Analysis of peptide PSY1 responding transcripts in the two Arabidopsis plant lines: wild type and psy1r receptor mutant
© Mahmood et al.; licensee BioMed Central Ltd. 2014
Received: 20 December 2013
Accepted: 20 May 2014
Published: 6 June 2014
Small-secreted peptides are emerging as important components in cell-cell communication during basic developmental stages of plant cell growth and development. Plant peptide containing sulfated tyrosine 1 (PSY1) has been reported to promote cell expansion and differentiation in the elongation zone of roots. PSY1 action is dependent on a receptor PSY1R that triggers a signaling cascade leading to cell elongation. However little is known about cellular functions and the components involved in PSY1-based signaling cascade.
Differentially expressed genes were identified in a wild type plant line and in a psy1r receptor mutant line of Arabidopsis thaliana after treatment with PSY1. Seventy-seven genes were found to be responsive to the PSY1 peptide in wild type plants while 154 genes were responsive in the receptor mutant plants. PSY1 activates the transcripts of genes involved in cell wall modification. Gene enrichment analysis revealed that PSY1-responsive genes are involved in responses to stimuli, metabolic processes and biosynthetic processes. The significant enrichment terms of PSY1-responsive genes were higher in psy1r mutant plants compared to in wild type plants. Two parallel responses to PSY1 were identified, differing in their dependency on the PSY1R receptor. Promoter analysis of the differentially expressed genes identified a light regulatory motif in some of these.
PSY1-responsive genes are involved in cellular functions and stimuli responses suggesting a crosstalk between developmental cues and environmental stimuli. Possibly, two parallel responses to PSY1 exist. A motif involved in light regulation was identified in the promoter region of the differentially expressed genes. Reduced hypocotyl growth was observed in etiolated receptor mutant seedlings.
KeywordsCellular functions Gene enrichment analysis Microarray Signaling cascade Small signaling peptides
In the past few years, our understanding of signals required for cell-to-cell communication during plant development has increased tremendously. Identification of components that mediate signaling serves as a landmark in understanding the mechanism of cell-to-cell communication in planta. Several components such as phytohormones, mobile transcription factors, mobile small RNAs and peptides serve this purpose [1, 2]. Phytohormones are lipophilic compounds which are active at very low concentrations and involved in plant growth ranging from embryogenesis to senescence . Similarly, small-secreted peptides are now emerging as growth regulators and many of them are involved in basic functions of cell growth and development. More than 1000 genes are annotated as encoding putatively secreted peptides in the Arabidopsis genome but very few are known to be involved in specific cellular signaling [2, 3]. However, the precise role and mechanism proceeded by secreted peptides is yet to be established. Secreted peptides have now been recognized as a new class of intracellular signal molecules, which coordinate and specify cellular functions in plants. As a new class of intracellular signal molecules, the role of these secreted peptides could be explored further.
Plant cells transduce signals utilizing surface receptors binding to ligands present in the apoplast . The S-locus receptor ZmPK1 from Maize was the first receptor kinase identified in plants , and many receptors have been identified in plants ever since [6, 7]. Signaling molecules can elicit different signaling pathways, and a single receptor can also respond to more than one signal molecule . Perception of signal molecules , and adjustability to different environmental conditions  are interesting characteristics of these signaling cascades. Plants demonstrate different growth patterns under different environmental conditions owing to asymmetric elongation or cell division [11–14]. They also exhibit flexibility in the size and numbers of produced organs to ensure diversity and specificity in perception of external stimuli [1, 2, 10–15].
