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Naturally occurring spinach defensins confer tolerance to citrus greening and potato zebra chip diseases
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-27 DOI: 10.1111/pbi.70013
Carmen S. Padilla, Sonia C. Irigoyen, Manikandan Ramasamy, Mona B. Damaj, Michelle M. Dominguez, Denise Rossi, Renesh H. Bedre, William O. Dawson, Choaa El-Mohtar, Michael S. Irey, Kranthi K. Mandadi
<p>Citrus greening or Huanglongbing (HLB) and potato zebra chip (ZC) are devastating crop diseases worldwide (Mora <i>et al</i>., <span>2021</span>; Stelinski <i>et al</i>., <span>2024</span>). The diseases are associated with two related, fastidious (unculturable), phloem-limited bacteria, ‘<i>Candidatus</i> Liberibacter asiaticus’ (<i>C</i>Las) and ‘<i>Ca</i>. Liberibacter solanacearum’ (<i>C</i>Lso) that occurs in the United States. They are transmitted by the insect vector <i>Diaphorina citri</i> Kuwayama and <i>Bactericera cockerelli</i> (Sulc.), respectively (Mora <i>et al</i>., <span>2021</span>).</p><p>Defensins are short (~40 to 50 amino acids) basic, cysteine-rich peptides integral to the innate immune system in plants, animals, and insects and possess broad-spectrum inhibitory activity against bacterial and fungal pathogens (Cornet <i>et al</i>., <span>1995</span>; Velivelli <i>et al</i>., <span>2018</span>). Here, we evaluated whether overexpressing defensins from spinach in citrus and potato can confer tolerance to ‘<i>Ca</i>. Liberibacter spp.’ diseases.</p><p>First, we characterized defensin-encoding genes from spinach (<i>Spinacia oleracea</i>) (Mirkov and Mandadi, <span>2020</span>; Segura <i>et al</i>., <span>1998</span>). The spinach defensins (<i>So</i>AMPs) are evolutionarily closer to Group II defensins of <i>Arabidopsis</i>, rice and <i>Medicago</i> (Figure S1a). They possess the conserved Gamma-thionin/knottin-fold and multiple cysteine residues in the amino acid sequence (Figure S1b), and three characteristic antiparallel <i>β</i>-sheets and an <i>α</i>-helix, stabilized by disulfide bridges in the predicted ternary structure (Figure S1c) (Cornet <i>et al</i>., <span>1995</span>).</p><p>Next, we evaluated the efficacy of spinach defensins spp. using <i>Rhizobium rhizogenes</i>-mediated hairy root transformation (Irigoyen <i>et al</i>., <span>2020</span>). Transgene expression was driven under the <i>Cauliflower mosaic virus</i> (CaMV) 35S promoter in the ‘<i>Ca</i>. Liberibacter spp.’ infected hairy roots (Figure 1a) (Irigoyen <i>et al</i>., <span>2020</span>). Both <i>So</i>AMP1 and <i>So</i>AMP2 expressing hairy roots showed 71–99% reduction (<i>P</i> ≤ 0.05 or <i>P</i> ≤ 0.01) of ‘<i>Ca</i>. Liberibacter spp.’ compared to negative controls (empty vector) (Figure 1b) (Table S1). Next, stable potato transgenic lines expressing <i>SoA</i>MP1 and <i>So</i>AMP2 were generated using the <i>Agrobacterium tumefaciens</i>-mediated plant transformation. Two independent transgenic lines and non-transformed (NT) plants (negative controls) were challenged with <i>C</i>Lso-carrying potato psyllids in controlled no-choice assays. The non-transformed plants developed characteristic zebra chip-associated shoot chlorosis and yellowing symptoms at 28 days post-infection (Figure 1c). Strikingly, the <i>So</i>AMP-expressing transgenic plants showed attenuated disease symptoms (Figure 1c), reduced <i>C</i>Lso titre (2.1–5.2% for <i>So</i
