Pub Date : 2026-01-01DOI: 10.1016/j.stress.2025.101212
Qiuling Hui , Emmanouil Flemetakis , Heinz Rennenberg , Bin Hu
Soil salinization and its accompanying soil degradation pose a major threat to plant growth and the sustainability of terrestrial ecosystems worldwide. Therefore, exploring methods to improve the efficiency of phytoremediation of saline soils has been the focus of current research. The symbiosis between biological nitrogen-fixing (BNF) plants and rhizosphere microorganisms plays a crucial role in improving plant resilience and to cope with salt stress. Especially the interaction between nitrogen (N2)-fixing bacteria and mycorrhizal fungi can mitigate the negative effects of salt stress on N2-fixing plants. However, a comprehensive review on the mechanisms of interaction between N2-fixing bacteria and mycorrhizal fungi that confer salt tolerance to N2-fixing plants is still lacking. In this review, we summarize the effects of salt stress on N2-fixing plants and their root colonizing microorganisms with a focus on mechanisms of interaction between N2-fixing bacteria and mycorrhizal fungi under salt stress. These interactions enhance host plant resilience through nutrient complementation, hormonal regulation, and improved antioxidant capacity, but may also be antagonistic through nutrient competition. Finally, we identified research gaps of the analyses of the tripartite symbioses of N2-fixing plants, N2-fixing bacteria, and mycorrhizal fungi to elucidate future research directions.
{"title":"The significance of microbial-root symbioses for the salt tolerance of N2-fixing plants","authors":"Qiuling Hui , Emmanouil Flemetakis , Heinz Rennenberg , Bin Hu","doi":"10.1016/j.stress.2025.101212","DOIUrl":"10.1016/j.stress.2025.101212","url":null,"abstract":"<div><div>Soil salinization and its accompanying soil degradation pose a major threat to plant growth and the sustainability of terrestrial ecosystems worldwide. Therefore, exploring methods to improve the efficiency of phytoremediation of saline soils has been the focus of current research. The symbiosis between biological nitrogen-fixing (BNF) plants and rhizosphere microorganisms plays a crucial role in improving plant resilience and to cope with salt stress. Especially the interaction between nitrogen (N<sub>2</sub>)-fixing bacteria and mycorrhizal fungi can mitigate the negative effects of salt stress on N<sub>2</sub>-fixing plants. However, a comprehensive review on the mechanisms of interaction between N<sub>2</sub>-fixing bacteria and mycorrhizal fungi that confer salt tolerance to N<sub>2</sub>-fixing plants is still lacking. In this review, we summarize the effects of salt stress on N<sub>2</sub>-fixing plants and their root colonizing microorganisms with a focus on mechanisms of interaction between N<sub>2</sub>-fixing bacteria and mycorrhizal fungi under salt stress. These interactions enhance host plant resilience through nutrient complementation, hormonal regulation, and improved antioxidant capacity, but may also be antagonistic through nutrient competition. Finally, we identified research gaps of the analyses of the tripartite symbioses of N<sub>2</sub>-fixing plants, N<sub>2</sub>-fixing bacteria, and mycorrhizal fungi to elucidate future research directions.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101212"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145925159","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2025.101216
Seok-Yeong Jang , Myung-Hwi Kim , Sora Kim , Buyoung Kim , Andika Septiana Suryaningsih , Yu Lim Park , Sun-Jung Kwon , Jang-Kyun Seo
Plant viruses exploit host cellular machinery to fold, stabilize, and target their movement proteins (MPs) to plasmodesmata (PD), enabling viral cell-to-cell and systemic spread. In this study, we identified Nicotiana benthamiana HSP70–HSP90 organizing protein (NbHOP) as a proviral host factor that interacts with the Broad bean wilt virus 2 (BBWV2) MP, VP37. Yeast two-hybrid and co-immunoprecipitation assays revealed a specific interaction between VP37 and NbHOP. Subcellular localization analyses showed that NbHOP, which predominantly accumulates in the nucleus, is relocalized to PD upon co-expression with VP37 or during BBWV2 infection. Bimolecular fluorescence complementation confirmed that VP37 and NbHOP directly interact at PD. Domain mapping further demonstrated that the C-terminal region of TPR2B domain in NbHOP is required for VP37 binding. Functional assays demonstrated that NbHOP is essential for efficient BBWV2 infection: NbHOP silencing significantly reduced both systemic infection and cell-to-cell movement, whereas its overexpression enhanced viral cell-to-cell movement. Together with our previous finding that VP37 associates with HSP90, these results support a model in which VP37 co-opts the HSP90–HOP module to ensure proper folding, stabilization, and tubule formation at PD. This study uncovers an unrecognized role of HOP in plant–virus interactions and highlights the conserved HSP90–HOP chaperone complex as a key host machinery exploited for viral intercellular trafficking.
