Genome-wide co-expression analysis predicts protein kinases as important regulators of phosphate deficiency-induced root hair remodeling in Arabidopsis
© Lan et al.; licensee BioMed Central Ltd. 2013
Received: 4 December 2012
Accepted: 20 March 2013
Published: 1 April 2013
Phosphorus (P) is one of the essential but often limiting elements for plants. Based on transcriptional profiling we reported previously that more than 3,000 genes are differentially expressed between phosphate (Pi)-deficient and Pi-sufficient Arabidopsis roots (MCP 11(11):1156–1166, 2012). The current study extends these findings by focusing on the analysis of genes that encode protein kinases (PK) and phosphatases (PP) by mining PK and PP genes that were differentially expressed in response to Pi deficiency.
Subsets of 1,118 and 205 annotated PK and PP genes were mined on the basis of the TAIR10 release of the Arabidopsis genome. Analysis of RNA-seq data showed that 92 PK and 19 PP genes were not detected in roots (zero reads in three biological repeats); 96 PK and 10 PP showed low abundance (≤ 10 reads). Gene ontology analysis revealed that the 188 PK genes with no or low expression level in Arabidopsis roots are mainly involved in pollen recognition, pollen tube growth or other processes not relevant for root hair formation. More than 50% of the cysteine-rich RLK (receptor-like protein kinase) subfamily genes belong to this group. Among the 29 PP genes with no or low expression level, purple acid phosphatases, haloacid dehalogenase-like hydrolases, and PP2C genes with functions in the dephosphorylation of RNA polymerase II C-terminal domain and mRNA capping were enriched. Subsets of 173 PK and 35 PP genes were differentially expressed under Pi-deficient conditions. Putative functional modules (clusters) of these PK and PP genes were constructed based on co-expression analysis using the MACCU toolbox. A co-expression network comprising 65 known or annotated PK and PP genes (60 PK and 5 PP genes, respectively) was subdivided into several highly co-expressed gene sub-clusters. The largest sub-cluster was composed of 22 genes, most of which have been assigned to the RLK superfamily and were associated with cell wall metabolism, pollen tube and/or root hair development and growth.
We here provide comprehensive ‘digital’ transcriptional information on PK and PP genes in Arabidopsis roots. The co-expression network derived from our data mining approach sets the stage for follow-up experimentation that helps to complete our understanding of the post-translational regulation of Pi deficiency-induced changes in root hair morphogenesis.
KeywordsProtein phosphorylation RNA sequencing Co-expression analysis Root hairs Phosphate deficiency
Phosphorous, mainly taken up as phosphate (Pi) by plants, is an essential micronutrient involved in signaling, metabolism and photosynthesis. The bioavailability of Pi is often very low due to its tendency to form complexes with soil cations. In agricultural systems, Pi deficiency is a major cause of severe yield losses in crops and poor quality of edible plant parts. Low Pi availability is often corrected by the application of large quantities of fertilizers, which is associated with environmental pollution and substantial costs. Understanding how plants adapt to low Pi availability is thus mandatory to develop Pi-efficient germplasms. To cope with low Pi availability, plants have evolved an array of adaptive processes aimed at improving Pi uptake and re-mobilization, comprising the acquisition and redistribution of Pi, alterations in developmental programs, and metabolic networks . Proteomic [2–4] and transcriptomic [5–11] profiling studies have uncovered several robustly changed processes in Pi-deficient plants, including the remodeling of lipid metabolism, changes in glycolytic carbon flux, alterations in root development, and rewired signaling pathways [12–14].
The mechanisms underlying the maintenance and recalibration of cellular Pi homeostasis are complex. The Myb-type transcription factor PHOSPHATE STARVATION RESPONSE1 (PHR1) is a central conserved regulator that controls a subset of Pi deficiency genes by binding to an imperfect palindromic sequence motif [15, 16]. Consistent with a critical regulatory role of PHR1 in Pi homeostasis, overexpression of PHR1 led to increased Pi accumulation . The activity of PHR1 is controlled by the SUMO E3 protein ligase SIZ1 , representing the most upstream component of the Pi deficiency signaling cascade identified so far. Another subset of Pi-responsive genes is regulated by the E2 ubiquitin conjugase PHOSPHATE2 (PHO2). A connection between these two central switches is established by MicroRNA399 (MiR399), which systemically controls PHO2 through transcript cleavage [19, 20]. MiR399 itself is strongly induced by Pi deficiency . The sensor for Pi remains to be discovered.