{"title":"Naturally occurring spinach defensins confer tolerance to citrus greening and potato zebra chip diseases","authors":"Carmen S. Padilla, Sonia C. Irigoyen, Manikandan Ramasamy, Mona B. Damaj, Michelle M. Dominguez, Denise Rossi, Renesh H. Bedre, William O. Dawson, Choaa El-Mohtar, Michael S. Irey, Kranthi K. Mandadi","doi":"10.1111/pbi.70013","DOIUrl":"https://doi.org/10.1111/pbi.70013","url":null,"abstract":"&lt;p&gt;Citrus greening or Huanglongbing (HLB) and potato zebra chip (ZC) are devastating crop diseases worldwide (Mora &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;2021&lt;/span&gt;; Stelinski &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;2024&lt;/span&gt;). The diseases are associated with two related, fastidious (unculturable), phloem-limited bacteria, ‘&lt;i&gt;Candidatus&lt;/i&gt; Liberibacter asiaticus’ (&lt;i&gt;C&lt;/i&gt;Las) and ‘&lt;i&gt;Ca&lt;/i&gt;. Liberibacter solanacearum’ (&lt;i&gt;C&lt;/i&gt;Lso) that occurs in the United States. They are transmitted by the insect vector &lt;i&gt;Diaphorina citri&lt;/i&gt; Kuwayama and &lt;i&gt;Bactericera cockerelli&lt;/i&gt; (Sulc.), respectively (Mora &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;2021&lt;/span&gt;).&lt;/p&gt;\u0000&lt;p&gt;Defensins are short (~40 to 50 amino acids) basic, cysteine-rich peptides integral to the innate immune system in plants, animals, and insects and possess broad-spectrum inhibitory activity against bacterial and fungal pathogens (Cornet &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;1995&lt;/span&gt;; Velivelli &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;2018&lt;/span&gt;). Here, we evaluated whether overexpressing defensins from spinach in citrus and potato can confer tolerance to ‘&lt;i&gt;Ca&lt;/i&gt;. Liberibacter spp.’ diseases.&lt;/p&gt;\u0000&lt;p&gt;First, we characterized defensin-encoding genes from spinach (&lt;i&gt;Spinacia oleracea&lt;/i&gt;) (Mirkov and Mandadi, &lt;span&gt;2020&lt;/span&gt;; Segura &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;1998&lt;/span&gt;). The spinach defensins (&lt;i&gt;So&lt;/i&gt;AMPs) are evolutionarily closer to Group II defensins of &lt;i&gt;Arabidopsis&lt;/i&gt;, rice and &lt;i&gt;Medicago&lt;/i&gt; (Figure S1a). They possess the conserved Gamma-thionin/knottin-fold and multiple cysteine residues in the amino acid sequence (Figure S1b), and three characteristic antiparallel &lt;i&gt;β&lt;/i&gt;-sheets and an &lt;i&gt;α&lt;/i&gt;-helix, stabilized by disulfide bridges in the predicted ternary structure (Figure S1c) (Cornet &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;1995&lt;/span&gt;).&lt;/p&gt;\u0000&lt;p&gt;Next, we evaluated the efficacy of spinach defensins spp. using &lt;i&gt;Rhizobium rhizogenes&lt;/i&gt;-mediated hairy root transformation (Irigoyen &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;2020&lt;/span&gt;). Transgene expression was driven under the &lt;i&gt;Cauliflower mosaic virus&lt;/i&gt; (CaMV) 35S promoter in the ‘&lt;i&gt;Ca&lt;/i&gt;. Liberibacter spp.’ infected hairy roots (Figure 1a) (Irigoyen &lt;i&gt;et al&lt;/i&gt;., &lt;span&gt;2020&lt;/span&gt;). Both &lt;i&gt;So&lt;/i&gt;AMP1 and &lt;i&gt;So&lt;/i&gt;AMP2 expressing hairy roots showed 71–99% reduction (&lt;i&gt;P&lt;/i&gt; ≤ 0.05 or &lt;i&gt;P&lt;/i&gt; ≤ 0.01) of ‘&lt;i&gt;Ca&lt;/i&gt;. Liberibacter spp.’ compared to negative controls (empty vector) (Figure 1b) (Table S1). Next, stable potato transgenic lines expressing &lt;i&gt;SoA&lt;/i&gt;MP1 and &lt;i&gt;So&lt;/i&gt;AMP2 were generated using the &lt;i&gt;Agrobacterium tumefaciens&lt;/i&gt;-mediated plant transformation. Two independent transgenic lines and non-transformed (NT) plants (negative controls) were challenged with &lt;i&gt;C&lt;/i&gt;Lso-carrying potato psyllids in controlled no-choice assays. The non-transformed plants developed characteristic zebra chip-associated shoot chlorosis and yellowing symptoms at 28 days post-infection (Figure 1c). Strikingly, the &lt;i&gt;So&lt;/i&gt;AMP-expressing transgenic plants showed attenuated disease symptoms (Figure 1c), reduced &lt;i&gt;C&lt;/i&gt;Lso titre (2.1–5.2% for &lt;i&gt;So&lt;/i","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"31 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143517828","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Harnessing promoter elements to enhance gene editing in plants: perspectives and advances.
