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Genome-wide identification and in silico characterization of major RNAi gene families in date palm (Phoenix dactylifera)

BMC Genomic Data volume 25, Article number: 31 (2024) Cite this article

Abstract

Background

Dates contain various minerals that are essential for good health. The major RNA interference (RNAi) gene families play a vital role in plant growth and development by controlling the expression of protein-coding genes against different biotic and abiotic stresses. However, these gene families for date palm are not yet studied. Therefore, this study has explored major RNAi genes and their characteristics in date palm.

Results

We have identified 4 PdDCLs, 7 PdAGOs, and 3 PdRDRs as RNAi proteins from the date palm genome by using AtRNAi genes as query sequences in BLASTp search. Domain analysis of predicted RNAi genes has revealed the Helicase_C, Dicer_dimer, PAZ, RNase III, and Piwi domains that are associated with the gene silencing mechanisms. Most PdRNAi proteins have been found in the nucleus and cytosol associated with the gene silencing actions. The gene ontology (GO) enrichment analysis has revealed some important GO terms including RNA interference, dsRNA fragmentation, and ribonuclease_III activity that are related to the protein-coding gene silencing mechanisms. Gene regulatory network (GRN) analysis has identified PAZ and SNF2 as the transcriptional regulators of PdRNAi genes. Top-ranked 10 microRNAs including Pda-miR156b, Pda-miR396a, Pda-miR166a, Pda-miR167d, and Pda-miR529a have been identified as the key post-transcriptional regulators of PdRNAi genes that are associated with different biotic/abiotic stresses. The cis-acting regulatory element analysis of PdRNAi genes has detected some vital cis-acting elements including ABRE, MBS, MYB, MYC, Box-4, G-box, I-box, and STRE that are linked with different abiotic stresses.

Conclusion

The results of this study might be valuable resources for the improvement of different characteristics in date palm by further studies in wet-lab.

Peer Review reports

Introduction

RNA interference (RNAi) is a common mechanism in which numerous forms of RNA molecules affect the expression of protein-coding genes at the transcriptional or post-transcriptional levels that influences different characteristics of plant including development, growth, stress responses, and antimicrobial defense [1]. This mechanism occurs in three pathways known as micro-RNA (miRNA), endogenous small interfering RNA (siRNA), and PIWI-interacting RNA (piRNA) biogenesis [2]. It is used as a tool for controlling gene expression and investigating gene function on a whole-genome scale [3,4,5,6,7,8]. The major RNAi genes are known as argonaute (AGO), RNA-dependent RNA polymerase (RDR), and Dicer-like (DCL) genes/proteins [9]. The RNAi mechanism is initiated by partially double-stranded stem-loop RNA or double-stranded RNA (dsRNA), which is cleaved into 21-24-nt short RNA (sRNA) duplexes by DCL [10]. Dicer endonucleases is a central component in the biogenesis of sRNA molecules [11]. AGO is an essential part of the RNA-induced silencing complex (RISC) [12] and RDR plays a key role in synthesizing dsRNAs from an RNA template [13]. The number of RNAi genes in the DCL, AGO, and RDR families in plants varies by species variations, such as 20 genes in Arabidopsis [14] and cucumber [15], 51 genes in Brassica species [16], 28 genes in maize [17] and tomato [18], 32 genes in rice [19], 19 genes in barley [20], 38 genes in foxtail millet [21], 22 genes in grapevine [22] and pepper [23], 25 genes in sweet orange [9], 36 genes in sugarcane [24], and 31 genes in tea [25] have been identified [26].

RNAi genes perform different biological activities in plants by controlling microbial (RNA and DNA viruses, viroids, insects, and, more recently, fungal diseases) stresses, expression of protein coding genes and chromatin condensation into heterochromatin [27,28,29,30,31,32,33,34,35,36]. Most plants contain four DCLs, with DCL1 causing microRNA synthesis and DCL2, DCL3, and DCL4 essential for 22-, 24-, and 21-nucleotide small interfering RNA (siRNA) biogenesis, respectively [37]. The DCL2 and DCL4 have roles in the creation of transacting siRNA, while DCL2 is primarily responsible for the generation of various-sized secondary siRNAs [38]. The integrated actions of DCL2, DCL3, and DCL4 play a vital role in disease response and protection [39]. The AGO1 is sensitive to virus attacks, confirming the concept that in plants, PTGS represents a defense system against viruses [40]. The AGO2 gene is activated in response to the presence of turnip crinkle virus (TCV) and cucumber mosaic virus (CMV) [41]. The RDR6 plays a significant role in RNA silencing processes [42] and all RDRs have an impact on plant development and stress responses [43]. The exogenously injected VICE12-dsRNA targets the VICE12 gene of apple scab fungus to inhibit its growth and conidial spore formation via the RNAi mechanism [44]. The transgenic tomato plant has been developed by applying the RNAi mechanism using exogenously injected CopE/TLR6-dsRNAs, resulting in a greater mortality rate for western flower thrips (WFT) than wild-type tomato plants when fed to WFT [45].