Besides the involvement of protein ubiquitination [18, 21], other posttranslational processes potentially involved in the Pi deficiency response have not been thoroughly investigated. An estimated one-third of all eukaryotic proteins undergoes reversible phosphorylation via protein kinases (PK) and phosphatases (PP), demonstrating the importance of this process. Modifications of protein with phosphate can affect protein structure, activity, localization, interaction, and stability, thereby regulating crucial processes such as metabolism and development. Several hundred genes encoding PKs and PPs were found to be differentially expressed upon Pi deficiency by transcriptional profiling of roots from Pi-deficient plants , suggesting that alterations in protein phosphorylation patterns induced by Pi deficiency are critical in the control of Pi homeostasis. For example, under Pi-limiting conditions the high-affinity phosphate transporterPHT1;1 was found to be induced and newly–synthesized PHT1;1 protein was phosphorylated by an yet unknown PK at the C-terminal 514 amino acid Ser, which is required for the precise localization of PHT1;1 to the plasma membrane .
Transcriptome analysis alone, however, is insufficient for defining potential roles of differentially expressed PKs and PPs genes in Pi homeostasis. Functional characterization of these genes by reverse genetic approaches such as increasing or decreasing their transcript level (by T-DNA insertion and/or RNAi) is required to elucidate their biological functions. However, individually assaying hundreds to thousands of differentially expressed genes without any selection filter would be extremely laborious. Systemic cluster analyses provide a means to filter and select genes of interest for the biological question addressed. Genes showing similar expression pattern under diverse conditions often have correlative functions , and the biological processes in which genes with unknown functions are involved can be predicted based on co-expression data (‘guilt by association’) [24, 25].
In the present study, the global expression of PK and PP genes in Arabidopsis roots was analyzed in order to gain insights into the regulation of the interplay of transcriptional and post-translational responses to Pi deficiency. By mining public databases, PK and PP genes that are differentially expressed upon Pi starvation were clustered into groups of closely correlated modules based on their co-expression under various sets of experimental conditions. Using this approach, we discovered several potentially critical regulatory PKs with roles in root hair development and growth under Pi deficiency.
Results and discussion
Digital information on the expression of protein kinase and phosphatase genes in Arabidopsis roots
Protein kinases and phosphoylases play key roles in regulating nearly all aspects of cellular processes. However, due to the use of microarray probe sets that have significant cross hybridization potential and are unable to distinguish highly similar genes of this subfamily, transcriptional information on the expression of PK and PP genes is incomplete in Arabidopsis. In addition, tissue-specific gene expression information of PKs and PPs is lacking. The RNA-seq technology has proven to provide precise digital information on gene expression, and is able to discriminate genes of high sequence identity . Using this technology, we previously examined global gene expression changes upon Pi deficiency in Arabidopsis roots . Focusing on the expression of PKs and PPs, we mined and re-analyzed our RNA-seq data set (NCBI: SRA050356.1). Based on the PK and PP gene families annotated in the TAIR10 release of Arabidopsis genome, a total of 1,118 PK (GO: 0004672, Additional file 1) and 205 PP (GO: 0004721, Additional file 2) genes was retrieved and compared with the RNA-seq data. We defined a gene as not being expressed if the unique read number was zero in all three biological repeats under normal (Pi-replete) conditions; low abundance of a transcript was defined by a unique read number ≤ 10 in either of the three biological repeats. A gene was defined as being highly expressed in Arabidopsis roots when the read number was higher than 2,000 in either of the three biological repeats. On the basis of these criteria, 92 PK genes were not detected in Arabidopsis roots, transcripts of 96 PK genes were low abundant; and 57 PK genes were highly expressed (Figure 1A and Additional file 3). For the 1,118 PK genes, 432 cognate proteins were identified with at least one uniquely matched peptide ( and Additional file 4). Generally, PK proteins were more likely detected when the associated transcript was highly abundant. However, proteins were also detected from about 20% of the genes with low abundant or absent transcripts (Figure 1C and Additional file 4) confirming the observation that gene expression is not always correlated with protein abundance .
