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Comparative transcriptomic analysis and identification of candidate genes related to Verticillium wilt resistance in Gossypium barbadense and Gossypium hirsutum
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-02-05 DOI: 10.1016/j.stress.2025.100759
Jieyin Zhao , Xingui Hu , Yuxiang Wang, Jiaxin Lu, Wenju Gao, Xuening Su, Quanjia Chen, Yanying Qu
The resistance to Verticillium wilt in Gossypium barbadense is generally greater than that in Gossypium hirsutum, and analyzing the differences in the mechanism and regulatory genes involved in Verticillium wilt resistance between G. barbadense and G. hirsutum is particularly important. Here, we report a transcriptomic study for phenotypic evaluation of Verticillium wilt resistance in G. hirsutum (TM-1) and G. barbadense (Hai7124) and a comparison of the transcriptomes at 7 time points after Verticillium dahliae inoculation. Phenotypic evaluation revealed that, compared with TM-1, Hai7124 was more resistant to Verticillium wilt. A total of 18,138 differentially expressed genes (DEGs), including 1470 transcription factors (TFs). Further analysis of the expression of hormone biosynthesis- and signal transduction-related genes revealed that most of the genes in the salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) biosynthesis pathways were highly expressed in Hai7124; the expression of SA and JA biosynthesis genes began to be significantly upregulated in the early stage of Verticillium wilt stress, while the expression of ET biosynthesis genes was upregulated mainly in the later stage. WGCNA-based binding sequence comparison revealed that MYB14 had nonsynonymous single nucleotide polymorphisms (SNPs) in 5 highly Verticillium wilt-resistant G. barbadense varieties compared to 5 highly Verticillium wilt-susceptible G. hirsutum varieties. Expression analysis revealed that GbMYB14 responded more rapidly to Verticillium wilt stress than the same gene in G. hirsutum. The resistance of G. barbadense and G. hirsutum to Verticillium wilt decreased after MYB14 silencing via virus induced gene silencing (VIGS), and leaf yellowing and necrosis in the GbMYB14-silenced plants were more obvious. Compared with those in G. hirsutum, the expression levels and of lignin biosynthesis pathway genes and the lignin content in GbMYB14-silenced plants were lower. In conclusion, our results provide a theoretical basis for an in-depth understanding of the molecular mechanism underlying the difference in Verticillium wilt resistance between G. barbadense and G. hirsutum and provide a new genetic resource for the study of cotton resistance to Verticillium wilt.
{"title":"Comparative transcriptomic analysis and identification of candidate genes related to Verticillium wilt resistance in Gossypium barbadense and Gossypium hirsutum","authors":"Jieyin Zhao ,&nbsp;Xingui Hu ,&nbsp;Yuxiang Wang,&nbsp;Jiaxin Lu,&nbsp;Wenju Gao,&nbsp;Xuening Su,&nbsp;Quanjia Chen,&nbsp;Yanying Qu","doi":"10.1016/j.stress.2025.100759","DOIUrl":"10.1016/j.stress.2025.100759","url":null,"abstract":"<div><div>The resistance to Verticillium wilt in <em>Gossypium barbadense</em> is generally greater than that in <em>Gossypium hirsutum</em>, and analyzing the differences in the mechanism and regulatory genes involved in Verticillium wilt resistance between G<em>. barbadense</em> and G<em>. hirsutum</em> is particularly important. Here, we report a transcriptomic study for phenotypic evaluation of Verticillium wilt resistance in G<em>. hirsutum</em> (TM-1) and G<em>. barbadense</em> (Hai7124) and a comparison of the transcriptomes at 7 time points after <em>Verticillium dahliae</em> inoculation. Phenotypic evaluation revealed that, compared with TM-1, Hai7124 was more resistant to Verticillium wilt. A total of 18,138 differentially expressed genes (DEGs), including 1470 transcription factors (TFs). Further analysis of the expression of hormone biosynthesis- and signal transduction-related genes revealed that most of the genes in the salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) biosynthesis pathways were highly expressed in Hai7124; the expression of SA and JA biosynthesis genes began to be significantly upregulated in the early stage of Verticillium wilt stress, while the expression of ET biosynthesis genes was upregulated mainly in the later stage. WGCNA-based binding sequence comparison revealed that MYB14 had nonsynonymous single nucleotide polymorphisms (SNPs) in 5 highly Verticillium wilt-resistant G<em>. barbadense</em> varieties compared to 5 highly Verticillium wilt-susceptible G<em>. hirsutum</em> varieties. Expression analysis revealed that <em>GbMYB14</em> responded more rapidly to Verticillium wilt stress than the same gene in G<em>. hirsutum</em>. The resistance of G<em>. barbadense</em> and G<em>. hirsutum</em> to Verticillium wilt decreased after MYB14 silencing via virus induced gene silencing (VIGS), and leaf yellowing and necrosis in the <em>GbMYB14</em>-silenced plants were more obvious. Compared with those in G<em>. hirsutum</em>, the expression levels and of lignin biosynthesis pathway genes and the lignin content in <em>GbMYB14</em>-silenced plants were lower. In conclusion, our results provide a theoretical basis for an in-depth understanding of the molecular mechanism underlying the difference in Verticillium wilt resistance between G<em>. barbadense</em> and G<em>. hirsutum</em> and provide a new genetic resource for the study of cotton resistance to Verticillium wilt.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100759"},"PeriodicalIF":6.8,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143330786","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Small open reading frames (sORFs): Driving big improvements in plant development and quality
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-02-05 DOI: 10.1016/j.stress.2025.100761
Kui Dong, Chaofan Shan, Dongyu Wen, Zifan Cui, Jun Cao