Plant peptide containing sulfated tyrosine (PSY1) is a tyrosine-sulfated peptide isolated from Arabidopsis cell suspension medium . It promotes cell expansion and differentiation in the elongation zone of roots at nanomolar concentration. This 18-amino acid glycopeptide is derived from a 75-amino acid precursor polypeptide containing an N-terminal signal peptide . PSY1 is believed to bind the extracellular domain of Leucine rich Repeat Receptor Like Kinase (LRR-LK), which is named as a receptor of PSY1 (PSY1R). PSY1 and its receptor PSY1R are expressed throughout the whole plant with higher expression in shoot apical meristem and elongation zone of roots. PSY1 is known to be highly up-regulated after wounding . Exogenous application of purified PSY1 peptide to suspension cell culture induces cellular proliferation, expansion and elongation while overexpression of Arabidopsis PSY1 causes longer roots with larger cotyledon as compared to wild type . Recently, receptor PSY1R and peptide PSY1 were found to be involved in plant defense [17, 18]. The PSY1R might integrate growth promotion and defense signals leading to modulation of cellular plasticity, and may allow the cells to adjust towards environmental changes.
In order to understand the role of PSY1 and its receptor PSY1R, a full genome microarray study was performed. Identification of genes responding to PSY1 is a bottleneck in explaining the specific signaling phenomenon. This is the first comprehensive study to elucidate components of the PSY1-based signaling cascade using full genome microarray in response to exogenously applied PSY1. We found that several genes, involved in plethora of physiological functions, are differentially expressed after PSY1 exposure. Our study indicates that two PSY1 responses exist. The promoter analysis leads to identification of a light regulatory motif in differentially expressed genes of psy1r mutant plants.
Results and discussion
Genome wide analysis of two plant lines after PSY1 treatment and validation of microarray data
Identification of enriched GO terms of differentially expressed genes in both plant lines
In the PSY1-treated psy1r mutant plants, 62 GO terms were found according to biological component (BP) and these numbers were higher in the PSY1-treated psy1r mutant plants than in untreated psy1r mutant plants. GO terms lacking in the untreated psy1r mutant is “response to auxin stimulus” and “cellular amino acid metabolic processes”. No differences were observed according to cellular component. When comparing molecular function GO terms of PSY1-treated and untreated psy1r plants, most prominent difference is the carboxylesterase activity observed in peptide-treated plants. This enzyme activity is completely absent in the untreated mutant plant line. These differences encouraged a more comprehensive analysis of differentially expressed genes in the two plant lines.
Receptor dependent and independent response to peptide PSY1
Interestingly, when analyzing the over-represented GO categories it is found that the PSY1R-independent pathway represents the cell wall modifications (hydrolase activity), while the PSY1R-dependent pathway represents the response to stimuli, regulation of transcription, metal ion transport, flower development and response to abscisic acid stimulus.
Identification of light-responsive ciselements in promoters of differentially expressed genes
Putative cis-regulatory motives statistically over-represented in the promoters of differentially expressed genes
PSY1 responsive genes in wild type (77 genes)
Differentially expressed genes in psy1rmutant plants (154 genes)
Differentially expressed genes in PSY1 treated wild type plants compared to PSY treated psy1rmutant plants (261 genes)
Hits out of 77 genes
Hits out of 154 genes
Hits out of 261 genes
Small signaling peptides perceived by receptors are situated in specific cells to control growth and development by eliciting a vast array of physiological responses. PSY1 is a secreted peptide and its action is dependent on a receptor PSY1R that triggers a signaling cascade leading to cell elongation. However, the targets of this signaling pathway are yet to be studied in detail. Our work revealed that addition of exogenous PSY1 leads to transcription of cell wall modifying enzymes, enzymes that might contribute to the loosening of the cell wall during elongation. Two parallel responses to PSY1 were found to exist (PSY1R-dependent and PSY1R-independent). This could suggest that other receptors for PSY1 peptides exist within the plant. PSY1-responsive genes encode several genes localized in cell wall that regulate carboxylestrase activity, while differentially expressed genes in psy1r mutant plants largely were localized to the nucleus with molecular function of ion binding and transcription factor activity. A major part of PSY1-responsive genes were involved in cell growth, cell differentiation and catabolic processes. Genome wide gene expression profiling based on GO revealed that most differentially expressed genes were involved in cellular functions and response to stimuli. This suggests a crosstalk between developmental cues and environmental stimuli. A promoter analysis revealed a specific cis-element present in 9% of the differentially expressed genes of psy1r mutant plants. This element has previously been found in genes regulated by light. Elongation growth of hypocotyls is closely linked to light and one can speculate that PSY1R is involved in the regulation of light response.
