Song Jiaqi, Wang Jiechen, Qin Rui, Ji Guangxin, Cui Congcong, Sun Nan, Qi Siyue, Ding Changjun, Zhang Huihui
{"title":"RNA-Seq-based WGCNA reveals the physiological and molecular responses of poplar leaves to NaHCO3 stress","authors":"Song Jiaqi, Wang Jiechen, Qin Rui, Ji Guangxin, Cui Congcong, Sun Nan, Qi Siyue, Ding Changjun, Zhang Huihui","doi":"10.1007/s00468-024-02577-8","DOIUrl":null,"url":null,"abstract":"<div><h3>Key message</h3><p>ABA and ET signal transduction play key roles in Populus simonii × Populus nigra response to NaHCO3 stress.</p><h3>Abstract</h3><p><i>Populus simonii</i> × <i>Populus nigra</i> is a fast-growing and resilient poplar variety widely promoted in northern China. However, its proliferation is significantly hindered in the Songnen Plain region of northern China due to the prevalence of soda saline-alkali lands primarily composed of NaHCO<sub>3</sub>. Current research on the response and adaptation of <i>Populus simonii</i> × <i>Populus nigra</i> to saline-alkali stress primarily focuses on neutral salts, with limited exploration into the physiological and molecular mechanisms in response to alkaline salt NaHCO<sub>3</sub>. This study utilized physiological and transcriptomic techniques to investigate the effects of different concentrations (0, 100, 200, and 300 mM) of NaHCO<sub>3</sub> stress on the photosynthetic function and antioxidant mechanism of <i>Populus simonii</i> × <i>Populus nigra</i>. Additionally, the key molecular mechanisms underlying its salt-alkali tolerance were explored using WGCNA. The results indicate that, compared to non-stress conditions, under NaHCO<sub>3</sub> stress, differentially expressed genes (DEGs) in <i>Populus simonii</i> × <i>Populus nigra</i> leaves are significantly enriched in KEGG pathways such as Photosynthesis and Plant hormone signal transduction. At 100 mM NaHCO<sub>3</sub>, there is no significant impact on the photosynthetic function of <i>Populus simonii</i> × <i>Populus nigra</i>, with a notable upregulation of numerous DEGs associated with photosynthetic electron transport, suggesting strong resistance of <i>Populus simonii</i> × <i>Populus nigra</i> to NaHCO<sub>3</sub> stress, with hormone signal transduction activation playing a crucial role in its adaptation to NaHCO<sub>3</sub> stress. At high concentration (300 mM) NaHCO<sub>3</sub>, although it inhibits the photosynthetic function of <i>Populus simonii</i> × <i>Populus nigra</i> and leads to severe oxidative damage, KEGG pathways related to antioxidant mechanisms such as Glutathione metabolism and Flavonoid biosynthesis are also significantly enriched. <i>Populus simonii</i> × <i>Populus nigra</i> can mitigate excessive reactive oxygen species (ROS) by increasing the activity of antioxidant enzymes such as Catalase (CAT) and Peroxidase (POD), and the accumulation of the osmotic regulator substance Proline (Pro) also plays a positive role in <i>Populus simonii</i> × <i>Populus nigra</i>'s adaptation to NaHCO<sub>3</sub> stress. Utilizing WGCNA, a module highly correlated with salt tolerance physiological indicators, represented by the \"Mediumorchid\" module, was identified. The KEGG enrichment analysis of DEGs in this module significantly enriched pathways closely associated with Plant hormone signal transduction, particularly the MAPK signaling pathway–plant pathway. Numerous genes in this pathway are involved in the synthesis and signal transduction pathways of Abscisic acid (ABA) and Ethylene (ET). Additionally, the most significantly enriched pathway in the GO functional enrichment analysis of DEGs in this module is “transcription regulator activity”, with the highest number of transcription factors belonging to the ET signal-related ERF family transcription factors (15), and the five highest connectivity hub genes also belong to the ERF family transcription factors, showing significant upregulation induced by NaHCO<sub>3</sub>. In conclusion, <i>Populus simonii</i> × <i>Populus nigra</i> is a poplar variety with strong adaptability to NaHCO<sub>3</sub> stress. The activation of ABA and ET signal transduction-related pathways is a key mechanism for <i>Populus simonii</i> × <i>Populus nigra</i>'s adaptation to NaHCO<sub>3</sub> stress, especially the ERF family transcription factors, which can serve as candidate genes for studying the salt-alkali resistance function of poplar.</p></div>","PeriodicalId":805,"journal":{"name":"Trees","volume":"39 1","pages":""},"PeriodicalIF":2.1000,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Trees","FirstCategoryId":"2","ListUrlMain":"https://link.springer.com/article/10.1007/s00468-024-02577-8","RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"FORESTRY","Score":null,"Total":0}
引用次数: 0
Key message
ABA and ET signal transduction play key roles in Populus simonii × Populus nigra response to NaHCO3 stress.