Small open reading frames (sORFs) are defined as short nucleotide sequences, typically no longer than 300 base pairs, which have the potential to encode small peptides. With the advent of sophisticated technologies such as bioinformatics, ribosome profiling, and mass spectrometry, the investigation of sORFs has experienced a transformative shift and significant expansion. This review provides a comprehensive analysis of the identification, categorization, functional mechanisms, and diverse roles of sORFs in plant development. In the plant, sORFs are pivotal components that enhance responses to both biotic and abiotic stresses by encoding small peptides that are either intricately involved in complex hormone regulation and signaling networks, or precisely regulate the expression of downstream resistance genes. The impact of sORFs extends well beyond stress resistance and they are also implicated in the developmental and physiological functions of plants. sORFs play a crucial role in determing the overall morphological architecture of plants, governing morphological changes throughout the plant life cycle, and are instrumental in regulating metabolite accumulation, which influences plant quality. The synergistic application of sORFs with gene editing technologies holds great promise, not only for devising novel strategies to improve plant quality, resulting in crops that are more resistant, nutrient-rich, and productive, but also for establishing innovative molecular breeding pathways. In summary, understanding and harnessing the potential of sORFs is a cutting-edge area of research that is poised to revolutionize the future of plant biology and agriculture, and ongoing exploration of their functions and mechanisms is anticipated to yield groundbreaking discoveries and practical applications in the future.
{"title":"Small open reading frames (sORFs): Driving big improvements in plant development and quality","authors":"Kui Dong,&nbsp;Chaofan Shan,&nbsp;Dongyu Wen,&nbsp;Zifan Cui,&nbsp;Jun Cao","doi":"10.1016/j.stress.2025.100761","DOIUrl":"10.1016/j.stress.2025.100761","url":null,"abstract":"<div><div>Small open reading frames (sORFs) are defined as short nucleotide sequences, typically no longer than 300 base pairs, which have the potential to encode small peptides. With the advent of sophisticated technologies such as bioinformatics, ribosome profiling, and mass spectrometry, the investigation of sORFs has experienced a transformative shift and significant expansion. This review provides a comprehensive analysis of the identification, categorization, functional mechanisms, and diverse roles of sORFs in plant development. In the plant, sORFs are pivotal components that enhance responses to both biotic and abiotic stresses by encoding small peptides that are either intricately involved in complex hormone regulation and signaling networks, or precisely regulate the expression of downstream resistance genes. The impact of sORFs extends well beyond stress resistance and they are also implicated in the developmental and physiological functions of plants. sORFs play a crucial role in determing the overall morphological architecture of plants, governing morphological changes throughout the plant life cycle, and are instrumental in regulating metabolite accumulation, which influences plant quality. The synergistic application of sORFs with gene editing technologies holds great promise, not only for devising novel strategies to improve plant quality, resulting in crops that are more resistant, nutrient-rich, and productive, but also for establishing innovative molecular breeding pathways. In summary, understanding and harnessing the potential of sORFs is a cutting-edge area of research that is poised to revolutionize the future of plant biology and agriculture, and ongoing exploration of their functions and mechanisms is anticipated to yield groundbreaking discoveries and practical applications in the future.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100761"},"PeriodicalIF":6.8,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143377250","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
GmERF57 negatively regulates root development and phosphate absorption in soybean
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-02-05 DOI: 10.1016/j.stress.2025.100763
Hongqing Zhu , Dandan Hu , Yifei Yang , Xuhao Zhai , Shanshan Zhang , Mengshi He , Huifang Zuo , Lina Zhang , Mengjun Xu , Shanshan Chu , Haiyan Lü , Hengyou Zhang , Yu Zhang , Dan Zhang
Low soil phosphate (Pi) availability is a primary limiting factor for crop growth and production due to its immobilization in soil, thereby impeding Pi uptake by plants. However, excessive supply of phosphorus fertilizer can result in eutrophication of water bodies. Therefore, improving Pi utilization and uptake efficiency in plants is crucial for sustainable agriculture. Previously, we identified soybean Ethylene Response Factor 57 (GmERF57) as a candidate gene responsible for q20, a major QTL associated with soybean low Pi (LP) tolerance-related traits identified through QTL mapping and genome-wide association analysis (GWAS). Population genomics analysis revealed that GmERF57 has undergone artificial selection, and allelic distribution analysis significantly correlated with traits associated with LP tolerance in soybean. Haplotype 2 (Hap2), carrying the T to C single nucleotide polymorphism (SNP), represents the optimal allele favoring LP tolerance. Silencing GmERF57 expression promoted root development and enhanced plant Pi uptake; conversely, overexpression of GmERF57 yielded contrasting phenotypes compared to silenced roots. We further uncovered that GmERF57 physically interacts with GmTUB1 (β-tubulin protein) and modulates soybean root architecture and Pi uptake capacity by downregulating GmTUB1 and other Pi starvation response genes. Overall, the results identified GmERF57 as a QTL gene associated with LP tolerance, elucidated its role in regulating LP tolerance, and further identified an optimal haplotype to facilitate breeding of LP-tolerant soybean cultivars.