The date palm trees are ancient Asian and African trees that are farmed for their delicious, edible and medicinal value [46]. One of the most nutritious fruits in the Middle East and North Africa is the date fruit [47]. There are more than 100 million date palm trees in the world [48]. It is well-known for its significant nutrients, dietary fiber, natural antioxidants and sources of rich bioactive compounds that are useful in the treatment of neurological diseases and cancer [49]. Moreover, date fruits are source of carbohydrates, alkaloids, fatty acids (palmitic, linoleic, lauric, and stearic acid), vitamins, carotenoids, flavonoids, polyphenolic compounds, and tannins, as well as other nutrients such as calcium, magnesium, potassium, and phosphorus [50]. Date palm harvest in the world has risen from 4.60 to 8.52 million tons from 1994 to 2018 (FAO. 2020). Date palm pollen is high in bioactive substances with phytochemical and nutritional properties, which could boost anti-infertility capabilities [51]. Date fruit flesh, peel, and pits have anti-mutagenic, hepatoprotective, anti-inflammatory, anti-diabetic, anti-bacterial, anti-viral, anti-fungal, anti-tumor, nephroprotective, heart disease protective, and anti-cancer characteristics [26]. Worldwide, up to 50% newly planted date palm trees and fruits are lossing due to the pathogenic infections and other environmental stresses [52,53,54]. To improve this situation, RNAi genes may play a vital role according to the literature review. However, so far, there has been no information regarding these major RNAi gene families in the economically important date palm. Therefore, this study aimed to gather extensive information on the major RNAi gene families (DCL, AGO, and RDR ) that may contribute to the growth and development of date palm.

Materials and methods

The data source and descriptions

To explore PdRNAi proteins (DCL, AGO, and RDR) from the date palm (Phoenix dactylifera) genome, we have considered its genome/proteome sequences from the National Center for Biotechnology Information (NCBI) database [55, 56] with GenBank accession number: GCA_009389715.1 (NCBI taxonomy ID: 42,345, BioSample: SAMN05011615, weblink: https://www.ncbi.nlm.nih.gov/genome/?term=Phoenix+dactylifera). This dataset has been utilized in comparative genomics study to identify male (Y) and female (X) chromosomes in date palm [57]. It has also been utilized in transcriptomics and genome-wide association studies [58, 59]. In this study, this genome dataset has been utilized to explore PdRNAi proteins by BLASTP search with the query sequences of A. thaliana RNAi (AtRNAi) proteins. Total 17 of 20 AtRNAi proteins (4 AtDCL, 10 AtAGO, and 3 AtRDR) sequence has been downloaded from the Arabidopsis Information Resource (TAIR) database that has been developed by P. Lamesch et al. (https://www.arabidopsis.org/) [60].

Integrated bioinformatics analyses

The integrated bioinformatics studies include BLASTP search, multiple sequence alignment (MSA), phylogenetic tree modeling, functional domain analysis, exon-intron structure of predicted PdRNAi of date palm, subcellular location, GO analysis, TFs analysis, CAREs analysis and miRNA analysis.

Identification of PdRNAi proteins

Exploring PdRNAi proteins by BLASTP serach

The date palm genome from the NCBI database has been analyzed using the basic local alignment search algorithm for proteins (BLASTP) [61] to explore PdRNAi genes. The protein sequences of RNAi genes have been retrieved using query coverage (≥ 50%) and E-values (0.00) [9, 62]. However, only the top-scorer aligned sequences have been considered as the sequences of PdRNAi genes. The genomic length, protein ID, CDS length, and encoded protein length of PdRNAi genes have been retrieved from the NCBI database. The molecular weight, pI, and GRAVY of PdRNAi protein sequences have been calculated using ExPASy [63].

Phylogenetic tree construction among PdRNAi and AtRNAi proteins to fix the names of PdRNAi proteins

The MSAs of the expected PdRNAi protein sequences have been constructed using the Clustal-W [64] method and the MEGAX [65] package. By performing phylogenetic tree analysis on the PdRNAi genes using the Neighbor-joining technique [66], 1,000 bootstrap repetitions [67] have been utilized to confirm the evolutionary connection. The evolutionary distances have been determined using the equal input technique [68].

Charaterization of PdRNAi

Conserved domains and motifs analysis of PdRNAi proteins with respect to AtRNAi proteins

Pfam has been used to search conserved domains in protein sequences [69]. The TBtools (a Toolkit for Biologists integrating various biological data-handling tools) has been used to display the Pfam’s result [70]. The conserved domains have been retrieved from the Pfam database to examine the PdRNAi proteins functional domains. We have investigated the conserved motifs in all of the anticipated PdDCL, PdAGO, and PdRDR proteins using the Multiple Expectation Maximization for Motif Elicitation (MEME) webtool [71]. The TBtools have been used to display the motif’s result [70].