{"title":"Broad bean wilt virus 2 movement protein VP37 relocalizes the host co-chaperone HOP from the nucleus to plasmodesmata to promote viral intercellular movement","authors":"Seok-Yeong Jang , Myung-Hwi Kim , Sora Kim , Buyoung Kim , Andika Septiana Suryaningsih , Yu Lim Park , Sun-Jung Kwon , Jang-Kyun Seo","doi":"10.1016/j.stress.2025.101216","DOIUrl":"10.1016/j.stress.2025.101216","url":null,"abstract":"<div><div>Plant viruses exploit host cellular machinery to fold, stabilize, and target their movement proteins (MPs) to plasmodesmata (PD), enabling viral cell-to-cell and systemic spread. In this study, we identified <em>Nicotiana benthamiana</em> HSP70–HSP90 organizing protein (NbHOP) as a proviral host factor that interacts with the Broad bean wilt virus 2 (BBWV2) MP, VP37. Yeast two-hybrid and co-immunoprecipitation assays revealed a specific interaction between VP37 and NbHOP. Subcellular localization analyses showed that NbHOP, which predominantly accumulates in the nucleus, is relocalized to PD upon co-expression with VP37 or during BBWV2 infection. Bimolecular fluorescence complementation confirmed that VP37 and NbHOP directly interact at PD. Domain mapping further demonstrated that the C-terminal region of TPR2B domain in NbHOP is required for VP37 binding. Functional assays demonstrated that NbHOP is essential for efficient BBWV2 infection: <em>NbHOP</em> silencing significantly reduced both systemic infection and cell-to-cell movement, whereas its overexpression enhanced viral cell-to-cell movement. Together with our previous finding that VP37 associates with HSP90, these results support a model in which VP37 co-opts the HSP90–HOP module to ensure proper folding, stabilization, and tubule formation at PD. This study uncovers an unrecognized role of HOP in plant–virus interactions and highlights the conserved HSP90–HOP chaperone complex as a key host machinery exploited for viral intercellular trafficking.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101216"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145925236","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Salinity stress is a major abiotic constraint to rice cultivation, limiting growth and yield worldwide. Autophagy, a conserved recycling pathway, and microRNAs (miRNAs), key post-transcriptional regulators, are emerging as central players in stress adaptation, yet their integrated roles in salinity tolerance remain unclear. Here, we compared physiological, biochemical, and molecular responses of two salt-sensitive (IR64, BPT5204) and two salt-tolerant (CSR23, Luna Sankhi) rice varieties under salinity stress. Sensitive varieties showed growth inhibition, oxidative damage, and ion imbalance, whereas tolerant varieties maintained stronger antioxidant activity, selective K⁺ uptake, and osmolyte accumulation. Microscopy and gene expression analyses revealed earlier and stronger autophagy induction in sensitive lines, with differential regulation of ATG5, ATG8d, and ATG12 genes. Heterologous expression of these genes in E. coli enhanced tolerance to salt and osmotic stress, suggesting possible non-canonical roles. Small RNA sequencing indicated salt-stress led upregulation of miRNAs in sensitive varieties targeting autophagy, ion transport, redox balance, and growth pathways. qRT-PCR validation identified osa-miR1432-5p, osa-miR-1861e, and osa-miR-1874-3p as key regulators of autophagy, redox balance, and ionic homeostasis in contrasting genotypes. Notably, osa-miR1432-5p is predicted to target TOR (Target of Rapamycin), a master autophagy regulator, providing a potential direct link between miRNA control and autophagy activation in salt-sensitive rice. These regulatory modules, together with physiological and transcriptional adjustments, distinguish the proactive tolerance of CSR and LS from the reactive stress response of IR and BPT. GO enrichment analysis revealed that BPT suppresses growth and metabolic pathways under salinity, while CSR sustains redox regulation, peroxisomal function, and ion transport, conferring superior stress tolerance. Together, these findings demonstrate that autophagy and miRNA-mediated regulation shape contrasting salinity responses in rice. Tolerant varieties appear to adopt more proactive adaptive responses, while sensitive varieties rely on rapid but costly induction of autophagy and miRNAs. These insights highlight autophagy–miRNA interactions as a potential target for engineering salt-resilient rice.
盐胁迫是水稻种植的主要非生物制约因素，在世界范围内限制了水稻的生长和产量。自噬是一种保守的循环途径，而microrna （miRNAs）是关键的转录后调节因子，它们在胁迫适应中扮演着核心角色，但它们在耐盐性中的综合作用尚不清楚。本研究比较了2个盐敏感水稻品种（IR64、BPT5204）和2个耐盐水稻品种（CSR23、Luna Sankhi）在盐胁迫下的生理生化和分子反应。敏感品种表现出生长抑制、氧化损伤和离子失衡，而耐受性品种保持更强的抗氧化活性、选择性K +吸收和渗透物积累。显微镜和基因表达分析显示，敏感系的自噬诱导更早、更强，ATG5、ATG8d和ATG12基因的差异调控。这些基因在大肠杆菌中的异源表达增强了对盐和渗透胁迫的耐受性，提示可能的非规范作用。小RNA测序表明，盐胁迫导致敏感品种的mirna上调，靶向自噬、离子运输、氧化还原平衡和生长途径。qRT-PCR验证鉴定出osa-miR1432-5p、osa-miR-1861e和osa-miR-1874-3p是对比基因型中自噬、氧化还原平衡和离子稳态的关键调节因子。值得注意的是，预计sa- mir1432 -5p会靶向自噬主调控因子TOR (target of Rapamycin)，这在盐敏感水稻中提供了miRNA控制与自噬激活之间的潜在直接联系。这些调节模块，连同生理和转录调节，将CSR和LS的主动耐受性与IR和BPT的被动应激反应区分开来。氧化石墨烯富集分析表明，BPT在盐度条件下抑制生长和代谢途径，而CSR则维持氧化还原调节、过氧化物酶体功能和离子运输，从而具有更强的抗逆性。总之，这些发现表明，自噬和mirna介导的调控形成了水稻对盐度的不同反应。耐受性品种似乎采取更主动的适应性反应，而敏感品种依赖于快速但昂贵的自噬和mirna诱导。这些发现突出了自噬- mirna相互作用作为工程盐抗性水稻的潜在靶标。