{"title":"GmERF57 negatively regulates root development and phosphate absorption in soybean","authors":"Hongqing Zhu ,&nbsp;Dandan Hu ,&nbsp;Yifei Yang ,&nbsp;Xuhao Zhai ,&nbsp;Shanshan Zhang ,&nbsp;Mengshi He ,&nbsp;Huifang Zuo ,&nbsp;Lina Zhang ,&nbsp;Mengjun Xu ,&nbsp;Shanshan Chu ,&nbsp;Haiyan Lü ,&nbsp;Hengyou Zhang ,&nbsp;Yu Zhang ,&nbsp;Dan Zhang","doi":"10.1016/j.stress.2025.100763","DOIUrl":"10.1016/j.stress.2025.100763","url":null,"abstract":"<div><div>Low soil phosphate (Pi) availability is a primary limiting factor for crop growth and production due to its immobilization in soil, thereby impeding Pi uptake by plants. However, excessive supply of phosphorus fertilizer can result in eutrophication of water bodies. Therefore, improving Pi utilization and uptake efficiency in plants is crucial for sustainable agriculture. Previously, we identified soybean Ethylene Response Factor 57 (<em>GmERF57</em>) as a candidate gene responsible for <em>q20</em>, a major QTL associated with soybean low Pi (LP) tolerance-related traits identified through QTL mapping and genome-wide association analysis (GWAS). Population genomics analysis revealed that <em>GmERF57</em> has undergone artificial selection, and allelic distribution analysis significantly correlated with traits associated with LP tolerance in soybean. Haplotype 2 (Hap2), carrying the T to C single nucleotide polymorphism (SNP), represents the optimal allele favoring LP tolerance. Silencing <em>GmERF57</em> expression promoted root development and enhanced plant Pi uptake; conversely, overexpression of <em>GmERF57</em> yielded contrasting phenotypes compared to silenced roots. We further uncovered that GmERF57 physically interacts with GmTUB1 (β-tubulin protein) and modulates soybean root architecture and Pi uptake capacity by downregulating <em>GmTUB1</em> and other Pi starvation response genes. Overall, the results identified <em>GmERF57</em> as a QTL gene associated with LP tolerance, elucidated its role in regulating LP tolerance, and further identified an optimal haplotype to facilitate breeding of LP-tolerant soybean cultivars.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100763"},"PeriodicalIF":6.8,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143348782","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-02-05 DOI: 10.1016/j.stress.2025.100762
Jiqiang Yin , Ying Sun , Xinping Miao , Jiaxin Qu , Kunjie Zhang , Xue qing Han , Yichi Li , Jiahui Sun , Fanna Kong
The microfilament (MF) cytoskeleton, present in all eukaryotic cells, is not only essential for fundamental cellular processes but also is important in sensing and transducing external signals in response to various developmental cues and abiotic stresses. Neopyropia yezoensis, a species of seaweed belonging to the Rhodophyta, is an important macroalga that thrives in the intertidal zone. However, it remains uncertain whether the MF cytoskeleton of seaweed contributes to adaption to desiccation and rehydration. In this study, we present for the first time the evidence regarding the role of MFs in the desiccation tolerance of N. yezoensis. The organization and arrangement of MFs were significantly influenced by variations in the water content within thallus cells. Desiccation of the thallus induced changes of many actin and actin binding proteins (ABPs) at transcriptional, translational and post-translational phosphorylation levels. Notably, nine phosphosites from four proteins (actin, formin, septin, and fascin) showed changes in phosphorylation conditions. This indicate that phosphorylation modification was involved in MFs response to desiccation and rehydration stress. Transcriptome analysis revealed that Latrunculin A, an MF polymerization inhibitor, significantly suppressed the expression of actin and ABPs genes. Further analysis indicated that MF participates in the responses to desiccation in N. yezoensis by regulating plastid function, ROS levels, phosphorylation modification of proteins, Ca2+ signals and vesicle transport processes. Additionally, two MYB transcriptional factors were identified as being induced by regulating the MF cytoskeleton assembly. Finally, we developed a hypothesis concerning the regulation of the microfilament skeleton as a fundamental response to water loss in thalli of N. yezoensis. Our findings will enhance our understanding the adaption mechanisms of N. yezoensis to water stress and broaden our knowledge regarding the response of MF cytoskeleton to water stress. Furthermore, this research will provide valuable insights into the species distribution of intertidal zones.
