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. 2023 Sep 20:14:1252020.
doi: 10.3389/fgene.2023.1252020. eCollection 2023.

Integrated omics and machine learning-assisted profiling of cysteine-rich-receptor-like kinases from three peanut spp . revealed their role in multiple stresses

Kinza Fatima  1 , Muhammad Sadaqat  1 , Farrukh Azeem  1 , Muhammad Junaid Rao  2 , Norah A Albekairi  3 , Abdulrahman Alshammari  3 , Muhammad Tahir Ul Qamar  1
Affiliations

Integrated omics and machine learning-assisted profiling of cysteine-rich-receptor-like kinases from three peanut spp . revealed their role in multiple stresses

Kinza Fatima et al. Front Genet. .

Abstract

Arachis hypogaea (peanut) is a leading oil and protein-providing crop with a major food source in many countries. It is mostly grown in tropical regions and is largely affected by abiotic and biotic stresses. Cysteine-rich receptor-like kinases (CRKs) is a family of transmembrane proteins that play important roles in regulating stress-signaling and defense mechanisms, enabling plants to tolerate stress conditions. However, almost no information is available regarding this gene family in Arachis hypogaea and its progenitors. This study conducts a pangenome-wide investigation of A. hypogaea and its two progenitors, A. duranensis and A. ipaensis CRK genes (AhCRKs, AdCRKs, and AiCRKs). The gene structure, conserved motif patterns, phylogenetic history, chromosomal distribution, and duplication were studied in detail, showing the intraspecies structural conservation and evolutionary patterns. Promoter cis-elements, protein-protein interactions, GO enrichment, and miRNA targets were also predicted, showing their potential functional conservation. Their expression in salt and drought stresses was also comprehensively studied. The CRKs identified were divided into three groups, phylogenetically. The expansion of this gene family in peanuts was caused by both types of duplication: tandem and segmental. Furthermore, positive as well as negative selection pressure directed the duplication process. The peanut CRK genes were also enriched in hormones, light, development, and stress-related elements. MicroRNA (miRNA) also targeted the AhCRK genes, which suggests the regulatory association of miRNAs in the expression of these genes. Transcriptome datasets showed that AhCRKs have varying expression levels under different abiotic stress conditions. Furthermore, the multi-stress responsiveness of the AhCRK genes was evaluated using a machine learning-based method, Random Forest (RF) classifier. The 3D structures of AhCRKs were also predicted. Our study can be utilized in developing a detailed understanding of the stress regulatory mechanisms of the CRK gene family in peanuts and its further studies to improve the genetic makeup of peanuts to thrive better under stress conditions.

Keywords: abiotic stress; gene ontology enrichment; multi-stress-related genes; pangenome-wide; peanut; random forest; receptor-like kinases.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Workflow of the pangenome-wide identification of CRK genes in peanut, their structural and functional analysis, expression profiling, and multi-stress responsiveness.
FIGURE 2
FIGURE 2
Box plots showing the physiochemical characteristics of three Arachis species: (A) amino acid residues/protein length, (B) their molecular weight, (C) their isoelectric point, (D) aliphatic index, (E) insatiability index, and (F) the grand average of hydropathicity.
FIGURE 3
FIGURE 3
Phylogenetic tree of the CRK protein sequences from seven different plant species including three Arachis species, generated using the maximum likelihood method. Different groups are represented by specific clade and branch colors.
FIGURE 4
FIGURE 4
(A) Phylogenetic tree of AhCRKs, (B) structural features showing exon–intron organization, and (C) a conserved motif pattern of 71 AhCRK proteins.
FIGURE 5
FIGURE 5
(A) Chromosomal mapping of AhCRK genes; (B) segmental and tandem duplications among the AhCRK members. Gene label colors specify the group they belong to.
FIGURE 6
FIGURE 6
Cis-regulatory elements in the upstream promoter regions of the AhCRK genes. Each bar is representing the specific elements present in the particular gene.
FIGURE 7
FIGURE 7
Figure shows the predicted miRNAs potentially targeting the AhCRKs and the target sites.
FIGURE 8
FIGURE 8
(A) Network showing the interactions among AhCRK protein members and other related proteins. The green nodes are AhCRKs, and the blue nodes are other interacting proteins. (B) GO enrichment bubble plot representing the biological processes, their cellular components, potential molecular functions, and GO and KEGG pathways in which AhCRK proteins are potentially involved.
FIGURE 9
FIGURE 9
Heatmap representing the change in the expression level of AhCRKs in peanut leaves under (A) drought stress at 5, 7, and 9 days and in (B) salt stress. Blue color represents the downregulated expression, and red color represents the higher or upregulated expression.
FIGURE 10
FIGURE 10
Predicted 3D structures of three multi-stress-related AhCRKs. Structures are displayed based on secondary structures: blue colors represent spirals, red shapes represent turns, and purple shapes represent loops.
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