{"title":"Differential induction of autophagy and miRNA-mediated regulation modulate salt tolerance in contrasting rice varieties","authors":"Ashwini Talakayala , Navdeep Kaur , Wricha Tyagi , Pratap Kumar Pati , P.B. Kirti , Isha Sharma","doi":"10.1016/j.stress.2025.101200","DOIUrl":"10.1016/j.stress.2025.101200","url":null,"abstract":"<div><div>Salinity stress is a major abiotic constraint to rice cultivation, limiting growth and yield worldwide. Autophagy, a conserved recycling pathway, and microRNAs (miRNAs), key post-transcriptional regulators, are emerging as central players in stress adaptation, yet their integrated roles in salinity tolerance remain unclear. Here, we compared physiological, biochemical, and molecular responses of two salt-sensitive (IR64, BPT5204) and two salt-tolerant (CSR23, Luna Sankhi) rice varieties under salinity stress. Sensitive varieties showed growth inhibition, oxidative damage, and ion imbalance, whereas tolerant varieties maintained stronger antioxidant activity, selective K⁺ uptake, and osmolyte accumulation. Microscopy and gene expression analyses revealed earlier and stronger autophagy induction in sensitive lines, with differential regulation of <em>ATG5, ATG8d,</em> and <em>ATG12</em> genes. Heterologous expression of these genes in <em>E. coli</em> enhanced tolerance to salt and osmotic stress, suggesting possible non-canonical roles. Small RNA sequencing indicated salt-stress led upregulation of miRNAs in sensitive varieties targeting autophagy, ion transport, redox balance, and growth pathways. qRT-PCR validation identified <em>osa-miR1432-5p, osa-miR-1861e</em>, and <em>osa-miR-1874-3p</em> as key regulators of autophagy, redox balance, and ionic homeostasis in contrasting genotypes. Notably, <em>osa-miR1432-5p</em> is predicted to target <em>TOR</em> (Target of Rapamycin), a master autophagy regulator, providing a potential direct link between miRNA control and autophagy activation in salt-sensitive rice. These regulatory modules, together with physiological and transcriptional adjustments, distinguish the proactive tolerance of CSR and LS from the reactive stress response of IR and BPT. GO enrichment analysis revealed that BPT suppresses growth and metabolic pathways under salinity, while CSR sustains redox regulation, peroxisomal function, and ion transport, conferring superior stress tolerance. Together, these findings demonstrate that autophagy and miRNA-mediated regulation shape contrasting salinity responses in rice. Tolerant varieties appear to adopt more proactive adaptive responses, while sensitive varieties rely on rapid but costly induction of autophagy and miRNAs. These insights highlight autophagy–miRNA interactions as a potential target for engineering salt-resilient rice.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101200"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145976888","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2026.101229
Ramadoss Dhanuskodi , Yanni Dong , Cory Matthew , Tsanko Gechev , Paul P. Dijkwel
Legumes can fix nitrogen (N) by symbiotic N-fixation (SNF) through association with rhizobia. However, this comes at a higher carbon cost to the host as compared to direct N fertiliser uptake. We therefore hypothesised that the energy-intensive symbiosis process imposes additional growth and yield penalties to the SNF-dependent host under drought.
Medicago truncatula seedlings were either rhizobium-inoculated or N-fertilised, drought stress was applied 20 days post inoculation by withholding water for 12 days, and physiological and transcriptomic responses were measured.
Physiological analysis revealed that drought similarly reduced leaf water status in both rhizobium-inoculated and N-fertilised plants. However, only rhizobium-inoculated plants sustained N-acquisition and growth. Transcriptomic analysis revealed that these plants pre-activated jasmonic acid, proline, and trehalose biosynthesis before the onset of drought stress, and induced stress-tolerance hormone pathways in response to the drought. In contrast, N-fertilised plants acquired less N, upregulated ethylene biosynthesis and senescence, and induced strong death responses. Remarkably, despite contrasting molecular strategies, both plants achieved similar dry matter and yield when drought conditions continued throughout the plants’ lifecycle.
Contrary to our hypothesis, the results suggested that rhizobium-inoculated plants activated a tolerance mechanism through a priming-like response and sustained N-fixation under drought stress, whereas N-fertilised plants induced a contrasting survival strategy based on growth cessation and leaf senescence. This study advances our understanding of the distinct survival mechanisms of SNF-dependent and N-fertilised legumes under drought, and provides critical insights for advancing sustainable and climate-resilient crops by harnessing rhizobial symbiosis benefits.