Plant material and growth conditions
Experiments with Arabidopsis thaliana were performed on ecotype Columbia-0. Twenty-five milligram (mg) of seeds of two plant lines (wild type and psy1r knockout) were surface sterilized in a micro-centrifuge tube by treating them with ethanol and subsequently Klorin containing 0.2% tween for 10 min. Seeds were then washed again with ethanol for 10 min and rinsed with sterile water twice before subjecting them to imbibition and stratification at 4°C for three days. After stratification, seeds of the two plant lines were grown hydroponically.
Nutrient solution of hydroponic culture containing half strength of Murashige and Skoog medium (MS) with 1% (w/v) sucrose was prepared (pH 5.7, KOH) and sterilized by autoclaving. The stratified seeds of the two plant lines were grown in 500 mL-conical flasks containing 250 mL nutrient solution. Flasks were placed in a growth chamber on a shaker at 180 rpm under continuous light and sterilized conditions. The purified, natural PSY1 was obtained from Yoshikatsu Matsubyashi Lab, National Institute for basic biology, Japan and PSY1 applied to seedlings as described by Amano et al . After one week, plants were treated with the PSY1 peptide at 10 nM concentration for 4 hrs and then transferred into liquid nitrogen and stored at -80°C until RNA extraction.
RNA extraction and microarray
Total RNA was extracted from three biological replicates of 25 mg seedlings grown in hydroponic culture in sterile conditions using the RNeasy Plant mini kit (Qiagen). RNA integrity was assessed using an Agilent 2100 Bioanalyser with RNA 6000 Nano Assay (Agilent Technologies) and was processed for use on Arabidopsis (V4) Gene Expression Microarray (Agilent Technologies). Arabidopsis (V4) Gene Expression Microarray was used for RNA analysis according to manufacturer’s detail (Design ID: 21169, G2519F; Agilent Technologies, Palo Alto, CA, USA). Briefly, 200 ng of total RNA containing RNA spiked in Mix was reverse transcribed in to cDNA that was then in vitro transcribed into cRNA, labeled with cyanine 3-CTP using Agilent Low RNA Input Linear Amp Kit (Agilent Technologies). The Agilent RNA spike-in control targets are a set of 10 in vitro-synthesized poly-adenylated transcripts derived from the adenovirus E1A gene used to monitor the labeling reactions and the microarray performance. For labeled cRNA purification, 84 μl sterile H2O, 350 μl RLT buffer from Qiagen RNAeasy Mini Kit (Qiagen Technologies), and 250-μl EtOH were added. The purification steps followed the protocol described by the manufacturer.
After obtaining the required cRNA yield and incorporation rate of fluorescent dye cyanine 3-CTP, a hybridization step was carried out simultaneously for all three biological repeats. Hybridizations were carried out in Agilent’s SuperHyb Hybridization Chambers (Agilent Technologies) containing 5 μg of cyanine 3-labeled linearly amplified cRNA. The hybridization reaction was performed at 65°C for 17 hours using the Agilent DNA microarray hybridization oven (Agilent Technologies), following procedures described in the Agilent One-Color Microarray-Based Gene Expression Analysis protocol. The hybridized microarrays were disassembled in Agilent Gene Expression Wash Buffer 1 (Agilent Technologies) and then washed with the same buffer for 1 min at room temperature, followed by washing with Gene Expression Wash Buffer 2 for one min at 37°C. The microarrays were then scanned immediately using the Agilent DNA Microarray Scanner (Agilent Technologies). The images generated were analyzed with Agilent Feature Extraction Software. The raw data of hybridization was imported into the microarray analysis software GeneSpring 11.5 (Agilent Technologies). Normalization and background intensity determination for each feature performed using the Robust Multiarray Average summarization algorithm, as described by Irizarry et al. . Genes were considered differentially regulated if their normalized expression value was significantly different from the control (P < 0.05). One-way ANOVA with Benjamini Hochberg multiple testing corrections (false discovery rate of 0.05) was used to identify genes differentially regulated between treatment groups. Genes exhibiting more than a 2-fold enhanced or reduced transcription level in three independent experiments were considered to show significant alterations in expression.
