Transcriptome Profiling of Maize (Zea mays L.) Leaves Reveals Key Cold-Responsive Genes, Transcription Factors, and Metabolic Pathways Regulating Cold Stress Tolerance at the Seedling Stage

Abstract

Cold tolerance is a complex trait that requires a critical perspective to understand its underpinning mechanism. To unravel the molecular framework underlying maize (Zea mays L.) cold stress tolerance, we conducted a comparative transcriptome profiling of 24 cold-tolerant and 22 cold-sensitive inbred lines affected by cold stress at the seedling stage. Using the RNA-seq method, we identified 2237 differentially expressed genes (DEGs), namely 1656 and 581 annotated and unannotated DEGs, respectively. Further analysis of the 1656 annotated DEGs mined out two critical sets of cold-responsive DEGs, namely 779 and 877 DEGs, which were significantly enhanced in the tolerant and sensitive lines, respectively. Functional analysis of the 1656 DEGs highlighted the enrichment of signaling, carotenoid, lipid metabolism, transcription factors (TFs), peroxisome, and amino acid metabolism. A total of 147 TFs belonging to 32 families, including MYB, ERF, NAC, WRKY, bHLH, MIKC MADS, and C2H2, were strongly altered by cold stress. Moreover, the tolerant lines’ 779 enhanced DEGs were predominantly associated with carotenoid, ABC transporter, glutathione, lipid metabolism, and amino acid metabolism. In comparison, the cold-sensitive lines’ 877 enhanced DEGs were significantly enriched for MAPK signaling, peroxisome, ribosome, and carbon metabolism pathways. The biggest proportion of the unannotated DEGs was implicated in the roles of long non-coding RNAs (lncRNAs). Taken together, this study provides valuable insights that offer a deeper understanding of the molecular mechanisms underlying maize response to cold stress at the seedling stage, thus opening up possibilities for a breeding program of maize tolerance to cold stress.

Metabolic Insight into Cold Stress Response in Two Contrasting Maize Lines

“…Moreover, Chen et al [94] provided evidence for improved cold tolerance in maize under exogenous application of abscisic acid. A recent study concerning cold tolerance in maize depicted up-accumulation of ZEP, NCED, β-carotene isomerase β-carotene 3-hydroxylase, and ABA 8 -hydroxylase under cold stress [10]. Our results depicted up-accumulation of Feruloyltartaric acid (Fertaric acid), and Sinapyl alcohol under stress conditions in B144.…”

“…Protein oxidation by ROS is considered irreversible; however, proteins with sulfur-containing amino acids are an exception [76]. A previous report [10] addressing the cold tolerance in maize at the seedling stage suggested upregulation of genes encoding β-alanine aminotransferase and glutamate decarboxylase involved in the biosynthesis of β-alanine betaine and γ-aminobutyric acid, which play a crucial role in plant development under environmental stresses [77][78][79]. Our study depicted up-accumulation of 3-Hydroxy-3-methylpentane-1,5-dioic acid, L-Lysine-Butanoic Acid, L-Leucyl-L-phenylalanine, L-Alanyl-L-Phenylalanine, L-Glutamine, L-Lysine, L-Valyl-L-Phenylalanine, and L-Aspartyl-L-Phenylalanine in B144 under cold stress.…”

“…Disorganized cell membrane, altered osmotic stress, denatured proteins, and increased reactive oxygen species (ROS) could result in oxidative damage are among primary responses [47]. The sessile nature of plants helps develop complex responsive mechanisms, including multiple pathways under stress conditions [10,48]. Regulation pathways under cold stress may vary from species to species [49].…”

“…Therefore, chilling susceptibility in maize crop is one of the major concerns for optimum yield, which is drastically reduced when the plant is subjected to early-stage cold stress [6,7]. Although much work has been done to understand the biological mechanisms behind cold tolerance [8][9][10], there is a lack of studies addressing the metabolic responses resulting in increased/decreased tolerance levels in maize.…”

Effect of different seedling growing methods on the SPAD, NDVI values and some morphological parameters of four sweet corn (Zea mays L.) hybrids

“…Cold stress -one of these impeding abiotic stress factors -negatively affects corn growth from germination to harvest, resulting in considerable yield depressions. Cold stress harms plant growth and yield due to several abnormalities in physiological, molecular, and biochemical processes (Waititu et al 2021).…”