{"title":"Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone","authors":"Jiqiang Yin ,&nbsp;Ying Sun ,&nbsp;Xinping Miao ,&nbsp;Jiaxin Qu ,&nbsp;Kunjie Zhang ,&nbsp;Xue qing Han ,&nbsp;Yichi Li ,&nbsp;Jiahui Sun ,&nbsp;Fanna Kong","doi":"10.1016/j.stress.2025.100762","DOIUrl":"10.1016/j.stress.2025.100762","url":null,"abstract":"<div><div>The microfilament (MF) cytoskeleton, present in all eukaryotic cells, is not only essential for fundamental cellular processes but also is important in sensing and transducing external signals in response to various developmental cues and abiotic stresses. <em>Neopyropia yezoensis</em>, a species of seaweed belonging to the Rhodophyta, is an important macroalga that thrives in the intertidal zone. However, it remains uncertain whether the MF cytoskeleton of seaweed contributes to adaption to desiccation and rehydration. In this study, we present for the first time the evidence regarding the role of MFs in the desiccation tolerance of <em>N. yezoensis</em>. The organization and arrangement of MFs were significantly influenced by variations in the water content within thallus cells. Desiccation of the thallus induced changes of many actin and actin binding proteins (ABPs) at transcriptional, translational and post-translational phosphorylation levels. Notably, nine phosphosites from four proteins (actin, formin, septin, and fascin) showed changes in phosphorylation conditions. This indicate that phosphorylation modification was involved in MFs response to desiccation and rehydration stress. Transcriptome analysis revealed that Latrunculin A, an MF polymerization inhibitor, significantly suppressed the expression of actin and ABPs genes. Further analysis indicated that MF participates in the responses to desiccation in <em>N. yezoensis</em> by regulating plastid function, ROS levels, phosphorylation modification of proteins, Ca<sup>2+</sup> signals and vesicle transport processes. Additionally, two MYB transcriptional factors were identified as being induced by regulating the MF cytoskeleton assembly. Finally, we developed a hypothesis concerning the regulation of the microfilament skeleton as a fundamental response to water loss in thalli of <em>N. yezoensis</em>. Our findings will enhance our understanding the adaption mechanisms of <em>N. yezoensis</em> to water stress and broaden our knowledge regarding the response of MF cytoskeleton to water stress. Furthermore, this research will provide valuable insights into the species distribution of intertidal zones.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100762"},"PeriodicalIF":6.8,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143387617","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Maximizing nitrogen stress tolerance through high-throughput phenotyping in rice
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-02-05 DOI: 10.1016/j.stress.2025.100764
Nguyen Trung Duc , Amooru Harika , Dhandapani Raju , Sudhir Kumar , Renu Pandey , Ranjith Kumar Ellur , Gopala Krishnan S , Elangovan Allimuthu , Biswabiplab Singh , Ayyagari Ramlal , Ambika Rajendran , Ranjeet Ranjan Kumar , Madan Pal Singh , Rabi Narayan Sahoo , Viswanathan Chinnusamy
Nitrogen (N) is a significant nutrient element limiting rice yield and quality, a major staple crop consumed worldwide. N deficiency negatively affects the growth and development of rice by impacting vital physiological processes. Plants have developed multiple resilience strategies, including enhanced nitrogen use efficiency (NUE) to cope with N-deprived situations. NUE in rice is less than 40 %, and increased N application leads to high production costs and ecosystem damage. Improving NUE has been one of the major challenges of agriculture research in the recent past. NUE is an obfuscated trait governed by diverse physiological traits and controlled by complex genetic mechanisms. In recent years, a combination of multi-omics techniques (phenomics and genomics) has enhanced the N resilience maximization efforts of the agricultural research community. Phenomics technology has displayed the ability to perform systematic, organism-wide phenotyping of N stress response in diverse crops over the entire life cycle using non-invasive sensors on high throughput platforms (HTPs) in a more precise manner. These HTPs augment precision phenotyping (at the spatiotemporal scale) of component traits of NUE, which are difficult to phenotype mainly due to its dynamic interactive nature with the environment. Phenomics has drastically reduced the phenotype-genotype gap by optimally utilising other omics data for breeding climate smart cultivars with enhanced N stress tolerance. This review focuses on the recent advances in HTP-based phenotyping of NUE-related traits to identify novel QTLs/genes/signaling pathways associated with improved NUE both in controlled environments and field conditions.
{"title":"Maximizing nitrogen stress tolerance through high-throughput phenotyping in rice","authors":"Nguyen Trung Duc ,&nbsp;Amooru Harika ,&nbsp;Dhandapani Raju ,&nbsp;Sudhir Kumar ,&nbsp;Renu Pandey ,&nbsp;Ranjith Kumar Ellur ,&nbsp;Gopala Krishnan S ,&nbsp;Elangovan Allimuthu ,&nbsp;Biswabiplab Singh ,&nbsp;Ayyagari Ramlal ,&nbsp;Ambika Rajendran ,&nbsp;Ranjeet Ranjan Kumar ,&nbsp;Madan Pal Singh ,&nbsp;Rabi Narayan Sahoo ,&nbsp;Viswanathan Chinnusamy","doi":"10.1016/j.stress.2025.100764","DOIUrl":"10.1016/j.stress.2025.100764","url":null,"abstract":"<div><div>Nitrogen (N) is a significant nutrient element limiting rice yield and quality, a major staple crop consumed worldwide. N deficiency negatively affects the growth and development of rice by impacting vital physiological processes. Plants have developed multiple resilience strategies, including enhanced nitrogen use efficiency (NUE) to cope with N-deprived situations. NUE in rice is less than 40 %, and increased N application leads to high production costs and ecosystem damage. Improving NUE has been one of the major challenges of agriculture research in the recent past. NUE is an obfuscated trait governed by diverse physiological traits and controlled by complex genetic mechanisms. In recent years, a combination of multi-omics techniques (phenomics and genomics) has enhanced the N resilience maximization efforts of the agricultural research community. Phenomics technology has displayed the ability to perform systematic, organism-wide phenotyping of N stress response in diverse crops over the entire life cycle using non-invasive sensors on high throughput platforms (HTPs) in a more precise manner. These HTPs augment precision phenotyping (at the spatiotemporal scale) of component traits of NUE, which are difficult to phenotype mainly due to its dynamic interactive nature with the environment. Phenomics has drastically reduced the phenotype-genotype gap by optimally utilising other omics data for breeding climate smart cultivars with enhanced N stress tolerance. This review focuses on the recent advances in HTP-based phenotyping of NUE-related traits to identify novel QTLs/genes/signaling pathways associated with improved NUE both in controlled environments and field conditions.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100764"},"PeriodicalIF":6.8,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143419836","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Genome-wide association analysis for pollen viability under heat stress in peanut
