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.
关键信息aba和ET信号转导在胡杨×黑胡杨对NaHCO3胁迫的响应中起关键作用。摘要黑杨（Populus simmonii × Populus nigra）是中国北方广泛推广的速生抗逆性强的杨树品种。然而，在松嫩平原地区，由于主要由NaHCO3组成的钠盐碱地普遍存在，其扩散受到明显阻碍。目前关于胡杨（Populus simmonii × Populus nigra）对盐碱胁迫的响应和适应研究主要集中在中性盐方面，对碱盐NaHCO3的生理和分子机制探索较少。本研究利用生理和转录组学技术，研究了不同浓度（0、100、200和300 mM） NaHCO3胁迫对simonii × Populus nigra光合功能和抗氧化机制的影响。此外，利用WGCNA对其耐盐碱的关键分子机制进行了探讨。结果表明，与非胁迫条件相比，NaHCO3胁迫下，simonii × Populus nigra叶片中参与光合作用和植物激素信号转导等KEGG通路的差异表达基因（DEGs）显著富集。在100 mM NaHCO3条件下，simmonii × Populus nigra的光合功能没有受到显著影响，但与光合电子传递相关的多个deg显著上调，说明simmonii × Populus nigra对NaHCO3胁迫具有较强的抗性，其中激素信号转导的激活在其适应NaHCO3胁迫中起着至关重要的作用。高浓度（300 mM） NaHCO3虽然抑制了simonii × Populus nigra的光合功能，导致严重的氧化损伤，但与谷胱甘肽代谢、类黄酮生物合成等抗氧化机制相关的KEGG通路也显著富集。黑杨通过提高过氧化氢酶（CAT）和过氧化物酶（POD）等抗氧化酶的活性来缓解过多的活性氧（ROS），渗透调节物质脯氨酸（Pro）的积累也对黑杨适应NaHCO3胁迫起着积极的作用。利用WGCNA，鉴定出一个与耐盐生理指标高度相关的模块，以“中兰”模块为代表。本模块对DEGs进行KEGG富集分析，发现与植物激素信号转导密切相关的通路，特别是MAPK信号通路-植物通路显著富集。该途径中有许多基因参与脱落酸（ABA）和乙烯（ET）的合成和信号转导途径。此外，在本模块对DEGs的GO功能富集分析中，富集最显著的途径是“转录调节因子活性”，属于ET信号相关的ERF家族转录因子的转录因子数量最多（15个），最高的5个连接枢纽基因也属于ERF家族转录因子，均表现出NaHCO3诱导的显著上调。综上所述，黑杨是一个对NaHCO3胁迫适应性强的杨树品种。ABA和ET信号转导相关通路的激活是杨树适应NaHCO3胁迫的关键机制，尤其是ERF家族转录因子，可以作为研究杨树耐盐碱功能的候选基因。
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.
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