Applying the same criteria used for the PK genes, subsets of 19 and 10 PP genes were not detected or lowly expressed in Arabidopsis roots, respectively (Additional file 7). The trend of PP protein expression was similar to that of PK proteins (Figure 1D and Additional file 4). Among these two subsets, purple acid phosphatases (PAP), haloacid dehalogenase-like hydrolases (HAD), and PP2C genes were enriched, with gene products mainly localized in nucleus and functioning in the biological processes ‘dephosphorylation of RNA polymerase II C-terminal domain’ and ‘mRNA capping’ (Additional file 8). Products of the nine highly expressed PP genes (Additional file 7) were mainly involved in the formation of PP-1 and PP2A complexes associated with the biological processes ‘embryonic root morphogenesis’ and ‘phosphate ion homeostasis’ (Additional file 9). The lack of a transcriptional response of PP genes to Pi deficiency suggest that under normal conditions in Arabidopsis roots cellular Pi homeostasis is regulated by PPs, probably by protein de-phosphorylation. Uncovering the substrates regulated by these PP genes would strongly facilitate our understanding of cellular Pi homeostasis.
Identification of Pi-responsive genes encoding protein kinase and phosphatase in Arabidopsis roots
Although approximately one thousand genes have been identified as being Pi-responsive by using the full-genome Affymetric ATH1 gene chip [5–11], the technical limitations of the microarray technology renders a precise estimation of the changes in the expression of Pi-responsive genes difficult. Using RNA-seq, we defined a total of 3,106 genes as differentially expressed between Pi-sufficient and Pi-deficient Arabidopsis roots . Subsets of 173 PK and 35 PP genes, comprising diverse subfamilies were differentially expressed under Pi-deficient conditions (Additional file 10), some of which have been listed as Pi-responsive genes in earlier microarray studies [5–11]. Among the differentially expressed PK genes, members of the RLK superfamily genes, especially from the LRR-RLK subfamily, and genes from the CDPK-SnRK superfamily were enriched, while members of the PAP and PP-2C families were predominant in the differentially expressed genes encoding PPs. In total, 205 PK and PP genes were finally mined for further analysis. Among them, three genes (At1g49580, At2g01830 and At2g20050) are annotated as harboring both PK and PP activity. Gene ontology analysis revealed that those genes whose products are localized on the plasma membrane, the cell surface, the ER, the cell wall, or are associated with the ubiquitin ligase and calcineurin complexes were highly enriched (P < 0.01; Additional file 11). Purple acid phosphatases, members of the largest class of plant acid phosphatases, are generally assumed to be involved in intra-and/or extra-cellular Pi scavenging and recycling of Pi under Pi-deficient conditions. In Arabidopsis, the PAP family is composed of 29 members sharing conserved domains. Most PAPs are induced by Pi deficiency, some of which in an organ-specific manner [31, 32]. Precise digital expression information of the 29 members of the PAP family in Pi-deficient Arabidopsis rootsis presented by RNA-seq (Additional file 12), which completes gene expression information in Arabidopsis roots so far uncovered by microarray analysis and classic molecular techniques. It is unclear, however, whether the members of the PAP family harbor PP catalytic activity.