IF 10.1 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-27 DOI: 10.1111/pbi.14533
Nikita Gondalia, Luis Felipe Quiroz, Linyi Lai, Avinash Kumar Singh, Moman Khan, Galina Brychkova, Peter C McKeown, Manash Chatterjee, Charles Spillane

Genome-edited plants, endowed with climate-smart traits, have been promoted as tools for strengthening resilience against climate change. Successful plant gene editing (GE) requires precise regulation of the GE machinery, a process controlled by the promoters, which drives its transcription through interactions with transcription factors (TFs) and RNA polymerase. While constitutive promoters are extensively used in GE constructs, their limitations highlight the need for alternative approaches. This review emphasizes the promise of tissue/organ specific as well as inducible promoters, which enable targeted GE in a spatiotemporal manner with no effects on other tissues. Advances in synthetic biology have paved the way for the creation of synthetic promoters, offering refined control over gene expression and augmenting the potential of plant GE. The integration of these novel promoters with synthetic systems presents significant opportunities for precise and conditional genome editing. Moreover, the advent of bioinformatic tools and artificial intelligence is revolutionizing the characterization of regulatory elements, enhancing our understanding of their roles in plants. Thus, this review provides novel insights into the strategic use of promoters and promoter editing to enhance the precision, efficiency and specificity of plant GE, setting the stage for innovative crop improvement strategies.

{"title":"Harnessing promoter elements to enhance gene editing in plants: perspectives and advances.","authors":"Nikita Gondalia, Luis Felipe Quiroz, Linyi Lai, Avinash Kumar Singh, Moman Khan, Galina Brychkova, Peter C McKeown, Manash Chatterjee, Charles Spillane","doi":"10.1111/pbi.14533","DOIUrl":"https://doi.org/10.1111/pbi.14533","url":null,"abstract":"<p><p>Genome-edited plants, endowed with climate-smart traits, have been promoted as tools for strengthening resilience against climate change. Successful plant gene editing (GE) requires precise regulation of the GE machinery, a process controlled by the promoters, which drives its transcription through interactions with transcription factors (TFs) and RNA polymerase. While constitutive promoters are extensively used in GE constructs, their limitations highlight the need for alternative approaches. This review emphasizes the promise of tissue/organ specific as well as inducible promoters, which enable targeted GE in a spatiotemporal manner with no effects on other tissues. Advances in synthetic biology have paved the way for the creation of synthetic promoters, offering refined control over gene expression and augmenting the potential of plant GE. The integration of these novel promoters with synthetic systems presents significant opportunities for precise and conditional genome editing. Moreover, the advent of bioinformatic tools and artificial intelligence is revolutionizing the characterization of regulatory elements, enhancing our understanding of their roles in plants. Thus, this review provides novel insights into the strategic use of promoters and promoter editing to enhance the precision, efficiency and specificity of plant GE, setting the stage for innovative crop improvement strategies.</p>","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":" ","pages":""},"PeriodicalIF":10.1,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143514043","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Calcium-dependent protein kinase PpCDPK29-mediated Ca2+-ROS signal and PpHSFA2a phosphorylation regulate postharvest chilling tolerance of peach fruit
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-27 DOI: 10.1111/pbi.70024
Liangyi Zhao, Hua Cassan-Wang, Yaqin Zhao, Yinqiu Bao, Yuanyuan Hou, Yu Liu, Zhengguo Wu, Mondher Bouzayen, Yonghua Zheng, Peng Jin
Green and chemical-free hot water (HW) treatment can effectively reduce the chilling injury of peach fruit; however, the mechanism of inducing chilling resistance by heat treatment is still unclear. This study found that HW treatment could activate reactive oxygen species (ROS) signalling, forming ROS-Ca2+ signalling. Furthermore, we identified a peach Ca2+ sensor, calcium-dependent protein kinase 29 (PpCDPK29), as a positive regulator of postharvest chilling resistance. PpCDPK29 interacted with ROS-generating proteins (PpRBOHC/D) and antioxidant enzymes (PpSOD and PpCAT1) to jointly maintain ROS homeostasis. Meanwhile, we found that PpHSFA2a was phosphorylated by PpCDPK29 and transferred to the nucleus, which enhanced the binding ability of PpHSFA2a to the target genes. Here, PpHSFA2a activated the transcription of target genes PpHSP18.5, PpHSP70, PpGSTU7, PpGSTU19, PpGolS1 and PpBAM1, acted as molecular chaperones, improved ROS scavenging and enhanced osmoregulation to alleviate postharvest chilling injury of peach fruit. In summary, HW treatment could alleviate postharvest chilling injury in peach fruit by activating the PpCDPK29-mediated Ca2+-ROS and HSF-HSP signalling pathways, providing a novel signalling network for postharvest quality control of peach fruit.
