uptake of Cs+ or K+ in this condition. More K+ and Cs+ were accumulated per mg dry weight at the later stage of growth (day 12), but the pattern was maintained (Figure S1).
2.3. Cs+ Induces JA Signaling as well as HAK5 Expression
To further analyze the interplay between Cs+ perception and JA signaling, expression of the marker genes for JA signaling, PDF1.2 and VSP2[40–42], was investigated in response to Cs+. Both PDF1.2 and VSP2 levels were increased upon Cs+ treatment under the K+ sufficient condition, especially in the shoots (p < 0.05, Figure 3), suggesting the induction of the general JA pathway by Cs+. This induction was absent in the aos mutant (Figure S2). There was no additive effect of Cs+ on methyl jasmonate (MeJA)-induced VSP2 expression (Figure 3).
It has been reported that high-affinity K+ transporter, HAK5, is not only involved in K+ uptake, but also in Cs+ uptake . The expression of HAK5 is sharply induced in response to K+ deficiency , and there are some indications that Cs+ may cause K+ deficiency in plants. Therefore, we analyzed the transcript levels of HAK5 in response to Cs+ under the K+ sufficient condition. Expression of HAK5 was, indeed, induced in response to Cs+, and this induction also occurred in JA-related mutants, aos and coi1-16 (p < 0.05, Figure 4).
2.4. JA Antagonizes Cs+-Induced HAK5 Expression
Since HAK5 was found to be induced in response to Cs+, spatial localization of HAK5 was investigated. Transgenic plants carrying the HAK5 promoter fused to the luciferase reporter construct (HAK5promoter::LUC) were used, and their activities are known to be induced in K+ deficiency . In this study, low levels of luciferase activity were visible at root tips of untreated plants under the K+ sufficient condition (Figure 5). Upon Cs+ treatment, strong induction of luciferase activity was observed in the roots, and this induction was abolished by the addition of MeJA (Figure 5). The chemiluminescence intensity of these images and quantification of HAK5 transcripts in wild-type roots treated with Cs+ and MeJA are shown in Table S2 and Figure S3, respectively. Chemiluminescence images of HAK5promoter::LUC plants grown on 0.5 mM KCl with or without Cs+ are also presented in Figure S4.
Cs+ has no known nutritional or other function in plants. Thus far, scarcely any knowledge has been gained on how plants absorb Cs+ from the soil, how it is transported inside the plant body, and what is the plant response. However, an urgent need for improved phytoremediation methods for radioactive Cs+ has urged scientists to better understand the mechanism of Cs+ uptake, transport and perception in plants. In Arabidopsis, a possible mechanism for tolerance to heavy metals, such as arsenic, mercury and cadmium, has been reported [43,44], but whether the same tolerance mechanism applies for Cs+ is not yet known. A T-DNA insertion mutant which is impaired in Cs+ uptake has been isolated; however, the identity of the gene disturbed is not revealed .
The similarity of the nature between Cs+ and K+ and the involvement of phytohormone pathways in K+ deficiency response provoked us to investigate the relationship between phytohormone pathways and Cs+ response. For this purpose, various phytohormone-related mutants in Arabidopsis thaliana were analyzed for their response to Cs+. It has been reported that K+ deficiency response is observed under 100 μM K+ concentrations in Arabidopsis. Therefore, we used the 0.5 mM KCl condition, which is well above the threshold for “K+ deficient conditions”, but lower than what is generally taken as “K+ sufficient conditions” (1.75 mM KCl) , to create a “stringent condition” in selecting strong phenotype mutants for Cs+. Of those mutants tested, JA-related mutants, aos, coi1-16 and jar1-1, showed strong resistance to Cs+-induced growth inhibition. Our data suggest that the JA pathway, and possibly some other phytohormone pathways, is involved in plant response to Cs+. This is the first report, as far as we are aware, to demonstrate the interaction between Cs+ response and the JA pathway in plants. Some phytohormone pathways, including ethylene, auxin, cytokinin and JA, have been reported to be involved in response to K+ deficiency [15–20]; therefore, in the future, it will be interesting to investigate the relationship of the Cs+-induced JA pathway with K+ deficiency.
Although aos and coi1-16 were less responsive to Cs+, this was not because they accumulated less Cs+. Cs+ contents, as well as K+ contents, were comparable to those of wild-type plants, suggesting that the JA pathway is involved, at least partly, in the perception of Cs+, not in uptake. Classic downstream marker genes of the JA pathway, PDF1.2 and VSP2, represent two distinct branches of the signaling pathway [40–42]. Under the K+ sufficient condition, both of these marker genes were found to be increased in response to Cs+, especially in the aerial parts. This induction was not observed in the aos mutant, indicating that Cs+ induces JA biosynthesis and downstream signaling.