Construction of Pi-responsive PK and PP co-expression networks
Co-expression networks of the differentially expressed PK and PP genes were constructed using the MACCU software . Co-expressed genes were selected with a Pearson correlation coefficient cutoff of 0.7. This cutoff also has been used in earlier studies [9, 33]. Co-expression networks constructed with this cutoff are well suited to guide follow-up experiments (i.e. networksare neither too big nor too small). It should be mentioned that the co-expression network constructed here is restricted to roots and the 300 public microarrays mined for generating co-expression relationship were root-related experiments . Because protein regulation by phosphorylation is reversible and requires both PKs and PPs, the network was constructed from both PK and PP genes. The 205 differentially expressed PK and PP genes were loaded as guide genes to calculate the correlations. Correlations between guide genes were visualized by Cytoscape (http://www.cytoscape.org). In the co-expression network, a node represents a gene and an edge represents the correlation between two genes. The network of PK and PP genes responsive to Pi deficiency consists of 65 nodes and 96 edges (Additional file 13). The 65 nodes contain 60 genes that encode PKs and five genes that encode PPs (Additional file 14). The network can further be divided into two larger and seven smaller modules. Genes with similar expression pattern under diverse conditions can have correlative functions and may form a functional module . Only 34% of the input genes were constituents of the co-expression network, suggesting that the majority of PKs and PPs responsive to Pi deficiency are functionally diverse and involved in a variety of biological processes and metabolic pathways. It is noteworthy that, compared to14% of the input PP genes associated with co-expression network, the group of PKs is represented by 34% of the genes, even though the number of differentially expressed PP gene is slightly higher than that of PK genes (35 out of 205 PP genes and 173 out of 1,118 PK genes). Some modules contain only a few or none PP genes. For instance, the largest module contains only one PP gene, PAP11. These observations suggest that the regulation of biological processes may require a cascaded and/or coordinated protein phosphorylation by different PKs to adapt to environmental stresses, while the removal of phosphate from a phosphorylated protein by a PP is less specific. Because of the importance of PK in signaling and metabolism, it is reasonable to speculate that protein phosphorylation is one of the proprietary processes for plant cell to use the limited Pi under Pi deficiency.
Genes involved in unidimensional cell growth form the major module
To gain insight into the function of the genes associated with the network, GO enrichment analyses were performed. The biological processes ‘glycolysis’, ‘negative regulation of anion channels activity by blue light’, ‘unidimensional cell growth’, and ‘glucosinolate biosynthetic process’ were most strongly enriched (Additional file 15). This analysis supports the assumption that protein phosphorylation is an important regulatory level for diverse processes associated with the recalibration of the cellular Pi homeostasis. It has been documented that Pi deficiency alters cellular metabolism, mainly by enhanced carbon flux via glycolysis for increased synthesis of organic acids . Our data support these findings and further suggest that under Pi deficiency protein phosphorylation is an important regulator of glycolytic flux.
Protein kinases involved in pollen tube development and growth are co-expressed in Pi-deficient roots
Genes comprising PKPP1
Mean ± SD (−Pi/+Pi; P < 0.01)
Protein kinase superfamily protein
1.93 ± 0.92
AtPERK12, IGI1, Protein kinase superfamily protein
1.60 ± 0.38
ATCIPK18, ATWL1, CIPK18, SnRK3.20, WL1, CBL-interacting protein kinase 18
1.50 ± 0.45
S-locus lectin protein kinase family protein
1.99 ± 0.51
Leucine-rich repeat protein kinase family protein
3.03 ± 0.79
ANX1, Malectin/receptor-like protein kinase family protein
1.36 ± 0.08
Protein kinase superfamily protein with octicosapeptide/Phox/Bem1p domain
0.65 ± 0.03
AGC (cAMP-dependent, cGMP-dependent and protein kinase C) kinase family protein
3.65 ± 0.62
Protein kinase superfamily protein
2.19 ± 0.47
ATPAP11, PAP11, purple acid phosphatase 11
∞ (De novo synthesis)
Leucine-rich receptor-like protein kinase family protein
0.87 ± 0.04
Protein kinase superfamily protein
1.39 ± 0.02
U-box domain-containing protein kinase family protein
1.33 ± 0.13
U-box domain-containing protein kinase family protein
3.52 ± 0.39
Leucine-rich repeat protein kinase family protein
1.75 ± 0.12
U-box domain-containing protein kinase family protein
6.13 ± 1.12
CPK25, calcium-dependent protein kinase 25
1.39 ± 0.08
RHS10, root hair specific 10
1.43 ± 0.18
AGC1.7, AGC kinase 1.7
1.98 ± 0.44
IRE, AGC (cAMP-dependent, cGMP-dependent and protein kinase C) kinase family protein
1.38 ± 0.25
Protein kinase superfamily protein
1.38 ± 0.13
RSH3, root hair specific 3
1.42 ± 0.17
Protein kinases from the AGC and PERK subfamilies are critical for root hair development and growth under Pi deficiency
