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Early transcriptomic response to Fe supply in Fe-deficient tomato plants is strongly influenced by the nature of the chelating agent.

ABSTRACT: It is well known that in the rhizosphere soluble Fe sources available for plants are mainly represented by a mixture of complexes between the micronutrient and organic ligands such as carboxylates and phytosiderophores (PS) released by roots, as well as fractions of humified organic matter. The use by roots of these three natural Fe sources (Fe-citrate, Fe-PS and Fe complexed to water-extractable humic substances, Fe-WEHS) have been already studied at physiological level but the knowledge about the transcriptomic aspects is still lacking.The (59)Fe concentration recorded after 24 h in tissues of tomato Fe-deficient plants supplied with (59)Fe complexed to WEHS reached values about 2 times higher than those measured in response to the supply with Fe-citrate and Fe-PS. However, after 1 h no differences among the three Fe-chelates were observed considering the (59)Fe concentration and the root Fe(III) reduction activity. A large-scale transcriptional analysis of root tissue after 1 h of Fe supply showed that Fe-WEHS modulated only two transcripts leaving the transcriptome substantially identical to Fe-deficient plants. On the other hand, Fe-citrate and Fe-PS affected 728 and 408 transcripts, respectively, having 289 a similar transcriptional behaviour in response to both Fe sources.The root transcriptional response to the Fe supply depends on the nature of chelating agents (WEHS, citrate and PS). The supply of Fe-citrate and Fe-PS showed not only a fast back regulation of molecular mechanisms modulated by Fe deficiency but also specific responses due to the uptake of the chelating molecule. Plants fed with Fe-WEHS did not show relevant changes in the root transcriptome with respect to the Fe-deficient plants, indicating that roots did not sense the restored cellular Fe accumulation.

SUBMITTER: Zamboni A

PROVIDER: S-EPMC4705743 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Early transcriptomic response to Fe supply in Fe-deficient tomato plants is strongly influenced by the nature of the chelating agent.

Zamboni Anita A Zanin Laura L Tomasi Nicola N Avesani Linda L Pinton Roberto R Varanini Zeno Z Cesco Stefano S

BMC genomics 20160107

<h4>Background</h4>It is well known that in the rhizosphere soluble Fe sources available for plants are mainly represented by a mixture of complexes between the micronutrient and organic ligands such as carboxylates and phytosiderophores (PS) released by roots, as well as fractions of humified organic matter. The use by roots of these three natural Fe sources (Fe-citrate, Fe-PS and Fe complexed to water-extractable humic substances, Fe-WEHS) have been already studied at physiological level but t ...[more]

PMID: 26742479

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Project description:The mechanisms associated with the regulation of iron (Fe) homeostasis have been extensively examined, however, epigenetic regulation of these processes remains largely unknown. Here, we report that a naturally occurring epigenetic mutant, Colorless non-ripening (Cnr), displayed increased Fe-deficiency responses compared to its wild-type Ailsa Craig (AC). RNA-sequencing revealed that a total of 947 and 1,432 genes were up-regulated by Fe deficiency in AC and Cnr roots, respectively, while 923 and 1,432 genes were, respectively, down-regulated. Gene ontology analysis of differentially expressed genes showed that genes encoding enzymes, transporters, and transcription factors were preferentially affected by Fe deficiency. Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis revealed differential metabolic responses to Fe deficiency between AC and Cnr. Based on comparative transcriptomic analyses, 24 genes were identified as potential targets of Cnr epimutation, and many of them were found to be implicated in Fe homeostasis. By developing CRISPR/Cas9 genome editing SlSPL-CNR knockout (KO) lines, we found that some Cnr-mediated Fe-deficiency responsive genes showed similar expression patterns between SlSPL-CNR KO plants and the Cnr epimutant. Moreover, both two KO lines displayed Fe-deficiency-induced chlorosis more severe than AC plants. Additionally, the Cnr mutant displayed hypermethylation in the 286-bp epi-mutated region on the SlSPL-CNR promoter, which contributes to repressed expression of SlSPL-CNR when compared with AC plants. However, Fe-deficiency induced no change in DNA methylation both at the 286-bp epi-allele region and the entire region of SlSPL-CNR gene. Taken together, using RNA-sequencing and genetic approaches, we identified Fe-deficiency responsive genes in tomato roots, and demonstrated that SlSPL-CNR is a novel regulator of Fe-deficiency responses in tomato, thereby, paving the way for further functional characterization and regulatory network dissection.

Project description:IntroductionPlants respond to water stress with a variety of physiological and biochemical changes, but their response varies among species, varieties and cultivars. Waterlogging in tomato reduces plant growth, degrade chlorophyll and increase concentration of oxidative parameters. Priming can alleviate stress in plants caused by waterlogging enabling plants to be more tolerant to an additional stress in the current or even subsequent generation. The aim of this study was to evaluate tomato genotypes for their sensitivity to waterlogging stress applied during early vegetative growth and at full flowering stage.Materials and methodsThe study included two local genotypes, Trebinjski sitni (GB1126) and Žuti (GB1129), and the reference variety Novosadski jabučar (NJ), which is the variety most commonly used in Serbia and Bosnia and Herzegovina. The activity of class III peroxidase (POX), hydrogen peroxide (H2O2) content and malondialdehyde (MDA) content were measured spectrophotometrically, and for quantification of individual phenolic compounds, targeted approach was adopted, using UHPLC/DAD/(-)HESI-MS2 instrument (Dionex UltiMate 3000 UHPLC system with a DAD detector, configured with a triple quadrupole mass spectrometer TSQ Quantum Access Max (Thermo Fisher Scientific, Germany)).Results and discussionOxidative parameters (H2O2 and MDA) exhibited an increase in content in leaves of tomato plants that underwent waterlogging stress compared to control plants. Moreover, oxidative parameters showed positive correlation with proteins and phenolics content. The obtained correlations can indicate that one of the response strategies of tomato plants to waterlogging is the increased synthesis of proteins and phenolic compounds. The POX activity was not correlated with other parameters except with the polyphenols. A positive correlation was shown between POX activity and the content of phenolic compounds, indicating their independent roles in the removal of ROS. Changes in the phenolic profiles after the exposure of plants to waterlogging stress are recorded, and these changes were more severe in leaves and fruits of GB1129 and NJ genotypes than in GB1126. Thus, genotype GB1126 is the most efficient in maintaining the phenolic profiles of leaves and fruits, and therefore of the nutritive and organoleptic qualities of fruits following the exposure to waterlogging. Also, genotype GB1126 exhibited the ability to maintain the content of oxidative parameters during waterlogging at certain growth stages, implying certain waterlogging tolerance.ConclusionWaterlogging triggered stress memory but not at all growth stages. The most pronounced stress memory was obtained in fruit samples in the phase of full fruit maturity on the 1st truss. This study shed light on the defense mechanisms of tomato plants to repeated waterlogging stress from the perspectives of the changes in the composition of major phenolics, and pointed to the 5-O-caffeoylquinic acid and rutin as the chemical markers of the waterlogging stress tolerance in tomato. However, it remains to be determined whether this modulation has a positive or negative effect on the overall plant metabolism. Further investigations are needed to fully elucidate the benefits of waterlogging pretreatment in this context.

Dataset Information

Early transcriptomic response to Fe supply in Fe-deficient tomato plants is strongly influenced by the nature of the chelating agent.

Publications

Early transcriptomic response to Fe supply in Fe-deficient tomato plants is strongly influenced by the nature of the chelating agent.

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