PdRNAi genes structures with respect to AtRNAi genes

We have been used the Gene Structure Display Server (GSDS 2.0) to determine the gene structure of the anticipated PdRNAi genes [72]. The structure of the targeted genes of date palm has been compared with the A. thaliana gene structure through the exon-intron composition.

Sub-cellular localizations of PdRNAi proteins with respect to AtRNAi proteins

The subcellular location of reported PdRNAi proteins in the cell has been investigated by subcellular location analysis. The web tool WoLF PSORT has been used to predict the subcellular location of the targeted proteins [73]. We have been used the TBtools program to display the result [70].

Functional enrichment analysis of PdRNAi proteins

The Gene Ontology (GO) analysis has been carried out using an online database PlantTFDB to confirm the participation of PdRNAi proteins in biological processes (BPs) and molecular functions (MFs) terms [74]. The p-values has been calculated using Fisher’s exact test with Benjamini-Hochberg adjustments. We have considered a GO term with a p-value < 0.05 as statistically significant.

PdRNAi gene regulatory network analysis

In this study, the associated TF families of the PdRNAi genes in date palm has been analyzed using PlantTFcat, a widely used plant transcription factor database [75]. The regulatory network and sub-network has been constructed by integrating TFs and PdRNAi genes and analyzed using Cytoscape 3.9.0 [76]. From the network, we have identified the hub genes and related major hub TFs of PdRNAi based on the degree of connectivity. Cis-element analysis has been done by Plant CAREs [77] database. We have used the Plant miRNA ENcyclopedia (PmiREN) to download date palm mature_miRNA_expression and mature_miRNA_sequence [78]. After that, we have used Plant sRNA target (psRNATarget) [79] to identify the mature_miRNA_expression and mature_miRNA_sequence IDs that corresponded to our predicted PdRNAi genes. The TBtools program has been used to display this data [70]. The detailed pipeline of this study is given in Fig. 1.

Fig. 1
figure 1

The outline of this study

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Results

Identification of PdRNAi proteins

We have identified four DCL, seven AGO, and three RDR proteins from the date palm genome by top-scorer aligned sequences (Table 1). Therefore, we have considered these 14 PdRNAi proteins for further investigation. For the convenience of presentation, we have denoted P. dactylifera RNAi protein families as PdDCL, PdAGO, and PdRDR and A. thaliana RNAi protein families as AtDCLs, AtAGOs, and AtRDRs.

Table 1 Basic information of predicted DCL, AGO, and RDR protein families of P. dactylifera (Pd)
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Thereafter, we performed MSAs of PdRNAi and AtRNAi proteins to construct the phylogenetic tree. After that, we have built the phylogenetic tree based on the aligned sequences of the PdRNAi and AtRNAi protein families (Fig. 2). The names of 14 PdRNAi proteins have been denoted as 4 PdDCLs proteins (PdDCL-1, PdDCL-3a, PdDCL-3b, PdDCL-4), 7 PdAGOs proteins (PdAGO-1, PdAGO-2,3, PdAGO-4,8,9, PdAGO-5, PdAGO-6, PdAGO-7, PdAGO-10), and 3 PdRDRs proteins (PdRDR-1, PdRDR-2, PdRDR-6) based on the sequence similarity to AtRNAi proteins.

Fig. 2
figure 2

The combined phylogenetic tree. In this tree, the PdRNAi (PdDCLs, PdAGOs, and PdRDRs) and the model plant AtRNAi (AtDCLs, AtAGOs, AtRDRs) proteins have been represented by blue and red, respectively. Here DCLs, AGOs, and RDRs families have been represented by orange, purple, and green circles, respectively

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The lengths of PdDCL genes are ranging from CDS 2486 (PdDCL-3b) to 7331 (PdDCL-3a) bp and their protein lengths are ranging from 714 to 1824 amino acids (Table 1). The lengths of PdAGO genes are ranging from CDS 2980 (PdAGO-4,8,9) to 4236 (PdAGO-10) bp and their protein lengths are ranging from 852 to 973 amino acids (Table 1). The lengths of PdRDR genes are ranging from CDS 4231 (PdRDR-6) to 3670 (PdRDR-2) bp and their protein lengths are ranging from 1117 to 1198 amino acids (Table 1). The isoelectric point (pI) values of the PdDCL genes revealed that they are slightly acidic, with only the PdDCL-3b, which is slightly alkaline, with a maximum pI value of 7.8. The PdAGO genes pI values showed that they are alkaline. The pI values of the PdRDR genes demonstrated that they are nearly neutral.