Real time PCR
Aliquots of RNA samples used for the microarray analysis were also analyzed by real-time RT-PCR. Reverse transcription (RT) was performed with 2 μg of total RNA to obtain cDNA with SuperScript II and Oligo (dT)12-18 (Invitrogen) as the primer in a 20 μl reaction volume. Each cDNA sample was diluted 1:4 in sterile ddH2O, and 1 μl of this dilution was used as template for qPCR. Primers for the PCR reactions were designed by Beacon Designer™ to have a Tm of ~ 60°C and an optimal annealing temperature of 53–55°C with the length of the amplicons between 120 and 300 bp. Real-time PCR was performed with DyNAmo™ Flash SYBR® Green qPCR Kit (Qiagen) in 20 μL reactions according to manufacturer’s instruction. Each PCR reaction contains 5 μl of diluted cDNA (100 ng), 5 μl (0.5 μM) of both primers and 10 μl of DyNAmo™ Flash SYBR® Green master mix. The initial denaturing time was 7 min at 95°C, followed by 45 cycles consisting of 95°C for 10 s, 57°C for 15 s, 68°C for 30 s and 75°C for 1 s with a single fluorescence measurement. Then it was held at 60°C for 60s. A melting curve analysis of the generated products (65°C–95°C with a heating rate of 1°C s-1 and a continuous fluorescence measurement) was performed after the PCR cycles.
ACT2 (AT3G18780) was selected as a valid housekeeping gene since the expression of ACT2 did not change significantly in plant lines treated with the PSY1 peptide compared to untreated plant lines (Additional file 6: Figure S1). In addition to this, no significant changes in expression of ACT2 could be observed in the microarray data further demonstrating that the ACT2 expression is unaffected by the PSY1 peptide treatment. For relative quantification, amplification efficiencies (E) for primer set targeting each gene were determined in the following way: an aliquot of cDNA transcribed from 5 μg of total RNA was diluted with sterile ddH2O to 10-1, 10-2 and 10-3. Standard curves for each gene were performed using the undiluted and diluted cDNA to cover the range of all template concentrations. The specific primers for each gene were used. Gene-specific PCR efficiency was used to calculate the expression of target genes relative to the expression of ACT2 reference gene. The ∆CT value was calculated as follows: ∆CT (target genes) = CT (target gene)- CT (Reference gene), where CT is the cycle number at which PCR product exceeded a set threshold. Relative transcript level (RTL) was calculated through = 1× 2-∆CT.
Gene ontologies were analyzed for term enrichment using the AgriGO Single Enrichment Analysis tool with TAIR10 GO annotation (http://bioinfo.cau.edu.cn/agriGO/). GO enrichment was performed in AgriGO (FDR correction and Fisher’s exact test < 0.05) using the whole Arabidopsis genome as the background/reference.
Hypocotyl length measurements in dark grown plants
Seedlings of psy1r and wild type plants were grown on MS medium (0.8% (w/v) agar and 1% (w/v) sucrose) at 22°C for 5 days. Seedlings were transferred to transparencies, scanned and measured using the application ImageJ for hypocotyl length measurements.
Availability of supporting data
The data sets supporting the results of this article are included within the article (and its additional files along with list of genes). Raw microarray data were deposited to GEO public database and available under the accession number “GSE55684”. (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE55684).
Plant peptide containing sulfated tyrosine 1
Receptor of plant peptide containing sulfated tyrosine 1
Leucine rich repeat receptor like kinase
Real time polymerase chain reaction
Murashige and Skoog medium
Relative transcript level
Singular enrichment analysis
Analysis of variance.
The projected was supported by a grant from the Danish Research Foundation, FNU, #272-08-0504 (to ATF) and by the PUMPkin Centre - a Centre of Excellence funded by the Danish National Research Foundation.
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