{"title":"The rhizobium symbiosis in Medicago truncatula induces a priming-like response and enhances drought tolerance","authors":"Ramadoss Dhanuskodi , Yanni Dong , Cory Matthew , Tsanko Gechev , Paul P. Dijkwel","doi":"10.1016/j.stress.2026.101229","DOIUrl":"10.1016/j.stress.2026.101229","url":null,"abstract":"<div><div>Legumes can fix nitrogen (N) by symbiotic N-fixation (SNF) through association with rhizobia. However, this comes at a higher carbon cost to the host as compared to direct N fertiliser uptake. We therefore hypothesised that the energy-intensive symbiosis process imposes additional growth and yield penalties to the SNF-dependent host under drought.</div><div><em>Medicago truncatula</em> seedlings were either rhizobium-inoculated or N-fertilised, drought stress was applied 20 days post inoculation by withholding water for 12 days, and physiological and transcriptomic responses were measured.</div><div>Physiological analysis revealed that drought similarly reduced leaf water status in both rhizobium-inoculated and N-fertilised plants. However, only rhizobium-inoculated plants sustained N-acquisition and growth. Transcriptomic analysis revealed that these plants pre-activated jasmonic acid, proline, and trehalose biosynthesis before the onset of drought stress, and induced stress-tolerance hormone pathways in response to the drought. In contrast, N-fertilised plants acquired less N, upregulated ethylene biosynthesis and senescence, and induced strong death responses. Remarkably, despite contrasting molecular strategies, both plants achieved similar dry matter and yield when drought conditions continued throughout the plants’ lifecycle.</div><div>Contrary to our hypothesis, the results suggested that rhizobium-inoculated plants activated a tolerance mechanism through a priming-like response and sustained N-fixation under drought stress, whereas N-fertilised plants induced a contrasting survival strategy based on growth cessation and leaf senescence. This study advances our understanding of the distinct survival mechanisms of SNF-dependent and N-fertilised legumes under drought, and provides critical insights for advancing sustainable and climate-resilient crops by harnessing rhizobial symbiosis benefits.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101229"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145976892","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2025.101199
Qiangqiang Zhang , Xiu Deng , Xinzheng Han , Jian Ke , Haibing He , Cuicui You , Liquan Wu
Improving the adaptability of rice leaves to high-light under heat stress is essential for maximizing photosynthetic efficiency. This study examined the responses of leaf gas exchange and hydraulic parameters to intense light under heat stress (40 °C) in wild type (Nipponbare) and four genetically modified rice varieties (NAL1-K, NAL1-O, Ghd7.1-K, and Ghd7.1-O) that exhibited significant differences in leaf area (LA). When measured irradiance increased from 1000 to 2000 μmol m-2 s-1 under heat stress, the changes of photosynthetic rate (A2000-A1000) ranged from -2.8 μmol m-2 s-1 in NAL1-O to 14.9 μmol m-2 s-1 in NAL1-K. A negative correlation between A2000-A1000 and LA was observed. The varying responses of A to high-light were primarily associated with stomatal conductance (gs). Enhanced leaf hydraulic conductance (Kleaf) facilitated the gs response to high-light under heat stress conditions. Furthermore, this study revealed that, under high-light and heat stress conditions, Kleaf is predominantly regulated by leaf hydraulic conductance inside the xylem (Kx), and reduced LA can significantly improve Kx. These findings demonstrate that reducing LA can enhance Kleaf, thereby improving the response of A to high-light under heat stress.
{"title":"Reduced leaf size enhances photosynthetic acclimation to high-light under heat stress by enhancing hydraulic conductance in rice","authors":"Qiangqiang Zhang , Xiu Deng , Xinzheng Han , Jian Ke , Haibing He , Cuicui You , Liquan Wu","doi":"10.1016/j.stress.2025.101199","DOIUrl":"10.1016/j.stress.2025.101199","url":null,"abstract":"<div><div>Improving the adaptability of rice leaves to high-light under heat stress is essential for maximizing photosynthetic efficiency. This study examined the responses of leaf gas exchange and hydraulic parameters to intense light under heat stress (40 °C) in wild type (<em>Nipponbare</em>) and four genetically modified rice varieties (<em>NAL1-K, NAL1-O, Ghd7.1-K,</em> and <em>Ghd7.1-O</em>) that exhibited significant differences in leaf area (<em>LA</em>). When measured irradiance increased from 1000 to 2000 μmol m<sup>-2</sup> s<sup>-1</sup> under heat stress, the changes of photosynthetic rate (<em>A</em><sub>2000</sub><em>-A</em><sub>1000</sub>) ranged from -2.8 μmol m<sup>-2</sup> s<sup>-1</sup> in <em>NAL1-O</em> to 14.9 μmol m<sup>-2</sup> s<sup>-1</sup> in <em>NAL1-K</em>. A negative correlation between <em>A</em><sub>2000</sub><em>-A</em><sub>1000</sub> and <em>LA</em> was observed. The varying responses of <em>A</em> to high-light were primarily associated with stomatal conductance (<em>g</em><sub>s</sub>). Enhanced leaf hydraulic conductance (<em>K</em><sub>leaf</sub>) facilitated the <em>g</em><sub>s</sub> response to high-light under heat stress conditions. Furthermore, this study revealed that, under high-light and heat stress conditions, <em>K</em><sub>leaf</sub> is predominantly regulated by leaf hydraulic conductance inside the xylem (<em>K</em><sub>x</sub>), and reduced <em>LA</em> can significantly improve <em>K</em><sub>x</sub>. These findings demonstrate that reducing <em>LA</em> can enhance <em>K</em><sub>leaf</sub>, thereby improving the response of <em>A</em> to high-light under heat stress.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101199"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145924649","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2025.101182
Youwei Zhang , Rui Geng , Guokang Chen , Shuai Yuan , Lei Wang , Heping Fu
Melatonin is a conserved multifunctional signaling molecule in plants, which regulates many developmental processes and responds to stress. Although many studies have involved melatonin in plants, it is not clear whether the application of exogenous melatonin can improve their tolerance to salt damage NaCl + Na2SO4 (2:1). This study investigated the effects of different concentrations of melatonin (0, 50, 100, 150, 200, and 250 μmol·L-1) on seed germination, physiological characteristics, and transcriptome (12d) of Sophora alopecuroides under salt stress at different time (3d, 6d, 9d and 12d). The results showed that on the 12th day of salt stress, the germination rate (37.88 %), radicle (16.67 %), germ (38.87 %), total chlorophyll content (72.48 %), transpiration rate (45.17 %) decreased, and H2O2 (24.26 %), malondialdehyde content (10.95 %) increased. In particular, exogenous melatonin at 50 μmol·L-1can improve the germination index of Sophora alopecuroides seeds under salt stress, increase plant growth, biomass accumulation, root activity, regulate stomatal conductance and intercellular CO2 concentration, and improve photosynthetic efficiency. In addition, exogenous melatonin also reduced MDA content and reactive oxygen species (ROS)accumulation, alleviated oxidative damage and increased enzymatic and non-enzymatic antioxidant activities, including catalase, superoxide dismutase, polyphenol oxidase, peroxidase, flavonoids and carotenoids. Exogenous melatonin also promoted the accumulation of growth-related endogenous hormones (GA, IAA, MT) and the ability to change gene expression patterns. Discussion Transcriptomics analysis revealed significant changes in gene expression, especially in the comparison of T0 and T1 treatment groups. 4761 differentially expressed genes (DEGs) were identified, including arginine and proline metabolism, zeatin biosynthesis, pentose and glucuronic acid mutual transformation, galactose metabolism, and peroxisome synthesis pathways, which are essential for plant responses to salt stress. Our results provide preliminary mechanistic insights into how melatonin alleviates the combined salt stress of S. alopecuroides, and lay the foundation for molecular breeding strategies to enhance the salt tolerance of this crop.