The PdDCL proteins have a grand average hydropathicity index (GRAVY) or peptides hydrophobicity value that are ranging from − 0.138 (PdDCL-4) to -0.43 (PdDCL-1). The GRAVY value of the PdAGO proteins are ranging from − 0.316 (PdAGO-6) to -0.523 (PdAGO-5), whereas for PdRDR proteins are from − 0.255 (PdRDR-2) to -0.309 (PdRDR-1). We have also investigated the phylogenetic relationship between PdRNAi and Oryza sativa RNAi (OsRNAi) proteins. We have observed that PdDCLs, PdAGOs, and PdRDRs belong to the same clusters of OsDCLs, OsAGOs, and OsRDRs, respectively (Fig. S1).

Charaterization of PdRNAi proteins

Conserved domains and motifs of PdRNAi proteins with respect to AtRNAi proteins

In this study, we have compared the conserved domains of PdDCL, PdAGO, and PdRDR with the AtDCL, AtAGO, and AtRDR proteins. From Fig. 3, we have observed that both PdDCLs and AtDCLs shows almost similar conserved domains, including Helicase_C, Dicer_dimer, PAZ, RNase III, DND1-DSRM, DEAD, dsrm, ResIII domain. Both PdAGOs and AtAGOs have nearly identical conserved domains, such as Piwi, ArgoN, PAZ, ArgoL1, ArgoL2, ArgoMid, and Gly-rich_Ago1 domains. The Gly-rich_Ago1 domain has been found in PdAGO-1 and AtAGO-1. We have found that the PdRDRs and AtRDRs have almost the same conserved domains, including RNA-dependent RNA polymerase (RdRP) domain (Fig. 3). We have selected 10 significant motifs for PdRNAi and AtRNAi proteins by using MEME-suite analysis. Most of the PdDCL and AtDCL proteins have shown almost similar motif distributions. The annotated conserved motifs 1, 3, 4, 5, and 7 represents Ribonuclease 3 domain, motif 2 represents the Helicase-C domain, motif 6 represents the DEAD domain, motif 8 represents the Dicer dimer domain, and motif 10 represents the PAZ domain, of the predicted PdDCL proteins (Fig. S3A).

Fig. 3
figure 3

The conserved domains of AtRNAi and the PdRNAi proteins. Different color represents different conserved domains. Here Piwi indicates Piwi domain, ArgoN indicates N-terminal domain, PAZ indicates PAZ domain, ArgoL2 indicates Argonaute linker 2 domain, ArgoL1 indicates Argonaute linker 1 domain, ArgoMid indicates Mid domain of argonaute, Gly-rich_Ago1 indicates Glycine-rich region of Argonaut, RNase III indicates Ribonuclease III domain, Dicer_dimer indicates Dicer dimerization domain, Helicase_C indicates Helicase conserved C-terminal domain, dsrm indicates Double-stranded RNA binding motif, DEAD indicates DEAD/DEAH box helicase domain, RdRP indicates RNA dependent RNA polymerase, RRM_1 RNA recognition motif 1

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The annotated conserved motifs 1, 2, 3, 4, 6, 7, and 8 represent the Piwi domain, motif 5 represent the ArgoL1 domain, motif 10 represent the ArgoL2 domain and motif 9 represent the PAZ domain of predicted PdAGO proteins. The annotated conserved motifs 1–10 represent the RdRP domain of projected PdRDR proteins. The MEME studies of conserved motifs in the PdDCL, PdAGO, and PdRDR protein families have revealed comparable functional diversity in date palms. We have also compared the domains and motifs of PdRNAi proteins with OsRNAi proteins. We have perceived that PdDCLs, PdAGOs, and PdRDRs show similar domain and motif patterns according to OsDCLs, OsAGOs, and OsRDRs, respectively (Fig. S2 and S3B).

PdRNAi genes structures with respect to AtRNAi genes

The exon-intron structures of PdRNAi genes have been analyzed with respect to the AtRNAi genes to investigate the similarities of exon-intron between them. We have observed that the exon-intron structures of PdDCLs, PdAGOs, and PdRDRs are almost identical with the AtDCLs, AtAGOs, and AtRDRs (Fig. 4). According to the gene structure analysis, the PdDCLs have 19–28 exons, PdAGOs have 22–26 exons and PdRDRs have 3–6 exons, which has been nearly identical to AtDCLs AtAGOs and AtRDRs, respectively. The gene PdAGO-7 has three and PdAGO-2,3 gene has four exons. We have also compared the similarities of exon-intron patterns between PdRNAi and OsRNAi genes and found their similarities like AtRNAi genes (Fig. S4).

Fig. 4
figure 4

Structure of AtRNAi and the predicted PdRNAi genes

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Sub-cellular localizations of PdRNAi proteins with respect to AtRNAi proteins

Subcellular localization investigations has been carried out to learn more about the PdRNAi proteins cellular presence. The majority of PdRNAi, as well as AtRNAi proteins, have found in the nucleus, chloroplast, and cytosol, according to sub-cellular localization study (Fig. 5). Some of our PdRNAi proteins have also found in cell vacuoles, cytoskeletal and mitochondria (Fig. 5). In addition, We have also compared the sub-cellular locations between PdRNAi and OsRNAi proteins and noticed their similarities like AtRNAi proteins (Fig. S5).