Abstract
Populus simonii × Populus nigra is a fast-growing and resilient poplar variety widely promoted in northern China. However, its proliferation is significantly hindered in the Songnen Plain region of northern China due to the prevalence of soda saline-alkali lands primarily composed of NaHCO3. Current research on the response and adaptation of Populus simonii × Populus nigra to saline-alkali stress primarily focuses on neutral salts, with limited exploration into the physiological and molecular mechanisms in response to alkaline salt NaHCO3. This study utilized physiological and transcriptomic techniques to investigate the effects of different concentrations (0, 100, 200, and 300 mM) of NaHCO3 stress on the photosynthetic function and antioxidant mechanism of Populus simonii × Populus nigra. Additionally, the key molecular mechanisms underlying its salt-alkali tolerance were explored using WGCNA. The results indicate that, compared to non-stress conditions, under NaHCO3 stress, differentially expressed genes (DEGs) in Populus simonii × Populus nigra leaves are significantly enriched in KEGG pathways such as Photosynthesis and Plant hormone signal transduction. At 100 mM NaHCO3, there is no significant impact on the photosynthetic function of Populus simonii × Populus nigra, with a notable upregulation of numerous DEGs associated with photosynthetic electron transport, suggesting strong resistance of Populus simonii × Populus nigra to NaHCO3 stress, with hormone signal transduction activation playing a crucial role in its adaptation to NaHCO3 stress. At high concentration (300 mM) NaHCO3, although it inhibits the photosynthetic function of Populus simonii × Populus nigra and leads to severe oxidative damage, KEGG pathways related to antioxidant mechanisms such as Glutathione metabolism and Flavonoid biosynthesis are also significantly enriched. Populus simonii × Populus nigra can mitigate excessive reactive oxygen species (ROS) by increasing the activity of antioxidant enzymes such as Catalase (CAT) and Peroxidase (POD), and the accumulation of the osmotic regulator substance Proline (Pro) also plays a positive role in Populus simonii × Populus nigra's adaptation to NaHCO3 stress. Utilizing WGCNA, a module highly correlated with salt tolerance physiological indicators, represented by the "Mediumorchid" module, was identified. The KEGG enrichment analysis of DEGs in this module significantly enriched pathways closely associated with Plant hormone signal transduction, particularly the MAPK signaling pathway–plant pathway. Numerous genes in this pathway are involved in the synthesis and signal transduction pathways of Abscisic acid (ABA) and Ethylene (ET). Additionally, the most significantly enriched pathway in the GO functional enrichment analysis of DEGs in this module is “transcription regulator activity”, with the highest number of transcription factors belonging to the ET signal-related ERF family transcription factors (15), and the five highest connectivity hub genes also belong to the ERF family transcription factors, showing significant upregulation induced by NaHCO3. In conclusion, Populus simonii × Populus nigra is a poplar variety with strong adaptability to NaHCO3 stress. The activation of ABA and ET signal transduction-related pathways is a key mechanism for Populus simonii × Populus nigra's adaptation to NaHCO3 stress, especially the ERF family transcription factors, which can serve as candidate genes for studying the salt-alkali resistance function of poplar.
期刊介绍:
Trees - Structure and Function publishes original articles on the physiology, biochemistry, functional anatomy, structure and ecology of trees and other woody plants. Also presented are articles concerned with pathology and technological problems, when they contribute to the basic understanding of structure and function of trees. In addition to original articles and short communications, the journal publishes reviews on selected topics concerning the structure and function of trees.