{"title":"Molecular mechanisms of melatonin in mitigating compound salt stress in Sophora alopecuroides revealed by physiological and transcriptomic profiling","authors":"Youwei Zhang , Rui Geng , Guokang Chen , Shuai Yuan , Lei Wang , Heping Fu","doi":"10.1016/j.stress.2025.101182","DOIUrl":"10.1016/j.stress.2025.101182","url":null,"abstract":"<div><div>Melatonin is a conserved multifunctional signaling molecule in plants, which regulates many developmental processes and responds to stress. Although many studies have involved melatonin in plants, it is not clear whether the application of exogenous melatonin can improve their tolerance to salt damage NaCl + Na<sub>2</sub>SO<sub>4</sub> (2:1). This study investigated the effects of different concentrations of melatonin (0, 50, 100, 150, 200, and 250 μmol·L<sup>-1</sup>) on seed germination, physiological characteristics, and transcriptome (12d) of <em>Sophora alopecuroides</em> under salt stress at different time (3d, 6d, 9d and 12d). The results showed that on the 12th day of salt stress, the germination rate (37.88 %), radicle (16.67 %), germ (38.87 %), total chlorophyll content (72.48 %), transpiration rate (45.17 %) decreased, and H<sub>2</sub>O<sub>2</sub> (24.26 %), malondialdehyde content (10.95 %) increased. In particular, exogenous melatonin at 50 μmol·L<sup>-1</sup>can improve the germination index of <em>Sophora alopecuroides</em> seeds under salt stress, increase plant growth, biomass accumulation, root activity, regulate stomatal conductance and intercellular CO<sub>2</sub> concentration, and improve photosynthetic efficiency. In addition, exogenous melatonin also reduced MDA content and reactive oxygen species (ROS)accumulation, alleviated oxidative damage and increased enzymatic and non-enzymatic antioxidant activities, including catalase, superoxide dismutase, polyphenol oxidase, peroxidase, flavonoids and carotenoids. Exogenous melatonin also promoted the accumulation of growth-related endogenous hormones (GA, IAA, MT) and the ability to change gene expression patterns. Discussion Transcriptomics analysis revealed significant changes in gene expression, especially in the comparison of T0 and T1 treatment groups. 4761 differentially expressed genes (DEGs) were identified, including arginine and proline metabolism, zeatin biosynthesis, pentose and glucuronic acid mutual transformation, galactose metabolism, and peroxisome synthesis pathways, which are essential for plant responses to salt stress. Our results provide preliminary mechanistic insights into how melatonin alleviates the combined salt stress of <em>S. alopecuroides</em>, and lay the foundation for molecular breeding strategies to enhance the salt tolerance of this crop.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101182"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145924641","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2025.101156
Xianguan Zhi , Jiahui Yao , Shu Yao, Wenqi Deng, Ling Yan, Huihui Zhai, Chi Huang, Kaiyue Guo, Yang Gao, Chenchen Wang, XiaoBo Wang, Jiajia Li
High-temperature (HT) stress impairs soybean yield by disrupting anther function. miRNAs are critical regulators of plant stress responses, but their roles in soybean anther thermotolerance remain largely unexplored. We performed small RNA sequencing of anthers from HT-tolerant (JD21) and HT-sensitive (HD14) soybean lines under HT and control conditions. Comparative analysis revealed that HT- stress JD21 anthers (TJA) exhibited 16 up-regulated and 19 down-regulated differentially expressed miRNAs (DEMs) compared to controls (CJA), while HT-stress HD14 anthers (THA) showed 17 up-regulated and 24 down-regulated DEMs relative to its control (CHA). The HD14 exhibited more DEMs, potentially explaining JD21′s superior HT resistance. Integrated analysis of miRNA and mRNA expression identified 23 DEMs with targeted regulatory relationships to 43 differentially expressed genes (DEGs) (p<0.05). Bioinformatics analysis indicated that these target genes were primarily enriched in metabolic and cellular processes, response to stimuli, calvin cycle carbon fixation, and carbon metabolism. From this group, eight candidate miRNAs, including novel-m0226–5p (miR226–5p), miR5037c, and miR159e-5p, were selected for further investigation. Functional validation in Arabidopsis thaliana demonstrated that overexpression of miR226–5p, miR5037c, or miR159e-5p resulted in premature anthers non-dehiscence under HT stress, respectively. Furthermore, miR159e-5p overexpression lines specifically showed significantly reduced expression of heat shock transcription factors (HSFA1s) and heat shock proteins (HSPs), supporting a role for this miRNA in regulating thermotolerance. This study establishes as a central regulator of the soybean anther HT response via modulation of the HSFA1s-HSPs network, providing molecular insights into thermotolerance and potential targets for breeding HT-resistant soybean varieties.