{"title":"Calcium-dependent protein kinase PpCDPK29-mediated Ca2+-ROS signal and PpHSFA2a phosphorylation regulate postharvest chilling tolerance of peach fruit","authors":"Liangyi Zhao, Hua Cassan-Wang, Yaqin Zhao, Yinqiu Bao, Yuanyuan Hou, Yu Liu, Zhengguo Wu, Mondher Bouzayen, Yonghua Zheng, Peng Jin","doi":"10.1111/pbi.70024","DOIUrl":"https://doi.org/10.1111/pbi.70024","url":null,"abstract":"Green and chemical-free hot water (HW) treatment can effectively reduce the chilling injury of peach fruit; however, the mechanism of inducing chilling resistance by heat treatment is still unclear. This study found that HW treatment could activate reactive oxygen species (ROS) signalling, forming ROS-Ca<sup>2+</sup> signalling. Furthermore, we identified a peach Ca<sup>2+</sup> sensor, calcium-dependent protein kinase 29 (PpCDPK29), as a positive regulator of postharvest chilling resistance. PpCDPK29 interacted with ROS-generating proteins (PpRBOHC/D) and antioxidant enzymes (PpSOD and PpCAT1) to jointly maintain ROS homeostasis. Meanwhile, we found that PpHSFA2a was phosphorylated by PpCDPK29 and transferred to the nucleus, which enhanced the binding ability of PpHSFA2a to the target genes. Here, PpHSFA2a activated the transcription of target genes <i>PpHSP18.5</i>, <i>PpHSP70</i>, <i>PpGSTU7</i>, <i>PpGSTU19</i>, <i>PpGolS1</i> and <i>PpBAM1</i>, acted as molecular chaperones, improved ROS scavenging and enhanced osmoregulation to alleviate postharvest chilling injury of peach fruit. In summary, HW treatment could alleviate postharvest chilling injury in peach fruit by activating the PpCDPK29-mediated Ca<sup>2+</sup>-ROS and HSF-HSP signalling pathways, providing a novel signalling network for postharvest quality control of peach fruit.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"51 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143517825","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
SPDC-HG: An accelerator of genomic hybrid breeding in maize
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-27 DOI: 10.1111/pbi.70011
Zhenliang Zhang, Xin Wang, Yuxiang Zhang, Kai Zhou, Guangning Yu, Wenyan Yang, Furong Li, Xiusheng Guan, Xuecai Zhang, Zefeng Yang, Chenwu Xu, Yang Xu
Integrating multiple modern breeding techniques in maize has always been challenging. This study aimed to address this issue by applying a flexible sparse partial diallel cross design composed of 945 maize hybrids derived from 266 inbred lines across different heterotic groups. The research integrated genome-wide association studies, genomic selection and genomic evaluation of parental inbred lines to accelerate the breeding process for developing single-cross hybrids. Significant associations were identified for 7–25 stable single nucleotide polymorphisms (SNPs) associated with the general combining abilities (GCAs) of nine yield-related traits. Using the maizeGDB and NCBI databases, 264 candidate genes were screened and functionally annotated based on significant SNPs detected by at least three statistical methods. The marker set developed from these GCA SNPs significantly improved the prediction accuracy of hybrids across all traits. The GCA estimates of the inbred lines involved in the top 100 and bottom 100 hybrids consistently ranked at the top and bottom, thereby confirming the accuracy of the predictions. Furthermore, the top 100 crosses selected using BayesB, GBLUP and LASSO showed a 105.4–108.6% increase in average ear weight compared to the bottom 100 crosses in field validation, demonstrating strong selection gains. Notably, amongst the top 100 hybrids, A017/A037 and A037/A169, each containing six superior genotypes were registered as Suyu 161 and Tongyu 1701, respectively, by the National Crop Variety Approval Committee in China. These results highlight the effectiveness of genomic selection and provide valuable insights for advancing genomic hybrid breeding in maize.