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-02-03 DOI: 10.1016/j.stress.2025.100760
Hrishikesh P. Ingole , Gautam Saripalli , Zachary T. Jones , Manikannan Parthiban , Johnson Toyinbo , Sruthi Narayanan , Reyazul Rouf Mir , Sachin Rustgi
Peanut is one of the most important crops, providing nutrition and food security to millions worldwide. Pollen viability (PV) is a major determinant of yield in crops and is adversely impacted by heat stress. This study aimed to identify molecular markers associated with sustained PV under heat stress. We evaluated 72 genetically non-redundant genotypes from the U.S. peanut mini-core collection for PV under heat stress and compared them to the PV of "Georgia Green," a runner-type peanut variety used as a control. Seventy-two genotypes were grown under optimal conditions (28/22 °C day/night temperatures with a 16 h photoperiod). Once the plants reached the five-leaf stage, heat stress was applied for two weeks by raising the daytime temperature to 38 °C and the nighttime temperature to 28 °C. Un-opened flowers were collected and assayed for PV through in vitro pollen germination. PI 200441 from Japan exhibited the highest PV, while PI 504614 from Colombia showed the lowest. A genome-wide association study for PPV (percent pollen viability) under heat stress identified a marker on chromosome 20. Haplotype analysis revealed a 6 kb region, designated qPPVA20, containing three candidate genes, two of which (ribosomal protein and copper-transporting ATPase) showed high expression in reproductive organs. The co-localization of qPPVA20 with a previously reported QTL hotspot for heat stress-related traits makes these genes important targets for future validation. Markers associated with seed lipid compositional traits, such as behenate, arachidate, oleate, and eicosenoate content under optimal growth conditions, were also identified, with plans to investigate the impact of heat stress on these QTLs in a future study.
{"title":"Genome-wide association analysis for pollen viability under heat stress in peanut","authors":"Hrishikesh P. Ingole ,&nbsp;Gautam Saripalli ,&nbsp;Zachary T. Jones ,&nbsp;Manikannan Parthiban ,&nbsp;Johnson Toyinbo ,&nbsp;Sruthi Narayanan ,&nbsp;Reyazul Rouf Mir ,&nbsp;Sachin Rustgi","doi":"10.1016/j.stress.2025.100760","DOIUrl":"10.1016/j.stress.2025.100760","url":null,"abstract":"<div><div>Peanut is one of the most important crops, providing nutrition and food security to millions worldwide. Pollen viability (PV) is a major determinant of yield in crops and is adversely impacted by heat stress. This study aimed to identify molecular markers associated with sustained PV under heat stress. We evaluated 72 genetically non-redundant genotypes from the U.S. peanut mini-core collection for PV under heat stress and compared them to the PV of \"Georgia Green,\" a runner-type peanut variety used as a control. Seventy-two genotypes were grown under optimal conditions (28/22 °C day/night temperatures with a 16 h photoperiod). Once the plants reached the five-leaf stage, heat stress was applied for two weeks by raising the daytime temperature to 38 °C and the nighttime temperature to 28 °C. Un-opened flowers were collected and assayed for PV through <em>in vitro</em> pollen germination. PI 200441 from Japan exhibited the highest PV, while PI 504614 from Colombia showed the lowest. A genome-wide association study for PPV (percent pollen viability) under heat stress identified a marker on chromosome 20. Haplotype analysis revealed a 6 kb region, designated <em>qPPVA20</em>, containing three candidate genes, two of which (ribosomal protein and copper-transporting ATPase) showed high expression in reproductive organs. The co-localization of <em>qPPVA20</em> with a previously reported QTL hotspot for heat stress-related traits makes these genes important targets for future validation. Markers associated with seed lipid compositional traits, such as behenate, arachidate, oleate, and eicosenoate content under optimal growth conditions, were also identified, with plans to investigate the impact of heat stress on these QTLs in a future study.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100760"},"PeriodicalIF":6.8,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143419835","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Molecular insights into the functional role of PbNRT2.4 in potassium homeostasis and nutrient transport in Pyrus ussuriensis
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-01-30 DOI: 10.1016/j.stress.2025.100752
Han Yang , Hao Xu , Yujie Shi , Liyan Chen , Lijuan Zhang , Liping Kan , Yumeng Jin , Xinlan Mei , Yangchun Xu , Nazir Ahmed , Caixia Dong
Potassium (K), often referred to as the ‘quality element’, is essential for nutrient absorption in fruit trees, with the efficiency of the rootstock's nutrient utilization being a critical factor in the plant's overall nutrient status. Pyrus ussuriensis, identified as a variety with high potassium efficiency, demonstrates superior tolerance to potassium-deficient conditions and a significant affinity for potassium, compared to Pyrus betulifolia, attributed to its proficient capacity for potassium ion redistribution. This study delves into the molecular mechanisms underlying this high potassium efficiency, focusing on PbNRT2.4 gene, a pivotal regulatory factor in the absorption and translocation of potassium. Predominantly expressed in the roots, PbNRT2.4, is finely regulated by potassium concentrations, as well as exogenous sugar levels. Under K+ limitation, sucrose and sorbitol application significantly upregulates PbNRT2.4 expression in P. ussuriensis, thereby enhancing K+ absorption. In yeast systems, PbNRT2.4 facilitates K+ uptake, and its overexpression in hairy root systems, particularly in P. ussuriensis, leads to a marked increase in K+ influx in the root and xylem. Overexpression of this gene in pear callus tissues similarly increased intracellular K+ levels under K-deficient conditions. Interactions among PbNRT2.4, PbHAK11, and PbSDH1 proteins, elucidated using yeast two-hybrid, BiFC, and Co-IP assays, are crucial for modulating carbon and nitrogen metabolic processes, thereby harmonizing K+ absorption and transport. These findings provide a detailed understanding of potassium homeostasis at a molecular level.