{"title":"The role mechanism of miRNA regulating anther dehiscence in soybean under high temperature stress","authors":"Xianguan Zhi , Jiahui Yao , Shu Yao, Wenqi Deng, Ling Yan, Huihui Zhai, Chi Huang, Kaiyue Guo, Yang Gao, Chenchen Wang, XiaoBo Wang, Jiajia Li","doi":"10.1016/j.stress.2025.101156","DOIUrl":"10.1016/j.stress.2025.101156","url":null,"abstract":"<div><div>High-temperature (HT) stress impairs soybean yield by disrupting anther function. miRNAs are critical regulators of plant stress responses, but their roles in soybean anther thermotolerance remain largely unexplored. We performed small RNA sequencing of anthers from HT-tolerant (JD21) and HT-sensitive (HD14) soybean lines under HT and control conditions. Comparative analysis revealed that HT- stress JD21 anthers (TJA) exhibited 16 up-regulated and 19 down-regulated differentially expressed miRNAs (DEMs) compared to controls (CJA), while HT-stress HD14 anthers (THA) showed 17 up-regulated and 24 down-regulated DEMs relative to its control (CHA). The HD14 exhibited more DEMs, potentially explaining JD21′s superior HT resistance. Integrated analysis of miRNA and mRNA expression identified 23 DEMs with targeted regulatory relationships to 43 differentially expressed genes (DEGs) (<em>p<0.05</em>). Bioinformatics analysis indicated that these target genes were primarily enriched in metabolic and cellular processes, response to stimuli, calvin cycle carbon fixation, and carbon metabolism. From this group, eight candidate miRNAs, including <em>novel-m0226–5p</em> (<em>miR226–5p</em>), <em>miR5037c</em>, and <em>miR159e-5p</em>, were selected for further investigation. Functional validation in <em>Arabidopsis thaliana</em> demonstrated that overexpression of <em>miR226–5p, miR5037c</em>, or <em>miR159e-5p</em> resulted in premature anthers non-dehiscence under HT stress, respectively. Furthermore, <em>miR159e-5p</em> overexpression lines specifically showed significantly reduced expression of heat shock transcription factors (HSFA1s) and heat shock proteins (HSPs), supporting a role for this miRNA in regulating thermotolerance. This study establishes as a central regulator of the soybean anther HT response via modulation of the HSFA1s-HSPs network, providing molecular insights into thermotolerance and potential targets for breeding HT-resistant soybean varieties.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101156"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145925158","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2026.101218
Yachun Su , Zhuqing Wang , Yurong Luo , Qiugang Ding , Yifei Xia , Shoujian Zang , Tingting Sun , Khushi Muhammad , Chuihuai You , Youxiong Que
Class III peroxidases (PODs) are crucial for plant growth and stress responses, yet few have been characterized in sugarcane (Saccharum spp.). In this study, elevated POD activity was detected across eight sugarcane genotypes during their interaction with Sporisorium scitamineum, suggesting a role in smut defense. To further explore this gene family, 174 SoPOD genes, classified into seven subgroups, were identified in S. officinarum LA-purple. Family expansion primarily was assumed to result from whole-genome/segmental duplications (83.90 %), with Ka/Ks < 1 in 92.86 % of gene pairs. SoPOD promoters were enriched in stress- and hormone-related cis-regulatory elements. Transcriptome data revealed that SoPOD expression was tissue-specific and responsive to cold, drought, and S. scitamineum infection. Notably, SoPOD30 was exclusively upregulated in the resistant cultivar after infection but undetectable in the susceptible one. Its homolog ScPOD01 was subsequently isolated from sugarcane hybrid cultivars and shown to possess a canonical four-exon/three-intron gene structure and plasma membrane localization. Real-time quantitative PCR demonstrated ScPOD01 induction by S. scitamineum infection across all eight cultivars and under various abiotic stresses (abscisic acid, methyl jasmonate, hydrogen peroxide, polyethylene glycol, and sodium chloride). Interestingly, the transient expression of ScPOD01 in Nicotiana benthamiana activated immune responses, as evidenced by intensified DAB staining and upregulation of hypersensitive reaction- and SA-related genes, however its prokaryotic expression did not enhance bacterial stress tolerance. These findings uncover the evolutionary diversification and expression specificity of the sugarcane POD family and elucidate the immune function of ScPOD01, laying a foundation for understanding POD roles in sugarcane disease resistance.