It was also interesting to observe that K+ contents were reduced upon Cs+ treatment under the K+ sufficient condition. The competitive nature between Cs+ and K+ accumulation in Arabidopsis was demonstrated in a previous report . Although Cs+ has been used as a classic pharmacological inhibitor of K+ channels , our findings might also indicate that Cs+ could have been absorbed through the K+ uptake mechanism in a competitive manner. There are a few reports that suggest the possibility of K+ transporters/channels absorbing Cs+ in plants, including a low-affinity inward-rectifying channel in Arabidopsis, KAT1 , a high-affinity K+ transporter, HAK5 [12,48], and another K+ transporter, KUP9 . In this study, we indicated that the transcript levels of HAK5 were increased in response to Cs+ under the K+ sufficient condition. The reporter construct study using HAK5promoter::LUC showed that its promoter activity was particularly notable in the actively growing part of the roots, and this pattern was similar to that of the K+-starved plants . These findings, together with the results from the K+/Cs+ content study, agree with the hypothesis that Cs+ is absorbed through K+ uptake machinery in a competitive fashion.
JA treatment, on the other hand, was found to abolish Cs+-induced HAK5 expression in the reporter construct study, suggesting an antagonistic effect of JA on HAK5 expression. Since Cs+ seemingly induces both JA biosynthesis/signaling and HAK5 expression, this antagonism may function as a negative feedback mechanism to fine-tune Cs+ response in plants.
A summary of our findings on Cs+-induced growth inhibition and gene expression is shown as a model pathway in Figure 6. Cs+ induces JA biosynthesis and the downstream signaling pathway in Arabidopsis. This is probably the major pathway for Cs+-induced growth inhibition of roots, since a mutant incapable of producing JAs hardly shows any reduction in root length in response to Cs+. In parallel, Cs+ induces HAK5, a reporter gene for K+ deficiency . Further studies are required to elucidate whether Cs+ treatment causes K+ deficiency to induce HAK5 expression in plants. It will be interesting to test plant response to Cs+ under various K+ conditions, since plants are expected to exhibit different K+ uptake mechanisms, according to K+ availability. It was also indicated that the JA pathway might antagonize HAK5 expression. The mechanism in which this antagonism occurs awaits elaboration; however, it is possible that one of APETALA2/Ethylene Response Factor (AP2/ERF) transcription factors induced by the JA signaling pathway binds to the GCC-box of the HAK5 promoter to regulate its expression. HAK5 has been reported to be regulated by an ERF/AP2 transcription factor, RAP2.11, in response to K+ deficiency . Meanwhile, JA-inducible AP2/ERFs are known to regulate expression of a series of GCC-box-containing genes, such as PDF1.2, through direct binding to the GCC-boxes of the promoter region [51–53]. Recently, involvement of cytokinin in K+ deficiency response and HAK5 expression has been reported . It will be also interesting to further investigate the involvement of biosynthesis and the signaling of cytokinin and other phytohormones in Cs+ response in plants.
Here, we presented the first report that demonstrated the interplay between Cs+ response and JA signaling in plants. It was also highlighted that Cs+ uptake, Cs+-induced growth inhibition and gene expression were apparently regulated through different mechanisms. Elucidation of the fine balance between K+ and Cs+ to regulate plant response and growth is awaited.
4. Experimental Section
4.1. Plant Material and Growth Conditions
The Arabidopsis thaliana (L.) Heynh. accession Col-0 and Ler were used as wild-types. HAK5promoter::LUC was developed in the lab . aos[30,31], ein2-1  and jar1-1  are NASC stocks (Nottingham Arabidopsis Stock Centre, Loughborough, UK). coi1-16 , ipt1,3,5,7, ahk2;3, ers1-1 , aux1-7  and rga-24;gai-t6  were gifts from Dr. Turner, Dr. Kakimoto, Dr. Wen, Dr. Schachtman and Dr. Harberd. Seeds were surface-sterilized with 70% (v/v) ethanol and 0.05% (v/v) Triton X-100 and sown on media, indicated below. For the growth assay, media contained 0.5 mM KCl, 2 mM Ca(NO3)2, 0.5 mM phosphoric acid, 0.75 mM MgSO4, 50 μM H3BO3, 10 μM MnCl, 2 μM ZnSO4, 1.5 μM CuSO4, 0.075 μM NH4Mo7O24 and 74 μM Fe-EDTA, pH 5.8, with Ca(OH)2, 1% (w/v) sucrose and 0.5% (w/v) SeaKem agarose (Cambrex, Rockland, ME, USA) supplemented with or without 0.3 mM CsCl and for the rest of the study, media contained 1.75 mM KCl, 2 mM Ca(NO3)2, 0.5 mM phosphoric acid, 0.75 mM MgSO4, 50 μM H3BO3, 10 μM MnCl, 2 μM ZnSO4, 1.5 μM CuSO4, 0.075 μM NH4Mo7O24 and 74 μM Fe-EDTA, pH 5.8, with Ca(OH)2, 1% (w/v) sucrose and 0.5% (w/v) SeaKem agarose (Cambrex) supplemented with or without 0.3 mM CsCl or 2.5 μM MeJA. After stratifying for 3 to 4 days at 4 °C, plants were placed in a vertical orientation in a growth cabinet at 22 °C in a 16 h light/8 h dark photocycle with a light intensity of 70–90 μmol/m2/sec.