{"title":"SPDC-HG: An accelerator of genomic hybrid breeding in maize","authors":"Zhenliang Zhang, Xin Wang, Yuxiang Zhang, Kai Zhou, Guangning Yu, Wenyan Yang, Furong Li, Xiusheng Guan, Xuecai Zhang, Zefeng Yang, Chenwu Xu, Yang Xu","doi":"10.1111/pbi.70011","DOIUrl":"https://doi.org/10.1111/pbi.70011","url":null,"abstract":"Integrating multiple modern breeding techniques in maize has always been challenging. This study aimed to address this issue by applying a flexible sparse partial diallel cross design composed of 945 maize hybrids derived from 266 inbred lines across different heterotic groups. The research integrated genome-wide association studies, genomic selection and genomic evaluation of parental inbred lines to accelerate the breeding process for developing single-cross hybrids. Significant associations were identified for 7–25 stable single nucleotide polymorphisms (SNPs) associated with the general combining abilities (GCAs) of nine yield-related traits. Using the maizeGDB and NCBI databases, 264 candidate genes were screened and functionally annotated based on significant SNPs detected by at least three statistical methods. The marker set developed from these GCA SNPs significantly improved the prediction accuracy of hybrids across all traits. The GCA estimates of the inbred lines involved in the top 100 and bottom 100 hybrids consistently ranked at the top and bottom, thereby confirming the accuracy of the predictions. Furthermore, the top 100 crosses selected using BayesB, GBLUP and LASSO showed a 105.4–108.6% increase in average ear weight compared to the bottom 100 crosses in field validation, demonstrating strong selection gains. Notably, amongst the top 100 hybrids, A017/A037 and A037/A169, each containing six superior genotypes were registered as Suyu 161 and Tongyu 1701, respectively, by the National Crop Variety Approval Committee in China. These results highlight the effectiveness of genomic selection and provide valuable insights for advancing genomic hybrid breeding in maize.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"12 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143517829","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Gibberellin signalling mediates nucleocytoplasmic trafficking of Sucrose Synthase 1 to regulate the drought tolerance in rice.
IF 10.1 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-26 DOI: 10.1111/pbi.70020
Jishuai Huang, Bin Xie, Fengjun Xian, Kejia Liu, Qian Yan, Yurong He, Lin Zhu, Wei Liu, Yue Jiang, Yuting Chen, Leilei Peng, Yuwei Zhou, Jun Hu

The Green Revolution (GR) has substantially improved cereal crop yields and enhanced adaptation to diverse environmental challenges. However, the molecular and cellular mechanisms involving GR-related genes that regulate drought tolerance in plants remain largely unclear. Here, we reveal that the gibberellin (GA) signalling repressor SLENDER RICE 1 (SLR1) negatively regulates the abundance of the dehydration-responsive protein OsBURP3 to enhance drought tolerance in rice. OsBURP3 facilitates the translocation of Sucrose Synthase 1 (OsSUS1), from the cytosol to the nucleus, thereby decreasing the sucrose content. Mutation of OsBURP3 reduces the nucleus accumulation of OsSUS1 to enhance drought tolerance. SLR1 also competitively associates with OsBURP3 in the nucleus to release OsSUS1 back into the cytosol, resulting in elevated sucrose content. Cytological evidences confirm that sucrose contributes to the fine-tuning of the stomata aperture in rice leaves. Collectively, these findings provide a comprehensive framework for understanding the role of GA in regulating drought tolerance by mediating sucrose metabolism in crops.