{"title":"Decoding the genomic landscape of class III peroxidase family in Saccharum officinarum and the immune role of ScPOD01","authors":"Yachun Su , Zhuqing Wang , Yurong Luo , Qiugang Ding , Yifei Xia , Shoujian Zang , Tingting Sun , Khushi Muhammad , Chuihuai You , Youxiong Que","doi":"10.1016/j.stress.2026.101218","DOIUrl":"10.1016/j.stress.2026.101218","url":null,"abstract":"<div><div>Class III peroxidases (PODs) are crucial for plant growth and stress responses, yet few have been characterized in sugarcane (<em>Saccharum</em> spp.). In this study, elevated POD activity was detected across eight sugarcane genotypes during their interaction with <em>Sporisorium scitamineum</em>, suggesting a role in smut defense. To further explore this gene family, 174 <em>SoPOD</em> genes, classified into seven subgroups, were identified in <em>S. officinarum</em> LA-purple. Family expansion primarily was assumed to result from whole-genome/segmental duplications (83.90 %), with Ka/Ks < 1 in 92.86 % of gene pairs. <em>SoPOD</em> promoters were enriched in stress- and hormone-related <em>cis</em>-regulatory elements. Transcriptome data revealed that <em>SoPOD</em> expression was tissue-specific and responsive to cold, drought, and <em>S. scitamineum</em> infection. Notably, <em>SoPOD30</em> was exclusively upregulated in the resistant cultivar after infection but undetectable in the susceptible one. Its homolog <em>ScPOD01</em> was subsequently isolated from sugarcane hybrid cultivars and shown to possess a canonical four-exon/three-intron gene structure and plasma membrane localization. Real-time quantitative PCR demonstrated <em>ScPOD01</em> induction by <em>S. scitamineum</em> infection across all eight cultivars and under various abiotic stresses (abscisic acid, methyl jasmonate, hydrogen peroxide, polyethylene glycol, and sodium chloride). Interestingly, the transient expression of <em>ScPOD01</em> in <em>Nicotiana benthamiana</em> activated immune responses, as evidenced by intensified DAB staining and upregulation of hypersensitive reaction- and SA-related genes, however its prokaryotic expression did not enhance bacterial stress tolerance. These findings uncover the evolutionary diversification and expression specificity of the sugarcane POD family and elucidate the immune function of <em>ScPOD01</em>, laying a foundation for understanding <em>POD</em> roles in sugarcane disease resistance.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101218"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145925156","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2026.101245
Zedi Feng , Jiacen Wang , Zhifang Jiang , Xiaomei Wu , Jia Yao , Wenyuan Wu , Chaogang Shao , Xiaoxia Ma , Yijun Meng
Plants are sessile organisms vulnerable to environmental fluctuations. For survival, they have developed fascinating strategies to respond to the environmental stimuli. However, the molecular basis underlying the differentiated environmental responses among distinct plant species or subspecies remains under investigation. In this study, seven Arabidopsis ecotypes (Col-0 as the reference) and six rice varieties (Nipponbare as the reference) with distinct habitat parameters were selected to explore the molecular clues. Based on the transcriptome-wide m6A profiles, 1,428 to 3,099, and 1,295 to 2,766 differential m6A peaks associated with the protein-coding genes were identified from distinct subspecies of Arabidopsis and rice respectively. These peaks are highly enriched at the 3′ ends of the transcripts, and the genes containing higher numbers of the exons are more susceptible to hypo-methylation. Orthologous gene analysis showed that around 30% of the differential peak-associated genes shared common functions between Arabidopsis and rice. Functional annotations and analysis of the stress-treated methylome data supported the involvement of the differential peak-associated genes in environmental responses. In-depth mechanism study showed that both m6A modification and SNPs were likely to have a direct impact on differential exon expression. The influence of m6A modification was also observed on the expression of circRNAs whose host genes are environment-responsive. Summarily, our results provided the genomic and epitranscriptomic clues for the differential expression of the stress-responsive genes which might lead to the differential environmental responses at the subspecies level.
{"title":"Involvement of genomic variations and m6A modification in differential gene expression related to environmental responses: A subspecies-level study in plants","authors":"Zedi Feng , Jiacen Wang , Zhifang Jiang , Xiaomei Wu , Jia Yao , Wenyuan Wu , Chaogang Shao , Xiaoxia Ma , Yijun Meng","doi":"10.1016/j.stress.2026.101245","DOIUrl":"10.1016/j.stress.2026.101245","url":null,"abstract":"<div><div>Plants are sessile organisms vulnerable to environmental fluctuations. For survival, they have developed fascinating strategies to respond to the environmental stimuli. However, the molecular basis underlying the differentiated environmental responses among distinct plant species or subspecies remains under investigation. In this study, seven <em>Arabidopsis</em> ecotypes (Col-0 as the reference) and six rice varieties (Nipponbare as the reference) with distinct habitat parameters were selected to explore the molecular clues. Based on the transcriptome-wide m<sup>6</sup>A profiles, 1,428 to 3,099, and 1,295 to 2,766 differential m<sup>6</sup>A peaks associated with the protein-coding genes were identified from distinct subspecies of <em>Arabidopsis</em> and rice respectively. These peaks are highly enriched at the 3′ ends of the transcripts, and the genes containing higher numbers of the exons are more susceptible to hypo-methylation. Orthologous gene analysis showed that around 30% of the differential peak-associated genes shared common functions between <em>Arabidopsis</em> and rice. Functional annotations and analysis of the stress-treated methylome data supported the involvement of the differential peak-associated genes in environmental responses. In-depth mechanism study showed that both m<sup>6</sup>A modification and SNPs were likely to have a direct impact on differential exon expression. The influence of m<sup>6</sup>A modification was also observed on the expression of circRNAs whose host genes are environment-responsive. Summarily, our results provided the genomic and epitranscriptomic clues for the differential expression of the stress-responsive genes which might lead to the differential environmental responses at the subspecies level.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101245"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146022520","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-01DOI: 10.1016/j.stress.2025.101206