4.2. Root Growth Assay
Seedlings grown for 7 days were removed from media, and the root lengths were measured directly on a ruler wetted with 70% (v/v) glycerol. The relative % of root growth was calculated according to the formula, y/x × 100, where x was the average of root lengths of untreated seedlings and y was the root lengths of each Cs+-treated seedling and was averaged. One-way ANOVA with Dunnett’s multiple comparison posttest (p < 0.05) was performed using Prism (GraphPad Software, La Jolla, CA, USA) to determine the statistical significance.
4.3. Element Analysis
Seedlings grown for 7 days were washed in Milli-Q water, dried on a piece of paper towel, placed in a paper envelope and dried in an oven at 65 °C for 3–4 days. Approximately 2 mg of dried samples were extracted in 1 mL of 60% (v/v) HNO3 at 125 °C for 1 h, followed by 1 mL of 30% (v/v) H2O2 and diluted with Milli-Q water to get a total volume of 10 mL. For K+ analysis, samples were further diluted 10 times with 6% (v/v) HNO3. For Cs+ analysis, 0.1% (w/v) KCl was added to each sample and standard solution to prevent ionization of Cs+, according to the manufacturer’s instructions (PerkinElmer, Waltham, MA, USA). K+ and Cs+ contents were measured on a flame atomic absorption spectrometer AAnalyst 200 (PerkinElmer). Concentrations were calculated against each standard curve, and one-way ANOVA with Bonferroni′s multiple comparison posttest (p < 0.05) was performed using Prism to determine the statistical significance.
4.4. qRT-PCR Analysis
Seedlings grown for 7 days (for HAK5 expression) or 11 days (for VSP2 and PDF1.2 expression) were flash-frozen in liquid N2 and ground using a mixer mill. Total RNA was extracted, treated with DNaseI (Invitrogen, Carlsbad, CA, USA) and synthesized into cDNA using SuperScript III (Invitrogen). Quantitative real-time reverse transcription-PCR (qRT-PCR) was performed using THUNDERBIRD SYBR qPCR mix (TOYOBO, Osaka, Japan) and a Mx3000P qPCR system (Agilent Technologies, Santa Clara, CA, USA). The amplification conditions were 95 °C for 15 s and 60 °C for 30 s. The cycle was repeated 40 times, preceded by 95 °C for 1 min and followed by a dissociation program to create melting curves. Three technical replicates for each sample were run. The β-tubulin gene (TUB2) was used as a reference gene. The primers used were as follows: HAK5 forward 5’-CGAGACGGACAAAGAAGAGGAACC and reverse 5’-CACGACCCTTCCCGACCTAATCT ; VSP2 forward 5’-CCTAAAGAACGACACCGTCA and reverse 5’-TCGGTCTTCTCTGTTCCGTA ; PDF1.2 forward 5’-TTGCTGCTTTCGACGCA and reverse TGTCCCACTTGGCTTCTCG ; and TUB2 forward 5’-GCCAATCCGGTGCTGGTAACA and reverse 5’-CATACCAGATCCAGTTCCTCCTCCC . One-way ANOVA with Bonferroni’s multiple comparison posttest (p < 0.05) was performed using Prism to determine the statistical significance.
4.5. Luciferase Imaging
HAK5promoter::LUC grown for 11 days were sprayed with luciferin (Duchefa Biochemie, Haarlem, The Netherlands) and kept in the dark for a few minutes prior to imaging. NightSHADE LB 985 (Berthold, Bad Wildbad, Germany) was used to image luciferase chemiluminescence.
In this study, we have determined that JA signaling is involved in Cs+ perception in terms of root growth inhibition, but not in uptake of K+ and Cs+. This growth inhibition by Cs+ occurs presumably through biosynthesis of JAs and consequent stimulation of the downstream JA signaling pathway. In parallel, Cs+ induces expression of a high-affinity K+ transporter gene, HAK5, under the K+ sufficient condition in a JA signaling-independent manner. However, exogenous application of MeJA inhibits Cs+-induced expression of HAK5, suggesting a complicated “fine-tuning” regulation of Cs+ response in plants.
Many thanks to Prof. John Turner (University of East Anglia) for providing coi1-16 seeds, Prof. Tatsuo Kakimoto (Osaka University) for ipt1,3,5,7 and ahk2;3 seeds, Prof. Chi-Kuang Wen (Shanghai Institute for Biological Science, Chinese Academy of Science) for ers1-1 seeds, Dr. Daniel Schachtman (Donald Danforth Plant Science Center) for aux1-7 seeds and Prof. Nicholas Harberd (University of Oxford) for rga-24;gai-t6 seeds. This work was supported by funding from RIKEN and the Ministry of Agriculture, Forestry and Fisheries of Japan (I2012101).
Conflict of Interest
The authors declare no conflict of interest.
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