Zheng Shizhong, Liu Chufei, Zhou Ziwei, Xu Liyi, Ruan Biyuan, Chen Xiaohui
College of Biological Science and Engineering, Ningde Normal University, Ningde, China.
Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, China.
Front Plant Sci. 2024 Dec 5;15:1481169. doi: 10.3389/fpls.2024.1481169. eCollection 2024.
Heat stress is one of the main environmental factors limiting the growth, yield and quality of tea plants (). Trehalose involved in plant responses to multiple adverse environmental stresses, including heat stress. However, the roles of circular RNAs (circRNAs) and their involvement in the trehalose response to heat stress remain unknown.
In this study, circRNA-sequencing was performed to analyze the characteristics of circRNAs in trehalose-induced responses to heat stress in tea plants. Kyoto Encyclopedia of Genes and Genomes enrichment analysis was used to determine the potential function of circRNAs, and the expression of differentially expressed circRNAs (DECs) and their host genes related to Non-homologous end-joining (NHEJ) and Homologous recombination (HR) were analyzed. To further explore the effect of trehalose on DNA double strand breaks (DSBs), the reactive oxygen species (ROS) contents, specially hydrogen peroxide (HO) and superoxide anion (O2), in heat-stressed tea plants were investigated.
A total of 11402 circRNAs were detected from CK, T (heat stress) and TT (heat stress + trehalose) samples. Among these circRNAs, 573, 620 and 550 circRNAs were identified as differentially expressed in the T vs. CK, TT vs. CK and TT vs. T comparison groups, respectively. The host genes of DECs were enriched in NHEJ and HR pathways, implying a critical role of circRNAs in DSBs repair. The expression level of circKu70-1 and circKu70-3 showed positive correlations with their host gene, , while circKu70-2 exhibited an opposite expression trend. Similarly, circRad50 displayed a negative correlation with its host gene, . Notably, the expression of and , which are crucial for initiating DSB repair, was decreased in the trehalose-treated (TT) samples. This finding suggests that trehalose may play a role in modulating the expression of circRNAs and their host genes involved in NHEJ and HR pathways, ultimately contributing to reduced DSB damage during heat stress. Moreover, exogenous trehalose significantly reduced HO and O2 contents in tea plants under heat stress, suggesting that trehalose could mitigate heat-induced damage resulting from ROS overproduction.
Our results indicated that circRNAs play a crucial role in maintaining genome integrity. Specifically, they may function as molecular hubs that respond to changes of the levels of HO and O2 induced by trehalose, and subsequently regulate the DSBs mediated by their host genes. This, in turn, further impacts genome stability, ultimately enhancing heat tolerance in tea plants. Our findings provided new insight into the potential applications of trehalose as an agrochemical in tea plants and revealed the potential role of circRNAs in tea plants heat tolerance.
热胁迫是限制茶树生长、产量和品质的主要环境因素之一。海藻糖参与植物对多种逆境胁迫的响应，包括热胁迫。然而，环状RNA（circRNA）的作用及其在海藻糖对热胁迫响应中的参与情况尚不清楚。
在本研究中，进行了circRNA测序以分析茶树中海藻糖诱导的热胁迫响应中circRNA的特征。使用京都基因与基因组百科全书富集分析来确定circRNA的潜在功能，并分析差异表达的circRNA（DEC）及其与非同源末端连接（NHEJ）和同源重组（HR）相关的宿主基因的表达。为了进一步探究海藻糖对DNA双链断裂（DSB）的影响，研究了热胁迫茶树中活性氧（ROS）的含量，特别是过氧化氢（HO）和超氧阴离子（O2）。
从CK、T（热胁迫）和TT（热胁迫 + 海藻糖）样本中共检测到11402个circRNA。在这些circRNA中，分别在T与CK、TT与CK以及TT与T比较组中鉴定出573、620和550个差异表达的circRNA。DEC的宿主基因在NHEJ和HR途径中富集，这意味着circRNA在DSB修复中起关键作用。circKu70 - 1和circKu70 - 3的表达水平与其宿主基因呈正相关，而circKu70 - 2表现出相反的表达趋势。同样，circRad50与其宿主基因呈负相关。值得注意的是，在海藻糖处理的（TT）样本中，对启动DSB修复至关重要的 和 的表达降低。这一发现表明，海藻糖可能在调节参与NHEJ和HR途径的circRNA及其宿主基因的表达中发挥作用，最终有助于减少热胁迫期间的DSB损伤。此外，外源海藻糖显著降低了热胁迫下茶树中HO和O2的含量，表明海藻糖可以减轻ROS过量产生导致的热诱导损伤。
我们的结果表明，circRNA在维持基因组完整性方面起关键作用。具体而言，它们可能作为分子枢纽，响应海藻糖诱导的HO和O2水平变化，随后调节其宿主基因介导的DSB。这反过来又进一步影响基因组稳定性，最终提高茶树的耐热性。我们的研究结果为海藻糖作为茶树农用化学品的潜在应用提供了新的见解，并揭示了circRNA在茶树耐热性中的潜在作用。