Fig. 5
figure 5

Sub-cellular localization analysis of AtRNAi and PdRNAi proteins. Protein percentages

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are found in several biological components. In this analysis, nucl– nucleus, cyto– cytosol, chlo– chloroplast, vacu– vacuole, cysk– Cytoskeletal, mito– mitochondria, E.R.– Endoplasmic Reticulum, plas– plastid, pero– peroxisome.

Biological processes and molecular functions of PdRNAi proteins

The GO enrichment analysis has been performed to see how predicted PdRNAi proteins are connected with BPs and MFs. The study have identified several important BPs and MFs those are associated with gene silencing processes (Table 2). For example, 9 (PdDCL-1, PdDCL-3b, PdDCL-4, PdAGO-2,3, PdAGO-4,8,9, PdAGO-7, PdAGO-10, PdRDR-1, PdRDR-6) of 14 PdRNAi proteins have been engaged with BP term response to virus (GO:0009615; p-value: 1.8E-21), eight (PdDCL-1, PdDCL-3b, PdDCL-4, PdAGO-4,8,9, PdAGO-7, PdRDR-1, PdRDR-2, PdRDR-6) of 14 PdRNAi proteins have been found to be involved in the BP terms as production of siRNA (GO:0030422; p-value: 6.5E-21), RNA interference (GO:0016246; p-value: 1.4E-20), dsRNA fragmentation (GO:0031050; p-value: 3.1E-19). Our study also found that, 4 (PdDCL-1, PdDCL-3b, PdAGO-4,8,9, PdRDR-2) of 14 PdRNAi proteins have been found to be involved in the CC terms as nuclear lumen (GO:0031981; p-value: 0.00019), intracellular organelle lumen (GO:0070013; p-value: 0.00025), organelle lumen (GO:0043233; p-value: 0.00025), membrane-enclosed lumen (GO:0031974; p-value: 0.00026). Three (PdRDR-1, PdRDR-2, PdRDR-6) of 14 PdRNAi proteins have been found to be involved in the molecular function term RNA-directed RNA polymerase activity (GO:0003968; p-value: 2E-08). Three (PdDCL-1, PdDCL-3b, PdDCL-4) of 14 PdRNAi proteins have been found to be involved in the molecular functions terms as ribonuclease III activity (GO:0004525; p-value: 3.1E-08), double-stranded RNA-specific ribonuclease activity (GO:0032296; p-value: 3.1E-08). Two (PdAGO-2,3, PdAGO-4,8,9) of 14 PdRNAi proteins have been found to be involved in the MF term siRNA binding (GO:0035197; p-value: 2.2E-06). We have also compared the GOs of PdRNAi with AtRNAi and OsRNAi proteins and perceived their similarities (Table 2).

Table 2 GO enrichment analysis results with the AtRNAi, predicted PdRNAi and OsRNAi proteins
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PdRNAi gene regulatory network analysis

Trans-regulatory factors of PdRNAi genes

At first, we have identified transcription factors (TFs) with respect to AtRNAi, PdRNAi, and OsRNAi genes by using PlantTFcat web-tool. Then we have submitted AtRNAi, PdRNAi, and OsRNAi genes and associated TFs in Cytoscape to construct the network between them. We have found two (PAZ, SNF2) TFs in AtRNAi, PdRNAi, and OsRNAi genes (Fig. 6). The PAZ TF has been found to associated with (PdDCL-1, PdAGO-7, PdAGO-10, PdDCL-4, PdDCL-3a, PdDCL-3b, PdAGO-1, PdAGO-2,3, PdAGO-4,8,9, PdAGO-5, PdAGO-6, AtDCL-1, AtAGO-6, AtAGO-7, AtAGO-8, AtAGO-9, AtAGO-10, AtDCL-2, AtDCL-3, AtDCL-4, AtAGO-1, AtAGO-2, AtAGO-3, AtAGO-4, AtAGO-5, OsAGO1a, OsMEL1, OsAGO13, SHL4, OsPNH1, OsAGO17, OsAGO12, OsAGO11, OsAGO18, OsAGO15, OsAGO1b, OsDCL1a, OsDCL2a, OsDCL2b, OsDCL3a, OsDCL3b, SHO1, OsAGO1c, OsAGO1d, OsAGO2, OsAGO3, OsAGO4a, OsAGO4b, OsAGO4) AtRNAi, PdRNAi, and OsRNAi genes. The SNF2 associated with AtDCL-1, AtDCL-2, PdDCL-1, PdDCL-3a, and PdDCL-3b genes (Fig. 6).

