

Legume Genomics and Genetics, 2025, Vol. 16, No. 4
Received: 15 Jun., 2025 Accepted: 31 Jul., 2025 Published: 20 Aug., 2025
Heat stress is an important factor affecting the yield and adaptability of chickpeas, especially in the context of global climate change. To breed varieties that are both stress-resistant and high-yielding, it is necessary to conduct in-depth research on its heat-resistant molecular basis. This study reviewed the physiological and molecular responses of chickpeas at high temperatures, such as changes in photosynthetic efficiency, membrane stability, heat shock proteins (HSPs), and hormone signaling. Transcriptome studies have discovered many differentially expressed genes and regulatory networks; Proteomic and metabolomic analyses revealed that some stress-resistant related proteins, antioxidant substances, as well as metabolites such as proline and soluble sugars would accumulate at high temperatures. Genomic methods (such as QTL mapping and SNP analysis) have helped identify candidate gene loci, while the role of epigenetic modifications in heat tolerance responses has gradually been discovered. This study also presents a comparative case, conducting multi-omics analyses on heat-resistant and sensitive strains, demonstrating how to integrate the results to identify key candidate genes and metabolic pathways and apply them to the development of molecular markers. This study also systematically summarized the progress of multi-omics in the heat tolerance research of chickpeas, pointed out the difficulties faced in data integration, and proposed future research directions, which are expected to improve stress resistance in molecular design breeding and accelerate the breeding of heat-tolerant chickpea varieties.
1 Introduction
Chickpea (Cicer arietinum L.) is the second largest leguminous crop in the world. However, as the temperature rises, heat stress occurs more and more frequently, and this crop is under great threat. High temperatures, especially during the reproductive stage, can lead to a reduction in flowering, an increase in flower drop, and a decline in pod formation, thereby causing a significant drop in yield. This situation not only affects traditional wine regions but also new ones that are expanding (Paul et al., 2018; Devi et al., 2022; Jain et al., 2023; Naveed et al., 2025). Studies have found that for every 1 ℃ increase in temperature, the yield may decrease by 10% to 15%, and different genotypes respond significantly to high temperatures (Upadhyaya et al., 2011). The problem becomes even more complex when the planting methods change and the planting areas expand to warmer environments (Krishnamurthy et al., 2011; Gaur et al., 2013).
Heat resistance is crucial for maintaining the yield and quality of chickpeas. There are heat tolerance differences in germplasm resources, and identifying heat tolerance genotypes has always been an important direction in breeding (Devi et al., 2022; Chetariya et al., 2024. However, heat tolerance is a complex quantitative trait, jointly determined by many genes and regulatory networks (Mohanty et al., 2024). In recent years, multi-omics approaches (genomics, transcriptomics, proteomics and metabolomics) have brought about new breakthroughs in this type of research. These methods can help identify key genes, QTLS, proteins and metabolites related to heat stress, reveal the underlying physiological and molecular mechanisms, and also provide new ideas for breeding heat-tolerant varieties (Makonya et al., 2021; Yadav et al., 2022; Mohanty et al., 2024).
This study will first review the impact of high temperature on the yield and physiology of chickpeas, then summarize the latest progress of multi-omics technology in the research of heat tolerance mechanisms, and integrate the current understanding of the genetic and molecular basis of heat tolerance. The focus will be on how multi-omics methods can help identify candidate genes and related pathways, as well as the significance of these achievements for heat tolerance breeding. The objective of this study is to provide ideas for genetic improvement under climate change by integrating multi-omics data, thereby enhancing the yield and quality of chickpeas.
2 Physiological and Molecular Basis of Heat Tolerance in Chickpea
2.1 Physiological responses under heat stress (photosynthetic efficiency, membrane stability, transpiration regulation)
At high temperatures, chickpeas exhibit some beneficial physiological responses, which can help them better withstand heat. It mainly includes maintaining photosynthetic efficiency, maintaining membrane stability and regulating transpiration. Heat-resistant varieties usually have a higher photosynthetic rate, chlorophyll content, and quantum yield (Fv/Fm) of photosystem II, which are important for energy acquisition and growth. Their cell membranes are also more stable, with lower electrolyte leakage and malondialdehyde content, so cell functions can be protected at high temperatures (Kumar et al., 2017; Devi et al., 2022). In addition, tolerant strains generally have a higher water utilization rate and can accumulate more osmotic regulatory substances, which can maintain cellular turgor pressure and regulate transpiration (Pareek et al., 2019; Kumar et al., 2020; Wang et al., 2024). In the lutein cycle, pigments like zeaxanthin can dissipate excess light energy, thereby protecting the photosynthetic system.