Yuli Huang , Wenting Yuan , Lei Zhang , Pan Yang , Li Huang , Jiangming Ma , Zhiyong Zhang , Haimiao Wang
Clonal integration enables ramets to share resources by stolon, enhancing their adaptability to patches of heterogeneous resource supply in clonal plants. However, how clonal plants regulate photosynthetic capacity, endogenous protective enzymes and phytohormones to survive from heterogeneous drought were poorly understood. A pot experiment was conducted under heterogeneous drought conditions in mother and daughter plants in A. trewioides. Experiment treatments included (ⅰ) both well-watered mother and daughter plants (CK), (ⅱ) mother plant exposed to drought (SRWC of 45 ± 5 % for 9 days) + daughter plant well-watered (T1), and (ⅲ) mother plant well-watered + daughter plant exposed to drought (T2). Results showed that chlorophyll content and photosynthetic parameters were significantly reduced in drought plants whatever mother or daughter plants. However, daughter plants performed more vulnerable than mother plants when they were suffering from drought stress. Besides, hydrogen peroxide (H2O2) and malondialdehyde (MDA) in mother plants were significantly increased for treatment T1 compared with CK. In comparison, H2O2, superoxide dismutase (SOD) and peroxidase (POD) were significantly increased by 41.87 %, 15.68 % and 11.70 % in daughter plants for treatment T1 compared with CK. Moreover, abscisic acid (ABA) level was remarkedly increased in mother plants for treatment T1 relative to CK. Simultaneously, brassinosteroid (BR) and zeaxanthin (ZT) levels in daughter plants exhibited a significant increasing trend during rewatering stage for treatment T1 relative to CK. Furthermore, SOD and catalase (CAT) in daughter plants were notably increased by 142.28 % and 21.8 % for treatment T2 compared with CK. Interestingly, CAT and ABA were also increased by 33.54 % and 19.6 % in mother plants for treatment T2 compared with CK. Therefore, we concluded that clonal plants could up-regulated SOD, CAT and POD activities as well as phytohormones such as ABA, BR and ZT levels both in mother and daughter plants whoever suffering from drought stress, more interestingly, mother plants would enhanced activities of some endogenous protective enzyme and phytohormone, eg. CAT and ABA, in despite of mother plant well-watered, when connected daughter plant was exposed to drought stress, thereby promoting their adaptive capacity. These results were expected to provide a theoretical basis for understanding physiological integration characteristic to promote their adaptions to drought environmental surroundings in clonal plants.
{"title":"Plant drought tolerance was enhanced by positively regulating endogenous protective enzymes activities and phytohormones levels in a clonal plant of A. trewioides","authors":"Yuli Huang , Wenting Yuan , Lei Zhang , Pan Yang , Li Huang , Jiangming Ma , Zhiyong Zhang , Haimiao Wang","doi":"10.1016/j.stress.2025.101206","DOIUrl":"10.1016/j.stress.2025.101206","url":null,"abstract":"<div><div>Clonal integration enables ramets to share resources by stolon, enhancing their adaptability to patches of heterogeneous resource supply in clonal plants. However, how clonal plants regulate photosynthetic capacity, endogenous protective enzymes and phytohormones to survive from heterogeneous drought were poorly understood. A pot experiment was conducted under heterogeneous drought conditions in mother and daughter plants in <em>A. trewioides.</em> Experiment treatments included (ⅰ) both well-watered mother and daughter plants (CK), (ⅱ) mother plant exposed to drought (SRWC of 45 ± 5 % for 9 days) + daughter plant well-watered (T<sub>1</sub>), and (ⅲ) mother plant well-watered + daughter plant exposed to drought (T<sub>2</sub>). Results showed that chlorophyll content and photosynthetic parameters were significantly reduced in drought plants whatever mother or daughter plants. However, daughter plants performed more vulnerable than mother plants when they were suffering from drought stress. Besides, hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) and malondialdehyde (MDA) in mother plants were significantly increased for treatment T<sub>1</sub> compared with CK. In comparison, H<sub>2</sub>O<sub>2,</sub> superoxide dismutase (SOD) and peroxidase (POD) were significantly increased by 41.87 %, 15.68 % and 11.70 % in daughter plants for treatment T<sub>1</sub> compared with CK. Moreover, abscisic acid (ABA) level was remarkedly increased in mother plants for treatment T<sub>1</sub> relative to CK. Simultaneously, brassinosteroid (BR) and zeaxanthin (ZT) levels in daughter plants exhibited a significant increasing trend during rewatering stage for treatment T<sub>1</sub> relative to CK. Furthermore, SOD and catalase (CAT) in daughter plants were notably increased by 142.28 % and 21.8 % for treatment T<sub>2</sub> compared with CK. Interestingly, CAT and ABA were also increased by 33.54 % and 19.6 % in mother plants for treatment T<sub>2</sub> compared with CK. Therefore, we concluded that clonal plants could up-regulated SOD, CAT and POD activities as well as phytohormones such as ABA, BR and ZT levels both in mother and daughter plants whoever suffering from drought stress, more interestingly, mother plants would enhanced activities of some endogenous protective enzyme and phytohormone, eg. CAT and ABA, in despite of mother plant well-watered, when connected daughter plant was exposed to drought stress, thereby promoting their adaptive capacity. These results were expected to provide a theoretical basis for understanding physiological integration characteristic to promote their adaptions to drought environmental surroundings in clonal plants.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"19 ","pages":"Article 101206"},"PeriodicalIF":6.8,"publicationDate":"2026-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145924647","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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