Fig. 6
figure 6

The regulatory network among the TFs with PdRNAi, AtRNAi, And OsRNAi genes. The nodes of the network have been colored based on RNAi genes: AtRNAi: blue, OsRNAi: light green, and PdRNAi: orange. The node shape of the network have been based on RNAi genes: DCLs: triangle, AGOs: octagonal, and TFs: round

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Cis-regulatory factors of PdRNAi genes

The cis-acting regulatory elements (CAREs) study has been performed to investigate how those regulators controlled PdRNAi genes. According to our findings, the regulatory regions of PdRNAi genes have contained light-responsive (LR), hormone-responsive (HR), and stress-responsive (SR) related motifs (Fig. 7). The LR motifs including 3-AF1 binding site, ACE (ACGT-containing element), AE-box (activation element), Box 4 (involved in light responsiveness), G-box (CACGTG motif), GATA-motif, GT1-motif (GGTTAA, GGTAATT, GGTAAAT, GTTAC, TACAGT, and GGTAAA), I-box (AGATATGATAAAA), LAMP-element, Sp1 (specificity protein 1), TCT-motif (polypyrimidine initiator), and TCCC-motif have been found in PdRNAi genes (Fig. 7). The significant number of I-box LR motif has found in the expected PdRNAi genes. The cis-acting regulatory elements ABRE (involved in the abscisic acid responsiveness), O2-site (involved in zein metabolism regulation), P-box (gibberellin-responsive element), TCA-element (involved in salicylic acid responsiveness), and TGA-element (auxin-responsive element) has found in the promoter regions of PdRNAi genes, that are involved in the regulation of hormones (HR). Some of our PdRNAi genes are regulated by the cis-acting elements, including TC-rich repeats (involved in defense and stress responsiveness, MBS (MYB binding site involved in drought-inducibility), MYB (involved in drought-inducibility, LTR (involved in low-temperature responsiveness as stress-responsive (SR). We have also compared the cis-elements between PdRNAi and OsRNAi genes and observed their similarities like AtRNAi genes (Fig. S6).

Fig. 7
figure 7

The cis-acting regulatory elements of AtRNAi and predicted PdRNAi genes. The deep to light green color represent the presence degree of that element with the corresponding genes. (A) hormone-responsive cis-elements, (B) light-responsive cis-elements, and (C) stress-responsive cis-elements

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miRNA of PdRNAi genes

The purpose of the miRNA investigation is to see how miRNA regulates the expression of PdRNAi genes. We have detected eight key miRNAs, including Pda-miR156b, Pda-miR157b, Pda-miR159a, Pda-miR166a, Pda-miR167d, Pda-miR395c, Pda-miR396a, Pda-miR529a, Pda-miR482, Pda-miR2118 using PdRNAi genes (Figs. S7A, B). Six of the 14 PdRNAi genes have been regulated by the Pda-miR529a. Four of the 14 PdRNAi genes have been regulated by the Pda-miR396a. The PdDCL-1 has been regulated by Pda-miR166a, Pda-miR167d, Pda-miR396a, Pda-miR482, Pda-miR2118. The PdDCL-4 has been regulated by Pda-miR156b, Pda-miR159a, Pda- miR395c, Pda-miR396a. All of the miRNAs are found to expressed in the leaves and roots. Both Pda-miR166a and Pda-miR2118 have a high expression score in leaves and roots. Both Pda-miR156b and Pda-miR159a have a medium expression score in leaf. In root, the expression scores of Pda-miR156b, Pda-miR159a, Pda-miR396a, Pda-miR482 are medium. We have also studied the miRNAs and expressions of OsRNAi and AtRNAi genes to compare with PdRNAi genes. We have found that OsRNAi and AtRNAi have almost similar miRNAs and miRNA expressions according to PdRNAi genes (Figs. S7A, B).

Discussion

The major RNAi genes RDR, DCL, and AGO function as unique short RNAs that regulate a variety of biological processes and pathways by silencing protein-coding genes [80, 81]. In this study, we have identified 4 PdDCLs, 7 PdAGOs, and 3 PdRDRs as RNAi proteins from the date palm genome guided by AtRNAi proteins as a query sequence in BLASTp search based on MSAs. Then phylogenetic tree analysis has been performed to investigate the similarities of PdRNAi with AtRNAi and OsRNAi proteins. To validate the predicted PdRNAi proteins computationally, we have studied their characteristics and activities with respect to both AtRNAi and OsRNAi proteins. Here we considered OsRNAi proteins, since both of rice (Oryza sativa) and date palm belong to the same monocot commelinids clade (Fig. 2 and Fig. S1) [19]. In order to investigate the roles of PdRNAi proteins in the protein coding gene silencing, stress response and disease resistance, we have analyzed domains, structures, locations, molecular functions and regulatory factors of PdRNAi genes that are discussed below.

