Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)

Lidiia Samarina; Songbo Wang; Lyudmila Malyukova; Alexandr Bobrovskikh; Alexey Doroshkov; Natalia Koninskaya; Ruset Shkhalakhova; Alexandra Matskiv; Jaroslava Fedorina; Anastasia Fizikova; Karina Manakhova; Svetlana Loshkaryova; Tsiala Tutberidze; Alexey Ryndin; Elena Khlestkina

doi:10.3389/fpls.2023.1145793

Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)

Front Plant Sci. 2023 May 10:14:1145793. doi: 10.3389/fpls.2023.1145793. eCollection 2023.

Authors

Lidiia Samarina^{1

2}, Songbo Wang¹, Lyudmila Malyukova¹, Alexandr Bobrovskikh³, Alexey Doroshkov³, Natalia Koninskaya¹, Ruset Shkhalakhova¹, Alexandra Matskiv¹, Jaroslava Fedorina^{1

2}, Anastasia Fizikova^{1

2}, Karina Manakhova^{1

2}, Svetlana Loshkaryova¹, Tsiala Tutberidze¹, Alexey Ryndin¹, Elena Khlestkina^{2

4}

Affiliations

¹ Federal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, Russia.
² Center of Genetics and Life Sciences, Sirius University of Science and Technology, Sirius, Russia.
³ Institute of Cytology and Genetics Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia.
⁴ Federal Research Center, N. I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR), Saint Petersburg, Russia.

Abstract

Introduction: Low temperatures and drought are two main environmental constraints reducing the yield and geographical distribution of horticultural crops worldwide. Understanding the genetic crosstalk between stress responses has potential importance for crop improvement.

Methods: In this study, Illumina RNA-seq and Pac-Bio genome resequencing were used to annotate genes and analyze transcriptome dynamics in tea plants under long-term cold, freezing, and drought.

Results: The highest number of differentially expressed genes (DEGs) was identified under long-term cold (7,896) and freezing (7,915), with 3,532 and 3,780 upregulated genes, respectively. The lowest number of DEGs was observed under 3-day drought (47) and 9-day drought (220), with five and 112 genes upregulated, respectively. The recovery after the cold had 6.5 times greater DEG numbers as compared to the drought recovery. Only 17.9% of cold-induced genes were upregulated by drought. In total, 1,492 transcription factor genes related to 57 families were identified. However, only 20 transcription factor genes were commonly upregulated by cold, freezing, and drought. Among the 232 common upregulated DEGs, most were related to signal transduction, cell wall remodeling, and lipid metabolism. Co-expression analysis and network reconstruction showed 19 genes with the highest co-expression connectivity: seven genes are related to cell wall remodeling (GATL7, UXS4, PRP-F1, 4CL, UEL-1, UDP-Arap, and TBL32), four genes are related to calcium-signaling (PXL1, Strap, CRT, and CIPK6), three genes are related to photo-perception (GIL1, CHUP1, and DnaJ11), two genes are related to hormone signaling (TTL3 and GID1C-like), two genes are involved in ROS signaling (ERO1 and CXE11), and one gene is related to the phenylpropanoid pathway (GALT6).

Discussion: Based on our results, several important overlapping mechanisms of long-term stress responses include cell wall remodeling through lignin biosynthesis, o-acetylation of polysaccharides, pectin biosynthesis and branching, and xyloglucan and arabinogalactan biosynthesis. This study provides new insight into long-term stress responses in woody crops, and a set of new target candidate genes were identified for molecular breeding aimed at tolerance to abiotic stresses.

Keywords: cell wall biosynthesis; coexpression analysis; differentially expressed genes; light perception; lipid metabolism; phenilpropanoid pathway; stress tolerance; tea plant (Camellia sinensis).

Grants and funding

The study was funded by a grant from the Russian Science Foundation # 18-76-10001 (https://rscf.ru/project/21-76-03003/). Plant material for this study was provided by a program of the Ministry of Science and Higher Education of the Russian Federation (program # FGRW-2021-0008). All experiments with plants were conducted at Federal Research Centre the Subtropical Scientific Centre of the Russian Academy of Sciences. Data analysis and the manuscript processing were conducted at the Sirius University of Science and Technology and the N. I. Vavilov All-Russian Institute of Plant Genetic Resources. Gene network reconstruction was performed at the Institute of Cytology and Genetics.