2.2 Functions of heat shock proteins (HSPs) and heat shock transcription factors (HSFs)
Heat shock proteins (HSP) and heat shock transcription factors (HSF) are important molecular mechanisms by which chickpeas resist high temperatures. HSPS, such as HSP70 and HSP90, can act as chaperone proteins, maintaining the stability of other proteins and preventing aggregation at high temperatures. HSF, especially CaHSFA5, can regulate the expression of HSP and some stress response genes, thereby initiating a rapid protective response (Jeffrey et al., 2021; Mohanty et al., 2024). In heat-resistant strains, the expression levels of HSP and HSF increase, which is related to enhanced heat resistance, reduced oxidative damage and improved recovery ability after high temperature (Pareek et al., 2019; Makonya et al., 2021).
2.3 Roles of hormone signaling pathways (ABA, ethylene, jasmonic acid, etc.) in heat tolerance
Some hormone signaling pathways play a key role in chickpeas' response to high temperatures, including abscisic acid (ABA), ethylene and jasmonic acid. ABA and ethylene can regulate stomatal closure, promote the accumulation of osmotic regulators, and activate the antioxidant defense system, which can increase the survival rate of plants under heat stress (Paul et al., 2018). Genes related to these pathways, such as MYB44 and RAN1, are up-regulated at high temperatures, thereby enhancing heat tolerance. Jasmonic acid and salicylic acid also participate in regulation. They work in synergy with HSP and the antioxidant system to reduce cell damage. The study also found that exogenous application of these hormones or their analogues could further enhance the heat tolerance of chickpeas (Kumar et al., 2020).
3 Transcriptomic Insights into Molecular Regulation of Heat Tolerance
3.1 Identification and functional annotation of differentially expressed genes under heat stress
When conducting transcriptome analysis on chickpeas, it was found that tens of thousands of genes undergo differential expression (DEG) at high temperatures. These genes show different manifestations at different growth stages and in different varieties. A total of 14 544 unique DEGs were identified in leaf and root tissues, which were related to processes such as metabolism, cell wall changes, calcium signaling, and photosynthesis (Figure 1) (Kudapa et al., 2023). Further functional annotation and pathway analysis revealed that high temperature activates some metabolic pathways while enhancing secondary metabolite and hormone signaling (Danakumara et al., 2024). Among them, the genes encoding heat shock protein (HSP), heat shock transcription factor (HSF), and other stress response proteins are continuously highly expressed in heat-resistant strains (Chidambaranathan et al., 2018).
![]() Figure 1 Global transcriptome analysis of 48 samples from six contrasting heat stress-responsive chickpea genotypes (Adopted from Kudapa et al., 2023) Image caption: (A) Plant phenotype of chickpea heat-tolerant (ICCV 92944) and -sensitive (ICC 4567) genotypes in response to heat stress. (B) Heatmap for the transcriptome profiling has been shown based on the hierarchical clustering of Pearson’s correlations (R) for the 48 samples. The color scale indicates the degree of correlation. Samples were clustered based on their pairwise correlations. Genes with a normalized expression level FPKM≥1 in at least one of the 48 samples analyzed were designated as expressed and shown in the figure (Adopted from Kudapa et al., 2023) |
3.2 Regulatory networks and key transcription factors associated with heat tolerance
Transcriptome studies have identified some key families of transcription factors, including bHLH, ERF, WRKY, MYB and HSF, which are regulated differently at high temperatures (Danakumara et al., 2024). These factors will collectively form a complex network to regulate genes related to stress perception, signal transduction, and defense responses. For instance, HSF (particularly CaHSFA5) and HSP are the core for coping with high temperatures, while MYB44 and RAN1 are related to hormone signaling and adaptation processes (Mohanty et al., 2024). Co-expression analysis also indicated that these transcription factors were associated with some genes related to ROS clearance, synthesis of osmotic substances, and cell wall modification, thereby helping plants improve heat tolerance (Kudapa et al., 2023).
3.3 Construction of co-expression modules and heat response pathways
Through co-expression network analysis, the gene modules and pathways related to heat resistance can be linked together. These modules include differentially expressed genes, transcription factors and some non-coding Rnas (such as lincRNA), revealing their synergistic effects in the thermal response (Bhogireddy et al., 2023). These modules are enriched with genes related to photosynthesis, hormone signaling and stress defense, and are often linked to the major QTL (Kudapa et al., 2023; Kumar et al., 2023). When transcriptome data is used in conjunction with QTL mapping and GWAS, candidate genes and core regulatory points can be identified more quickly. This provides a clear goal for molecular breeding of heat-resistant chickpeas (Chidambaranathan et al., 2018; Danakumara et al., 2024; Mohanty et al., 2024).
