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Highlights • Three tea plant genotypes exhibit different cold tolerance during winter season. • Cold-resistant cultivar had lower ROS content and higher SOD activity. • Cold-resistant cultivar had higher expression levels of genes related to ROS scavenging. • Transcriptomic analysis found the candidate regulators which might confer cold tolerance in tea plant. Abstract Tea plants are sensitive to cold stress and exhibit a high degree of genetic variability for cold tolerance. To understand the networks controlling cold tolerance in tea plants, transcriptome analyses were performed for non-acclimated (NA) and cold-acclimated (CA) conditions using one cold-resistant cultivar and two cold-susceptible cultivars. The comparison analysis found that the candidate regulators, including those involved in the oxidative stress response pathway, genes encoding protein kinases such as MPKs and CIPKs and transcription factors such as WRKYs and MYBs, contributed to the different cold tolerances of the three cultivars. The positive regulatory mechanism of OST1-ICE1 and the negative regulatory mechanism of MPK3-ICE1 were increased and decreased in the cold-resistant cultivar under CA, respectively. Compared with the cold-resistant cultivar, the cold-susceptible cultivars exhibited a higher ROS content along with lower SOD activity in the two-year repeated tests and subsequently experienced more severe leaf damage. The expression levels of ROS production and scavenging genes were higher and lower, respectively, in the two cold-susceptible cultivars under CA. Together, our results indicate that OST1 and MPK3 play vital roles in tea plant cold tolerance regulation, and the activation of ROS-scavenging genes is a primary strategy for tea plants to cope with cold stress during the winter season. [ABSTRACT FROM AUTHOR]

• Four CsInvInhs were identified from three sequenced tea plant genomes. • CsInvInh1/2 may have functional redundancy in tea plant. • CsInvInhs mediate growth and cold response of tea plant mainly by inhibiting AI activity. Invertase inhibitor (InvInh) represses acid invertase (AI) activity though interacting with AI at post-translation level, which plays important roles in vegetative and reproductive processes and stress responses of plant. Our previous studies revealed that CsAI genes were involved in regulating cold response of tea plant, while the post-translation regulation mechanism of AI and the roles of InvInh in tea plant have not been reported yet. Herein, we identified 4 CsInvInhs , including 2 tandem repeat genes (CsInvInh1/2) and 2 segmental duplication genes (CsInvInh3/4), from three sequenced tea plant genomes, and further purified CsInvInh1/2 proteins. Bioinformatics analysis results showed that both of CsInvInh1/2 were located on chromosome (Chr) 5, while CsInvInh3/4 were respectively located on Chr9 and Chr12, which was consistent with the results of inter-species collinearity analysis. Under various abiotic stress conditions, the transcription levels of CsInvInhs were induced with different extent at different treatment time points. In addition, all of CsInvInhs differentially expressed among different tea plant cultivars under drought stress condition. Moreover, CsInvInh1/2 shared similar expression patterns in different tea plant tissues, and under cold stress or cold acclimation conditions, suggesting that CsInvInh1/2 may have functional redundancy in tea plant. Correlation analysis results showed that the changes of CWIN and VIN activities were not significantly correlated with the expression patterns of 5 CsAI genes, while negatively correlated with the expression patterns of 3 CsInvInhs in different tea plant tissues, and under cold stress or cold acclimation conditions, indicating that CsInvInhs participate in growth, development and cold response of tea plant mainly through inhibiting AI activity. These results will provide theoretical foundation for the cold-resistant molecular mechanism of tea plant, and also provide new genetic resources and approaches for cold-resistant molecular breeding of tea plant. [ABSTRACT FROM AUTHOR]