Members of sub-module PKPP1B (Figure 3B and Table 1) may play key roles in root hair development and elongation under both normal and Pi-deficient conditions. Three genes in this submodule, including the two root hair-specific genes RHS3 and RHS10 and IRE1 (INCOMPLETE ROOT HAIR ELONGATION 1) , have been related to root hair development and elongation. RHS3 and IRE1 belong to the AGC family while RSH10 belongs to the PERK family, indicating that kinases in these families are particularly important for root hair development and growth. All three genes were induced by Pi deficiency at the transcriptional level. Reverse genetic studies would be of help to decipher their physiological functions under Pi deprivation. Several other genes in this sub-module, including At4g25160, At5g61550, At4g31250, and At2g41970, have been reported to be part of a gene regulatory network comprising 208 root epidermal ‘core’ genes in Arabidopsis . All genes in this sub-module were induced by Pi-deficiency, implicating their involvement in root hair development and growth under Pi starvation. AGC1.7, belonging to AGCVIII subfamily, and its homologue AGC1.5 have been reported to be critical for the polarized growth of pollen tubes , but have not yet been associated with root hair development. Our analysis revealed that AGC1.7 was co-expressed with RSH3 and CPK25 (calcium-independent CDPK ) under Pi deficiency, suggesting that AGC1.7 supports a possible function in root hair development under Pi limiting conditions. The only gene that was repressed by Pi deficiency in the sub-module PKPP1B is CLV1. By binding to a small protein ligand CLV3, CLV1restricts the proliferation and/or promotes the differentiation of stem cells in the shoot apical meristem . Interestingly, RNA-seq analysis revealed that CLV1 was also highly expressed in Arabidopsis roots and decreased in response to Pi deficiency (Table 1), suggesting that CLV1 might be negatively regulating root hair development in response to Pi starvation.
Root epidermial core gene associated with PKs and PPs under Pi deficiency
In summary, we here provide precise digital information on the transcription of protein kinase and phosphatase genes in Arabidopsis roots at a genome-wide level. A root-specific co-expression network of Pi-responsive genes encoding protein kinases and phosphatases has been generated and putative novel players in Pi deficiency-induced root hair formation have been uncovered. Combined with the previously published root hair core genes , a comprehensive inventory for the regulation of root hair development and metabolism was obtained. The approach applied here will be useful to direct further studies by reverse genetic methods and eventually decipher the mechanisms by which root epidermal cells are re-programmed to adapt to Pi deficiency.
Data collection and processing
Transcriptome data of roots from plants grown in the presence or absence of Pi from 13-d-old Arabidopsis seedlings by RNA-seq were downloaded from a public database (NCBI: SRA050356.1) and analyzed as described in . Microarray data of 2,671 ATH1 arrays from the NASCarray database (http://affymetrix.arabidopsis.info/) were downloaded and normalized using the RMA function of the Affy package of the Bioconductor software. Among the 2,671 arrays, 300 root-related arrays were manually identified as described in . PK and PP genes were retrieved on the basis of TAIR 10 release of Arabidopsis genome.
Generation of co-expression networks and modules of Pi-responsive PK and PP genes using the MACCU toolbox
To generate root-specific networks of Pi-responsive PK and PP genes, differentially expressed PK and PP genes in the Arabidopsis roots were obtained using a Student t-test at a P value <0.05. Gene networks were constructed based on 300 publicly available root-related arrays using the MACCU toolbox as described in , with a Pearson correlation threshold of 0.7. The generated co-expression networks were visualized by Cytoscape (http://www.cytoscape.org). If one cluster of genes did not have any connection (without any edges) to any other cluster in the co-expression network, we referred to such a cluster as a module.
Construction of root hair-specific networks of Pi-responsive PK and PP genes
To obtain a root hair cell-specific network of Pi-responsive PK and PP genes, the 208 root epidermal ‘core’ genes were first mined from the datasheet described in . Next, Pi-responsive PK and PP genes involved in the module of pollen tube/root hair development and growth were extracted (bait genes), combined with the genes from the root epidermal ‘core’ (preys), and used for generating co-expression network using the MACCU toolbox with a Pearson correlation threshold of 0.7. The resulting networks shows only those nodes (genes) and edges (relationships between genes) that were linked by at least one edge must with bait. Edges linked to two preys were excluded.
The study was partially supported by the starting career grant from the Institute of Soil Science, Chinese Academy Sciences (Y225070000). We thank Drs. Wen-Dar Lin and Jorge Rodríguez Celma for their help in using the MACCU software and two anonymous reviewers for their valuable comments.
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