{"title":"Molecular insights into the functional role of PbNRT2.4 in potassium homeostasis and nutrient transport in Pyrus ussuriensis","authors":"Han Yang ,&nbsp;Hao Xu ,&nbsp;Yujie Shi ,&nbsp;Liyan Chen ,&nbsp;Lijuan Zhang ,&nbsp;Liping Kan ,&nbsp;Yumeng Jin ,&nbsp;Xinlan Mei ,&nbsp;Yangchun Xu ,&nbsp;Nazir Ahmed ,&nbsp;Caixia Dong","doi":"10.1016/j.stress.2025.100752","DOIUrl":"10.1016/j.stress.2025.100752","url":null,"abstract":"<div><div>Potassium (K), often referred to as the ‘quality element’, is essential for nutrient absorption in fruit trees, with the efficiency of the rootstock's nutrient utilization being a critical factor in the plant's overall nutrient status. <em>Pyrus ussuriensis</em>, identified as a variety with high potassium efficiency, demonstrates superior tolerance to potassium-deficient conditions and a significant affinity for potassium, compared to <em>Pyrus betulifolia</em>, attributed to its proficient capacity for potassium ion redistribution. This study delves into the molecular mechanisms underlying this high potassium efficiency, focusing on <em>PbNRT2.4</em> gene, a pivotal regulatory factor in the absorption and translocation of potassium. Predominantly expressed in the roots, <em>PbNRT2.4</em>, is finely regulated by potassium concentrations, as well as exogenous sugar levels. Under <em>K</em><sup>+</sup> limitation, sucrose and sorbitol application significantly upregulates <em>PbNRT2.4</em> expression in <em>P. ussuriensis</em>, thereby enhancing <em>K</em><sup>+</sup> absorption. In yeast systems, <em>PbNRT2.4</em> facilitates <em>K</em><sup>+</sup> uptake, and its overexpression in hairy root systems, particularly in <em>P. ussuriensis</em>, leads to a marked increase in <em>K</em><sup>+</sup> influx in the root and xylem. Overexpression of this gene in pear callus tissues similarly increased intracellular <em>K</em><sup>+</sup> levels under K-deficient conditions. Interactions among <em>PbNRT2.4, PbHAK11</em>, and <em>PbSDH1</em> proteins, elucidated using yeast two-hybrid, BiFC, and Co-IP assays, are crucial for modulating carbon and nitrogen metabolic processes, thereby harmonizing <em>K</em><sup>+</sup> absorption and transport. These findings provide a detailed understanding of potassium homeostasis at a molecular level.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100752"},"PeriodicalIF":6.8,"publicationDate":"2025-01-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143098872","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Deciphering the role of epigenetics in plant pathogen resistance: Strategies for sustainable sugarcane management
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-01-27 DOI: 10.1016/j.stress.2025.100754
Faisal Mehdi , Yuanli Wu , Shuzhen Zhang , Yimei Gan , Zhengying Cao , Shuting Jiang , Limei Zan , Benpeng Yang
Sugarcane, an important cash crop, is facing increasing threats to its sustainability from various biological stressors. Despite its economic importance, the complex molecular mechanisms involved in sugarcane's defense against pathogens especially the role of epigenetic regulators are not well understood. This review explores how epigenetic regulators contribute to sugarcane's defense mechanisms. It examines the functions of pathogenesis-related (PR) proteins and their interactions with epigenetic modifications. Under normal conditions, plants adjust their gene expression in response to pathogenic threats. Specific transcription factors are activated by external stimuli, which then enhance the expression of defense-related genes. Epigenetic mechanisms, such as histone modifications and DNA methylation, regulate these gene expressions related to biotic stress responses. Additionally, chromatin remodelers and non-coding RNAs work together to boost plant defenses, improving resistance and productivity in various environmental conditions. Importantly, these epigenetic processes create a form of environmental memory and priming, enabling plants to adapt to new challenges based on past experiences. This review offers a comprehensive overview of current knowledge regarding the epigenetic mechanisms that support sugarcane's defense against pathogens. It provides detailed insights into the complex interactions between plants and fungi and discusses innovative crop improvement strategies aimed at improving disease resistance and overall crop resilience. By clarifying these molecular pathways, the review lays a foundation for future research that seeks to strengthen sugarcane against biotic stressors and ensure the sustainability of sugar and bioenergy production.