The domains and motifs of predicted PdRNAi proteins have displayed similar patterns compared with AtRNAi and OsRNAi proteins (Figs. 3 and 4 and Figs. S2, S3). All PdDCLs and three PdAGO proteins might be functions as protein coding gene silencers, since all PdDCLs and three PdAGOs belong to the same group of AtDCLs and AtAGOs (AtAGO-3, AtAGO-4, AtAGO-6, and AtAGO-9) protein [82,83,84,85,86,87,88]. The PdDCL-1 protein may produce 21 and 22nt sRNAs from small stem-loop RNA substrates, whereas PdDCL-2, PdDCL-3, and PdDCL-4 proteins may produce 22nt, 24nt, and 21nt sRNAs from large dsRNA, respectively [89]. The PAZ and RNase III domains in Dicer (PdDCLs) synthesize silencing-associated sRNAs from a larger dsRNA [12, 90]. The RDR (PdRDRs) synthesize the majority of long dsRNAs in plants [91]. The PdRDR-6 protein may be required for the production of trans-acting siRNAs (tasiRNAs) because it cleavages the dsRNA. The PdDCL-4 protein may synthesize the dsRNA from the miRNA-cleavage end, resulting in 21-nucleotide siRNA duplexes formation [92,93,94]. More specifically, the identified PIWI domain contains structural similarities with ribonuclease-H enzymes, which indicates that it may be responsible for cleaving the target mRNA [95]. The predicted DEAD-box and helicase domain may stimulate date palm to produce secondary siRNAs [96, 97]. The anticipated PAZ and RNase III domains may operate as an indication, creating miRNAs with comparable sizes [98]. The predicted PIWI and PAZ may recognize and cleave the target mRNA [99,100,101]. Most of the predicted PdRNAi proteins have been significantly enriched in the nucleus, cytosol, and chloroplast (Fig. 5 and Fig. S5), where the first two locations are known to be involved with the occurrence of the RNA silencing mechanism [102, 103]. The GO enrichment analysis of PdRNAi genes has detected some vital BP and MF terms that are directly involved with the gene silencing mechanisms and those terms are almost identical with AtRNAi and OsRNAi genes (Table 2). Out of 14 predicted PdRNAi proteins, 8 proteins are involved with the biological process terms as production of siRNA (GO:0030422) [104], RNA interference (GO:0016246) [105], and dsRNA fragmentation (GO:0031050) [106]. The GO:0030422 term is associated with the 24nt hc-siRNA and 21nt siRNA production pathways [107]. Eukaryotic cells use siRNAs (GO:0030422, GO:0035197) [108,109,110,111] to bind and enhance the degradation of specific endogenous mRNAs generated by dsRNA (GO:0031050. GO:0032296) [112,113,114], to decrease protein synthesis at the post-transcriptional stage. The PdRDR proteins are involved with the molecular function term RNA-directed RNA polymerase activity (GO:0003968) [115], which is associated with RNA-mediated gene silencing in plants [116]. Three PdDCL proteins are involved with the terms of the molecular function as ribonuclease III activity (GO:0004525) [117,118,119] which specifically cleave dsRNAs for RNAi mechanisms in plants [90]. Two PdRNAi proteins are involved with the molecular function term siRNA binding (GO:0035197), which is essential to the RNAi mechanisms [111]. TFs are key regulatory factors that are involved in the activation or deactivation of upstream signaling pathways and bind to specific promoter regions (i.e., cis-acting elements) of their target genes to increase or inhibit the transcriptional rate of those genes [120]. Our detected PAZ-Argonaute [121] (similar as OsRNAi) genes, a member of the PTGS family of TFs, may require for RNAi pathway (Fig. 6). The SNF2 is linked with three PdRNAi genes. The SNF2 protein may supply ATP-driven motor components for remodeling systems that may control gene silencing of PdRNAi genes [122]. The miRNAs function as critical regulators of eukaryotic gene expression by targeting mRNAs for break-down or translation inhibition [123]. PdRNAi and OsRNAi almost similar miRNAs (Figs. S7A, B). Our detected miRNAs have a variety of significant activities, including gene silencing (miR159a, miR482) [124, 125]. Thus the predicted PdRNAi genes through sRNAs may play a vital role for the protein coding genes silencing.

