Effect of shading on physiological attributes and comparative transcriptome analysis of Camellia sinensis cultivar reveals tolerance mechanisms to low temperatures

Abstract

Tea is a vital beverage crop all over the world, including in China. Low temperatures restrict its growth, development, and terrestrial distribution, and cold event variability worsens cold damage. However, the physiological and molecular mechanisms of Camellia sinensis under shade in winter remain unclear. In our study, tea leaves were utilized for physiological attributes and transcriptome analysis in November and December in three shading groups and no-shade control plants. When compared to the no-shade control plants, the shading group protected tea leaves from cold damage, increased photochemical efficiency (Fv/Fm) and soil plant analysis development (SPAD), and sustained chlorophyll a, chlorophyll b, chlorophyll, and carotenoid contents by physiological mean. Then, transcriptome analysis revealed 20,807 differentially expressed genes (DEGs) and transcription factors (TFs) in November and December. A comparative study of transcriptome resulted in 3,523 DEGs and many TFs under SD0% vs. SD30%, SD0% vs. SD60%, and SD0% vs. SD75% of shading in November and December. Statistically, 114 DEGs were downregulated and 72 were upregulated under SD0% vs. SD30%. SD0% vs. SD60% resulted in 154 DEGs, with 60 downregulated and 94 upregulated. Similarly, there were 505 DEGs of which 244 were downregulated and 263 were upregulated under SD0% vs. SD75% of shading throughout November. However, 279 DEGs were downregulated and 105 were upregulated under SD0% vs. SD30%. SD0% vs. SD60% resulted in 296 DEGs, with 172 downregulated and 124 upregulated. Finally, 2,173 DEGs were regulated in December, with 1,428 downregulated and 745 upregulated under SD0% vs. SD75%. These indicate that the number of downregulated DEGs in December was higher than the number of upregulated DEGs in November during low temperatures. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses of differentially expressed genes were highly regulated in the photosynthesis, plant hormone signal transduction, and mitogen-activated protein kinase (MAPK) signaling pathways. However, qRT-PCR and RNA-seq relative expression of photosynthetic (DEGs) Lhcb2 in both November and December, plant hormone (DEGs) BRI1 and JAZ in November and IAA and ERF1 in December, and key DEGs of MAPK signal transduction FLS2, CHIB, and MPK4 in November and RBOH, MKK4_5, and MEKK1 in December in three shading groups and no-shade control plants responded to tea cold tolerance. The enhanced expression of light-harvesting photosystem I gene Lhca5, light-harvesting photosystem II gene Lhcb2, and mitogen-activated protein kinases MEKK1 and MPK4/6 enhance the cold-tolerance mechanism of C. sinensis. These comprehensive transcriptomic findings are significant for furthering our understanding of the genes and underlying regulatory mechanisms of shade-mediated low-temperature stress tolerance in horticultural crops.

Molecular mechanisms underlying coordinated responses of plants to shade and environmental stresses

“…It should be noted that when plants are suffering both shade and cold stress, the combinative effects of shade and cold tend to enhance cold tolerance in Arabidopsis, tomato, tobacco and Camellia sinensis through CBF‐dependent or CBF‐independent pathways (Franklin & Whitelam, 2007; Huang et al., 2016; Patel et al., 2013; Wang et al., 2016, 2018; Wang, Yan, et al., 2020; Zaman et al., 2023). However, although PIF4 promotes cold tolerance in tomato, all PIFs characterized so far negatively regulate cold tolerance in Arabidopsis (Jiang et al., 2017; Kidokoro et al., 2009; Lee & Thomashow, 2012; Wang, Chen, et al., 2020).…”

Effect of Shading on Physiological Attributes and Proteomic Analysis of Tea during Low Temperatures

“…Low temperatures have a significant impact on the chloroplast, which is the primary organelle affected by cold exposure in plants. The effect of low temperatures on tea cell membranes leads to changes in their structure and shape, the restriction of cell membrane permeability, and damage to the cell membranes in tea leaves [ 3 ]. This damage hinders the ability to recuperate from stress due to the loss of cellular integrity.…”

“…This damage hinders the ability to recuperate from stress due to the loss of cellular integrity. Several studies have been undertaken on the effects of low temperature on tea growth and the development of morphological, physiological, and gene expression characteristics [ 3 , 4 , 5 ]. Plants emit stress signals and trigger many transcription factors when they perceive low temperatures.…”

“…These variables contribute to the plant’s capacity to withstand stress and regulate the activation of genes that react to cold and other environmental stimuli [ 6 ]. Ultimately, this results in the altering of multiple biological processes, including photosynthesis, signaling, transcription, metabolism, cell wall modification, biochemical changes, physiological adaptation, and metabolic changes [ 1 , 3 ]. Low temperatures pose significant limitations on plants, leading to various changes in their structure, physiology, and biochemistry.…”

“…The effect of shading on tea plants grown during low temperatures can depend on several environmental factors such as the specific tea cultivar, the duration of shade, and the intensity, severity, and duration of the low temperatures [ 3 , 16 ]. In our previous study, we also reported that 60% of shade-sheltered tea leaves during mild temperatures inhibited cold damage and enhanced the cellular attributes during low temperatures.…”