4 Integrated Proteomics and Metabolomics Studies
4.1 Dynamic changes in protein expression profiles under heat stress
Proteomic studies on chickpeas at high temperatures have found that many proteins related to protein synthesis, intracellular transport, defense and material transport are significantly upregulated, especially in heat-resistant strains. There are significant differences in the expression of key proteins such as HSP70, ribulose diphosphate carboxylase/oxygenase activase, plastipline and protoporphyrin oxidase. These proteins can help plants maintain photosynthesis and protect cells at high temperatures (Makonya et al., 2021). In addition, in heat-resistant strains, proteins related to electron transport chains, amino acid synthesis and secondary metabolites are also more abundant, indicating that they play a role in maintaining physiological and biochemical stability.
4.2 Accumulation and regulation of metabolites such as proline, soluble sugars, and antioxidants
Metabolomics studies have shown that heat-resistant chickpea products accumulate more polysaccharides, amino acids (including proline), sugar alcohols and tricarboxylic acid cycle (TCA) intermediates under high-temperature stress (Pareek et al., 2019; Yadav et al., 2022). These substances can regulate osmotic pressure, maintain cell membrane stability, and provide energy, thereby enhancing heat resistance. Meanwhile, an increase in the levels of antioxidant-related metabolites and enzymes (such as SOD, GPX, APX, CAT) can reduce oxidative damage. In addition, the metabolism of alanine, aspartic acid, glutamic acid and the pentose phosphate pathway are more active in heat-resistant strains.
4.3 Synergistic interactions between proteins and metabolites and integration of signaling pathways
Comprehensive proteomics and metabolomics research has found that proteins and metabolites often work together in response to heat stress. For instance, the upregulation of sucrose phosphatase and sucrose phosphatase is consistent with sugar accumulation, which contributes to energy metabolism and stress adaptation (Makonya et al., 2021; Yadav et al., 2022). In addition, the interaction among heat shock proteins, antioxidant enzymes and metabolic regulation can form a powerful defense network. Calcium signaling, MAPK and hormone signal-related genes will also be involved, further integrating these reactions (Pareek et al., 2019). This synergistic effect enables heat-resistant varieties to better adapt to the environment at high temperatures.
5 Contributions of Genomics and Epigenetics
5.1 Mapping and characterization of heat-tolerance-related QTLs and candidate genes
Advances in genomics have enabled researchers to identify QTLS related to the heat resistance of chickpeas and determine their locations. Several major regions were identified by the high-density genetic map established using SNP markers, such as CaLG05, CaLG06 and CaLG07. These QTLS can explain the differences in many important traits, including plump pods, seed yield, podding rate and some physiological indicators at high temperature (Paul et al., 2018; Jha et al., 2021; Kumar et al., 2023; Danakumara et al., 2024). Through Meta-QTL analysis, researchers further narrowed down these regions and identified several candidate genes, such as CaHSFA5 (high-temperature transcription factor), pollen receptor-like kinase 3, and flower-promoting factor 1. These genes are closely related to flowering, pollen germination and plant growth at high temperatures (Mohanty et al., 2024). Therefore, these QTLS and genes provide important targets for molecular marker-assisted selection and genome-assisted breeding, which is conducive to the cultivation of heat-tolerant varieties.
5.2 Analysis of genotypic variation and single nucleotide polymorphisms (SNPs)
GWAS and genotyping sequencing have revealed a large number of genotype differences among different populations of chickpeas and have also identified thousands of SNPS related to heat tolerance. These SNPS are significantly associated with some key traits, such as yield, flowering time, canopy closure degree and some physiological indicators (Thudi et al., 2014; Danakumara et al., 2024). Many SNPS are located near or inside the gene coding region, involving stress response, hormone signaling and protein regulation (Paul et al., 2018; Jha et al., 2021) High heritability and superphilic isolates were also discovered in population studies, which indicates that there is great potential to utilize natural genetic diversity to enhance heat tolerance.
5.3 Roles of DNA methylation and histone modifications in regulating heat tolerance
At present, research on chickpeas mainly focuses on genetic maps and SNP variations. However, in studies on related crops and a small number of chickpeas, there is already evidence suggesting that epigenetic mechanisms can also affect the heat stress response. For instance, DNA methylation and histone modification can regulate the expression of some heat-responsive genes. These modifications may act on genes in major QTL regions, thereby affecting the stability and heritability of heat-tolerant traits (Chen, 2024; Mohanty et al., 2024).
