Genome-wide transcriptional profiling provides clues to molecular mechanisms underlying cold tolerance in chickpea

Abstract

Chickpea is an important food legume cultivated in several countries. A sudden drop in autumn temperature, freezing winter temperature, and late spring cold events result in significant losses in chickpea production. The current study used RNA sequencing of two cold tolerant (Saral) and sensitive (ILC533) Kabuli chickpea genotypes to identify cold tolerance-associated genes/pathways. A total of 200.85 million raw reads were acquired from the leaf samples by Illumina sequencing, and around 86% of the clean reads (199 million) were mapped to the chickpea reference genome. The results indicated that 3710 (1980 up- and 1730 down-regulated) and 3473 (1972 up- and 1501 down-regulated) genes were expressed differentially under cold stress in the tolerant and sensitive genotypes, respectively. According to the GO enrichment analysis of uniquely down-regulated genes under cold stress in ILC533, photosynthetic membrane, photosystem II, chloroplast part, and photosystem processes were enriched, revealing that the photosynthesis is severely sensitive to cold stress in this sensitive genotype. Many remarkable transcription factors (CaDREB1E, CaMYB4, CaNAC47, CaTCP4, and CaWRKY33), signaling/regulatory genes (CaCDPK4, CaPP2C6, CaMKK2, and CaHSFA3), and protective genes (CaCOR47, CaLEA3, and CaGST) were identified among the cold-responsive genes of the tolerant genotype. These findings would help improve cold tolerance across chickpea genotypes by molecular breeding or genetic engineering.

Freezing stress response of wild and cultivated chickpeas

“…Interestingly, overall, genes related to stress responses, stimuli responses, secondary metabolite processes, and photosynthesis were significantly over-represented in CDC Consul, while Kesen_075 exhibited enrichment in genes linked to endogenous stimulus responses and photosynthesis. Similar responses to cold stress were observed in a recent study in chickpea where cold tolerant and sensitive genotypes were studied at 4°C under control conditions ( Akbari et al., 2023 ). They found that the secondary metabolite pathway and photosynthesis were affected by the cold treatment ( Akbari et al., 2023 ).…”

“…Similar responses to cold stress were observed in a recent study in chickpea where cold tolerant and sensitive genotypes were studied at 4°C under control conditions ( Akbari et al., 2023 ). They found that the secondary metabolite pathway and photosynthesis were affected by the cold treatment ( Akbari et al., 2023 ). Photosynthesis serves as the primary mechanism for harnessing light energy to produce carbohydrates and is disrupted during exposure to lower temperatures in chickpea ( Zeitelhofer et al., 2022 ; Akbari et al., 2023 ).…”

“…We further investigated the ten QTL and identified 2681 genes within their borders ( Supplementary Table 5 ). Among these are 58 that are both differentially expressed and have previously been reported to be involved in cold stress tolerance mechanisms ( Shi et al., 2015 ; Shi et al., 2015 ; Zhu, 2016 ; Abdullah et al., 2022 ; Akbari et al., 2023 ; Raza et al., 2023 ) ( Supplementary Table 6 ). Few of these genes were either up- or down-regulated in both the genotypes whereas some genes were significantly differentially expressed only in one genotype ( Supplementary Table 6 ).…”

“…It hampers the growth, yield, and overall quality of various crop species ( Yadav, 2010 ; Zhu, 2016 ; Kaloki et al., 2019 ). Plants, being immobile organisms, have developed diverse physiological, biochemical, and molecular mechanisms to counteract the effects of cold stress ( Akbari et al., 2023 ; Rastgoo et al., 2023 ). These mechanisms are finely tuned by a complex network of transcription factors and proteins, all working together to enhance a plant’s ability to withstand cold conditions.…”

“…Of these, one QTL was detected in a single environment while the other two QTLs were important in all six environments ( Mugabe et al., 2019 ). Another recent study has reported a few cold responsive genes and proposed potential molecular mechanism related to cold stress tolerance in chickpea ( Akbari et al., 2023 ). More specifically, the researchers found that photosynthesis was severely affected by cold stress.…”