{"title":"Deciphering the role of epigenetics in plant pathogen resistance: Strategies for sustainable sugarcane management","authors":"Faisal Mehdi ,&nbsp;Yuanli Wu ,&nbsp;Shuzhen Zhang ,&nbsp;Yimei Gan ,&nbsp;Zhengying Cao ,&nbsp;Shuting Jiang ,&nbsp;Limei Zan ,&nbsp;Benpeng Yang","doi":"10.1016/j.stress.2025.100754","DOIUrl":"10.1016/j.stress.2025.100754","url":null,"abstract":"<div><div>Sugarcane, an important cash crop, is facing increasing threats to its sustainability from various biological stressors. Despite its economic importance, the complex molecular mechanisms involved in sugarcane's defense against pathogens especially the role of epigenetic regulators are not well understood. This review explores how epigenetic regulators contribute to sugarcane's defense mechanisms. It examines the functions of pathogenesis-related (PR) proteins and their interactions with epigenetic modifications. Under normal conditions, plants adjust their gene expression in response to pathogenic threats. Specific transcription factors are activated by external stimuli, which then enhance the expression of defense-related genes. Epigenetic mechanisms, such as histone modifications and DNA methylation, regulate these gene expressions related to biotic stress responses. Additionally, chromatin remodelers and non-coding RNAs work together to boost plant defenses, improving resistance and productivity in various environmental conditions. Importantly, these epigenetic processes create a form of environmental memory and priming, enabling plants to adapt to new challenges based on past experiences. This review offers a comprehensive overview of current knowledge regarding the epigenetic mechanisms that support sugarcane's defense against pathogens. It provides detailed insights into the complex interactions between plants and fungi and discusses innovative crop improvement strategies aimed at improving disease resistance and overall crop resilience. By clarifying these molecular pathways, the review lays a foundation for future research that seeks to strengthen sugarcane against biotic stressors and ensure the sustainability of sugar and bioenergy production.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100754"},"PeriodicalIF":6.8,"publicationDate":"2025-01-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143330785","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Plant growth-promoting endophytic consortium improved artemisinin biosynthesis via modulating antioxidants, gene expression, and transcriptional profile in Artemisia annua (L.) under stressed environments
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-01-26 DOI: 10.1016/j.stress.2025.100757
Arpita Tripathi , Praveen Pandey , Shakti Nath Tripathi , Alok Kalra
Artemisia annua L., an important medicinal plant in traditional Chinese medicine, produces an array of secondary metabolites, most notably artemisinin, a potent anti-malarial phytomolecule. However, its low concentration restricts its supply, necessitating a sustainable approach for increasing in planta artemisinin biosynthesis. The biosynthesis of secondary metabolites in plants relies on a multi-step cellular cascade known to be triggered by linked endophytes. Since no single endophyte can up-regulate every step in the biosynthesis process, we tried a consortium of four endophytes: ART1 (Bacillus subtilis), ART2 (Bacillus licheniformis), ART7 (Burkholderia sp.) and ART9 (Acinetobacter pittii) regulating key artemisinin biosynthesis pathway genes and transcriptional factors (TFs) for attaining maximum artemisinin yield. Intriguingly, all the endophytes inoculated plants showed enhanced growth, greater adaptability, and ability to mitigate environmental stresses, which might be attributed to the improved accumulation of chlorophyll, carotenoid, protein, catalase (CAT), superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR) while reduction in proline and 1-Aminocyclopropane-1-carboxylic acid (ACC) level. Moreover, consortia and ART7 enhanced remarkable biomass in all four environments viz., normal (41.78 %, 29.05 %), drought (62.91 %, 29.37 %), salinity (35.15 %, 23.71 %), and waterlogging (48.37 %, 39.52 %); as well as artemisinin content in normal (51.61 %, 41.16 %), drought (32.87 %, 28.76 %), salinity (25.64 %, 19.23 %), and waterlogging (31.57 %, 28.07 %) compared to control. This stimulation of artemisinin by consortia and ART7 emerged from the up-regulation of major structural genes like CYP7AV1, DXS1, HMGR, DXR1, FPS, ADS, ADH2, SQC, ALDH, HMGS, ADH1, and ISPH while down-regulation of SQS, that enabled the metabolic flux flowed toward artemisinin biosynthesis and were able to disrupt the restricted enzymatic stages in the artemisinin biosynthesis pathway; besides, TFs such as bZIP, AP2, C3H, ARF, E2F, MYB, WRKY, MYC, and ERF modulate gene expression, and these proved as possible candidates for studying adaptation to multiple stress and their mechanisms. In summary, our study reflects the potential of the endophytic consortium for strengthening one endophyte's functional vulnerability with another to gain maximum artemisinin yield and plant tolerance against various stresses via regulating essential metabolic pathway genes.