We found that two PdAGO genes, which belong to the gene groups of AtAGO-10 and AtAGO-7 genes and are associated with A. thaliana development, may the best candidates for date palm development [126, 127]. The PdRNAi belong to the gene groups of OsDCL-4, OsAGO-1 (a-d), and SHL2, which may enhance the expressions of target genes during early floral/panicle development [19]. The PdAGO-5 gene, like OsMEL-1 and OsAGO-4 genes, might be expressed in reproductive organs and influence panicle and seed development. Similar to OsPNH-1, the PdAGO-10 gene may influence SAM and leaf development [19]. The PdRDR-2, similar to OsRDR-2, may affect flower development [19]. The PdDCL1, PdAGO1, PdAGO4, and PdRDR5 genes may play essential roles in stress response [128]. The PdDCLs might stimulate leaf or stem development in date palm as the intron number of each of PdDCLs and OsDCLs is almost the same as that of AtDCLs [28, 81, 90, 129,130,131,132,133] (Fig. 4 and Fig. S4) [134]. We have also found our detected cis-regulatory elements in OsRNAi (Fig. 7 and Fig. S6). Previous research has found that our predicted LR-related motifs play an important role in the photosynthetic process of leaves [9, 135,136,137,138]. The cis-acting regulatory elements ABRE [139, 140], O2-site [141], P-box, TCA-element, and TGA-element [141,142,143] have been discovered in the promoter regions of PdRNAi genes, that are involved in the regulation of hormones (HR). The TCA-elements, MYC, ABRE, and 3-AF1 binding sites are significant cis-regulatory elements of PdRNAi genes that might be played a vital role against plant’s bio/abiotic stress [144]. The regulatory effect of MYC on miRNA expression can be either positive or negative [145, 146]. Some of our PdRNAi genes are regulated as stress-responsive (SR) by the cis-acting elements, including TC-rich repeats [147], MBS, MYB [148], LTR [149]. Some of PdRNAi genes are influenced by the cis-acting factors, including Box-4, G-box, I-box, GT1 motif, GATA-motif, and TCT-motif that plays an important role as light response (LR) of several species [135,136,137,138, 150,151,152,153,154]. Because of LR-related motifs are important in photosynthetic mechanisms in plant leaves, the PdRNAi genes might be played an important role in improvement of date palms [155]. Our detected miRNAs have a variety of significant activities, including plant improvement (miR156b, miR157b, and miR396a) [156,157,158] and stress tolerance (miR166a, miR395e, miR529a) [159,160,161]. Thus, the predicted PdRNAi might be improved the quality of date palm fruits by promoting photosynthetic activity, a shorter flowering period, meristem, leaf, seed improvement and plant enhancement against different biotic and abiotic stresses.

We found that all PdDCLs and three PdAGOs belong to the same gene groups of AtDCLs and AtAGOs, which have anti-pathogen activity in Arabidopsis and may protect P. dactylifera from pathogens [40, 162,163,164,165,166]. The Ribonuclease III (found in PdDCLs) can resist pathogens [167] and the PdRDR proteins may have antiviral activity [168]. Date palm antiviral [169] and antifungal [170] defense may rely heavily on RdRP (GO:0003968) activity [171]. The dsRNA-specific ribonuclease activity (GO:0032296) [172] may target several date palm RNA viruses [173]. Our detected miRNAs in PdRNAi genes may have a variety of significant activities, including resistance to disease (miR167d, miR2118) [174, 175]. Thus, our predicted PdRNAi genes might be enhanced the date palm growth and development by regulating the respective protein coding genes against disease risks.

Conclusion

In this study, we have identified 4 PdDCL, 7 PdAGO, and 3 PdRDR genes as PdRNAi genes guided by AtRNAi genes through bioinformatics analysis. To gain a better knowledge of PdRNAi corresponding to AtRNAi and OsRNAi gene families, we have investigated their phylogenetic relationship, domain components, genomic structure, subcellular localization, functional annotations, TFs, cis-elements, and miRNAs. The analysis results of this study have indicated that the PdAGO-5, PdAGO-7, and PdAGO-10 genes might be highly involved in growth and development, and PdDCL1, PdAGO1, PdAGO4 and PdRDR5 might be effective against different stresses in date palm. So far, this is the first study to shed light on the major RNAi gene families of date palms. Therefore, the knowledge gathered from this study might be useful resources to enhanced the date palm production by regulating the respective protein coding genes against biotic and abiotic stresses. However, wet-lab experiments are needed to confirm that PdRNAi genes regulate date palm growth and development through the silencing mechanism of the releted protein-coding genes under various stresses.

Data availability

The dataset on date palm genome analyzed in this study has downloaded from the NCBI database with GenBank Accession Number: GCA_009389715.1 (NCBI taxonomy ID: 42345, BioSample:SAMN05011615, https://www.ncbi.nlm.nih.gov/genome/?term=Phoenix+dactylifera) using the published date palm genome sequence. The rest of the data that have used in this study will be available on request.

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  1. Bioinformatics Lab, Department of Statistics, Faculty of Science, University of Rajshahi, 6205, Rajshahi, Bangladesh

    Darun Naim, Asif Ahsan & Nurul Haque Mollah

  2. Department of Botany, Faculty of Biological Sciences, University of Rajshahi, 6205, Rajshahi, Bangladesh

    Darun Naim & Ahmed Imtiaj

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M.D.N., A.I., and M.N.H.M. conceptualization, M.A.A. data and software support, review & editing, M.D.N. formal analysis, M.D.N. draft writing, A.I. and M.N.H.M. review & editing, M.N.H.M supervision.

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Naim, D., Ahsan, A., Imtiaj, A. et al. Genome-wide identification and in silico characterization of major RNAi gene families in date palm (Phoenix dactylifera). BMC Genom Data 25, 31 (2024). https://doi.org/10.1186/s12863-024-01217-x

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