6 Case Study: A Multi-Omics Investigation of Heat Tolerance in Chickpea
6.1 Comparative multi-omics analysis between heat-tolerant and sensitive genotypes
By comparing chickpeas of different genotypes, researchers found that heat-resistant strains and sensitive strains differ significantly at the molecular and physiological levels. Proteomics results show that heat-resistant strains can up-regulate some proteins related to protein synthesis, intracellular transport, defense and transport. For example, heat shock protein 70 (HSP70), ribulose diphosphate carboxylase/oxygenase activase and sucrose phosphate synthase. These proteins help plants maintain a better physiological state at high temperatures (Makonya et al., 2021). The comparison of the genome and transcriptome also identified key QTLS and differentially expressed genes related to podding stage, seed yield and chlorophyll content. The results indicated that the heat-resistant strains could maintain higher photosynthetic efficiency and membrane stability under high-temperature conditions (Figure 2) (Paul et al., 2018; Devi et al., 2022; Kumar et al., 2023).
![]() Figure 2 Morphological symptoms of heat stress (HS) observed on in chickpea plants, showing plant height; under in the control condition (a), reduced plant height; under the HS environment (b), healthy leaves in the; under control condition (c), leaf chlorosis under HS (d), and leaf scorching ofleaves (e), and leaf bleaching (f) ofleaflets due to photooxidation under HS (e,f) (Adopted from Devi et al., 2025) |
6.2 Identification and validation of key candidate genes and metabolic pathways
The multi-omics combination approach has identified some important genes, such as CaHSFA5 (heat shock transcription factor), pollen receptor-like kinase 3 (CaPRK3), and flower-promoting factor 1 (CaFPF1). These genes regulate flowering time, pollen germination and plant growth at high temperatures (Kumar et al., 2023). Metabolic pathway analysis also indicated that starch and sucrose metabolism, antioxidant defense, and hormone signaling play key roles in heat tolerance formation (Naveed et al., 2025). These results were verified through functional annotation, gene expression analysis and physiological experiments, indicating that they were indeed associated with high-temperature adaptation (Makonya et al., 2021).
6.3 Application of multi-omics results in developing molecular markers for heat tolerance
Researchers combined genomic, transcriptomic and proteomic data to develop molecular markers related to heat resistance. These markers are related to the major QTL and candidate genes. SNP markers found in heat-tolerant strains have been used for marker-assisted selection, which can help accelerate the breeding of heat-tolerant chickpeas (Paul et al., 2018; Jha et al., 2018) Through Meta-QTL analysis, these markers were further optimized to enhance their accuracy and reliability in breeding (Kumar et al., 2023). This method enables selection in early generations and aggregates favorable alleles together, thereby enhancing the heat tolerance of the variety.
7 Concluding Remarks
The multi-omics approach combines genomics, transcriptomics, proteomics and metabolomics, enabling us to gain a deeper understanding of the heat resistance of chickpeas. These methods have helped scientists identify some key QTLS, candidate genes (such as CaHSFA5, CaPRK3 and WRKY40), proteins and metabolites, and also revealed the complex regulatory networks and physiological processes behind heat tolerance. The combination of multi-omics has also promoted the development of molecular markers, accelerated marker-assisted selection, and provided assistance for the breeding of heat-resistant chickpea varieties.
However, challenges still exist. Heat resistance is controlled by many genes and is also affected by the environment, which makes both research and breeding rather complicated. Many of the QTL confidence intervals discovered now are too large to be directly applied in breeding. Large-scale multi-omics data are also difficult to integrate and interpret, requiring more powerful bioinformatics tools and standardized phenotypic analysis methods, which are not always easy to achieve. The functional verification of candidate genes and the application of omics achievements in the field remain major challenges.
Future research can be approached from several directions. For instance, the scope of QTL can be further narrowed down by using meta-QTL and fine plotting. Multi-omics research can also be extended to epigenomics and phenomics. In the field environment, high-throughput phenotypic analysis methods still need to be improved. Functional genomics, gene editing and systems biology are crucial for verifying candidate genes and clarifying their roles in heat tolerance. By combining multi-omics data with genomic selection and molecular design breeding, there is hope to cultivate chickpea varieties with stronger heat tolerance and greater stability, thereby ensuring yields under climate change.
Acknowledgments
We would like to express our gratitude to the reviewers for their valuable feedback, which helped improve the manuscript.
Conflict of Interest Disclosure
The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.
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