{"title":"Plant growth-promoting endophytic consortium improved artemisinin biosynthesis via modulating antioxidants, gene expression, and transcriptional profile in Artemisia annua (L.) under stressed environments","authors":"Arpita Tripathi ,&nbsp;Praveen Pandey ,&nbsp;Shakti Nath Tripathi ,&nbsp;Alok Kalra","doi":"10.1016/j.stress.2025.100757","DOIUrl":"10.1016/j.stress.2025.100757","url":null,"abstract":"<div><div><em>Artemisia annua</em> L., an important medicinal plant in traditional Chinese medicine, produces an array of secondary metabolites, most notably artemisinin, a potent anti-malarial phytomolecule. However, its low concentration restricts its supply, necessitating a sustainable approach for increasing <em>in planta</em> artemisinin biosynthesis. The biosynthesis of secondary metabolites in plants relies on a multi-step cellular cascade known to be triggered by linked endophytes. Since no single endophyte can up-regulate every step in the biosynthesis process, we tried a consortium of four endophytes: ART1 (<em>Bacillus subtilis</em>), ART2 (<em>Bacillus licheniformis</em>), ART7 (<em>Burkholderia</em> sp.) and ART9 (<em>Acinetobacter pittii</em>) regulating key artemisinin biosynthesis pathway genes and transcriptional factors (TFs) for attaining maximum artemisinin yield. Intriguingly, all the endophytes inoculated plants showed enhanced growth, greater adaptability, and ability to mitigate environmental stresses, which might be attributed to the improved accumulation of chlorophyll, carotenoid, protein, catalase (CAT), superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR) while reduction in proline and 1-Aminocyclopropane-1-carboxylic acid (ACC) level. Moreover, consortia and ART7 enhanced remarkable biomass in all four environments viz., normal (41.78 %, 29.05 %), drought (62.91 %, 29.37 %), salinity (35.15 %, 23.71 %), and waterlogging (48.37 %, 39.52 %); as well as artemisinin content in normal (51.61 %, 41.16 %), drought (32.87 %, 28.76 %), salinity (25.64 %, 19.23 %), and waterlogging (31.57 %, 28.07 %) compared to control. This stimulation of artemisinin by consortia and ART7 emerged from the up-regulation of major structural genes like <em>CYP7AV1, DXS1, HMGR, DXR1, FPS, ADS, ADH2, SQC, ALDH, HMGS, ADH1,</em> and <em>ISPH</em> while down-regulation of <em>SQS</em>, that enabled the metabolic flux flowed toward artemisinin biosynthesis and were able to disrupt the restricted enzymatic stages in the artemisinin biosynthesis pathway; besides, TFs such as <em>bZIP, AP2, C3H, ARF, E2F, MYB, WRKY, MYC,</em> and <em>ERF</em> modulate gene expression, and these proved as possible candidates for studying adaptation to multiple stress and their mechanisms. In summary, our study reflects the potential of the endophytic consortium for strengthening one endophyte's functional vulnerability with another to gain maximum artemisinin yield and plant tolerance against various stresses via regulating essential metabolic pathway genes.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100757"},"PeriodicalIF":6.8,"publicationDate":"2025-01-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143098944","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Transcriptome-derived networks reconstruct distinct immune strategies to counteract fungal infection under different iron availability between Arabidopsis and rice
IF 6.8 Q1 PLANT SCIENCES Pub Date : 2025-01-26 DOI: 10.1016/j.stress.2025.100756
Antoni Garcia-Molina , Héctor Martín-Cardoso , María Ribaya , Blanca San Segundo , Sílvia Busoms
Fe, an essential element for plants to sustain central biological functions, recently emerged as a modulator of immunity. However, our understanding of the crosstalk between Fe and defence is limited. Here, we report antagonistic immune phenotypes in Arabidopsis thaliana and Oryza sativa infected by Colletotrichum higginsianum and Magnaporthe oryzae under different Fe nutritional status. Functional and topological analysis of transcriptional networks unveiled differences in complexity and hierarchy for similar biological functions, as well as in Fe usage and distribution, between the two pathosystems, with a focus on the plant side. Mechanistically, our results are consistent with a regulatory role of Fe in the biosynthesis of the defensive metabolites glucosinolates in A. thaliana (joint effect hypothesis), whereas O. sativa uses Fe to trigger oxidative stress at infection sites (metal defence). Nevertheless, common regulatory features might differently coordinate the transcriptome responses of both species. An evolutionary interpretation of divergences in the interplay between Fe and plant immunity is discussed.
{"title":"Transcriptome-derived networks reconstruct distinct immune strategies to counteract fungal infection under different iron availability between Arabidopsis and rice","authors":"Antoni Garcia-Molina ,&nbsp;Héctor Martín-Cardoso ,&nbsp;María Ribaya ,&nbsp;Blanca San Segundo ,&nbsp;Sílvia Busoms","doi":"10.1016/j.stress.2025.100756","DOIUrl":"10.1016/j.stress.2025.100756","url":null,"abstract":"<div><div>Fe, an essential element for plants to sustain central biological functions, recently emerged as a modulator of immunity. However, our understanding of the crosstalk between Fe and defence is limited. Here, we report antagonistic immune phenotypes in <em>Arabidopsis thaliana</em> and <em>Oryza sativa</em> infected by <em>Colletotrichum higginsianum</em> and <em>Magnaporthe oryzae</em> under different Fe nutritional status. Functional and topological analysis of transcriptional networks unveiled differences in complexity and hierarchy for similar biological functions, as well as in Fe usage and distribution, between the two pathosystems, with a focus on the plant side. Mechanistically, our results are consistent with a regulatory role of Fe in the biosynthesis of the defensive metabolites glucosinolates in <em>A. thaliana</em> (joint effect hypothesis), whereas <em>O. sativa</em> uses Fe to trigger oxidative stress at infection sites (metal defence). Nevertheless, common regulatory features might differently coordinate the transcriptome responses of both species. An evolutionary interpretation of divergences in the interplay between Fe and plant immunity is discussed.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"15 ","pages":"Article 100756"},"PeriodicalIF":6.8,"publicationDate":"2025-01-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143098873","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
期刊
Plant Stress
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