{"title":"Gibberellin signalling mediates nucleocytoplasmic trafficking of Sucrose Synthase 1 to regulate the drought tolerance in rice.","authors":"Jishuai Huang, Bin Xie, Fengjun Xian, Kejia Liu, Qian Yan, Yurong He, Lin Zhu, Wei Liu, Yue Jiang, Yuting Chen, Leilei Peng, Yuwei Zhou, Jun Hu","doi":"10.1111/pbi.70020","DOIUrl":"https://doi.org/10.1111/pbi.70020","url":null,"abstract":"<p><p>The Green Revolution (GR) has substantially improved cereal crop yields and enhanced adaptation to diverse environmental challenges. However, the molecular and cellular mechanisms involving GR-related genes that regulate drought tolerance in plants remain largely unclear. Here, we reveal that the gibberellin (GA) signalling repressor SLENDER RICE 1 (SLR1) negatively regulates the abundance of the dehydration-responsive protein OsBURP3 to enhance drought tolerance in rice. OsBURP3 facilitates the translocation of Sucrose Synthase 1 (OsSUS1), from the cytosol to the nucleus, thereby decreasing the sucrose content. Mutation of OsBURP3 reduces the nucleus accumulation of OsSUS1 to enhance drought tolerance. SLR1 also competitively associates with OsBURP3 in the nucleus to release OsSUS1 back into the cytosol, resulting in elevated sucrose content. Cytological evidences confirm that sucrose contributes to the fine-tuning of the stomata aperture in rice leaves. Collectively, these findings provide a comprehensive framework for understanding the role of GA in regulating drought tolerance by mediating sucrose metabolism in crops.</p>","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":" ","pages":""},"PeriodicalIF":10.1,"publicationDate":"2025-02-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143514042","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Autosuppression of MdNAC18.1 endowed by a 61-bp promoter fragment duplication delays maturity date in apple
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-26 DOI: 10.1111/pbi.14580
Bo Zhang, Xiaofei Wang, Qianyu Yue, Weihan Zhang, Haofeng Liu, Tingting Zhang, Lingling Zhao, Qingmei Guan, Chunxiang You, Jianping An, Yuepeng Han, Liao Liao
Maturity date considerably influences fruit marketing period and commercial value and it is of particular importance in apple due to its association with fruit firmness that determines storage and shelf life, but the underlying mechanism remains unclear. In this study, we report a 61-bp fragment duplication in the MdNAC18.1 promoter that underpins maturity date variation in apple. MdNAC18.1 is the crucial major gene for maturity date and was found to regulate fruit ripening by activating transcription of ethylene biosynthetic genes and ripening-related transcription factors, including the MdNAC18.1 homologue MdNAC72 and the main regulator of JA signalling MdMYC2. Interestingly, MdNAC18.1 was capable of binding to the promoter itself containing an additional NAC recognition site that arose from the 61-bp duplication to repress its own expression, but could not bind to its own promoter without the 61-bp duplication. Thus, the MdNAC18.1 allele with autosuppression function produces a phenotype of delayed maturity date and slower softening of fruit compared to that without autoregulation function. Our results demonstrate an autosuppression module that regulates the overall tempo of fruit ripening through fine-tuning ethylene biosynthesis.
{"title":"Autosuppression of MdNAC18.1 endowed by a 61-bp promoter fragment duplication delays maturity date in apple","authors":"Bo Zhang, Xiaofei Wang, Qianyu Yue, Weihan Zhang, Haofeng Liu, Tingting Zhang, Lingling Zhao, Qingmei Guan, Chunxiang You, Jianping An, Yuepeng Han, Liao Liao","doi":"10.1111/pbi.14580","DOIUrl":"https://doi.org/10.1111/pbi.14580","url":null,"abstract":"Maturity date considerably influences fruit marketing period and commercial value and it is of particular importance in apple due to its association with fruit firmness that determines storage and shelf life, but the underlying mechanism remains unclear. In this study, we report a 61-bp fragment duplication in the <i>MdNAC18.1</i> promoter that underpins maturity date variation in apple. <i>MdNAC18.1</i> is the crucial major gene for maturity date and was found to regulate fruit ripening by activating transcription of ethylene biosynthetic genes and ripening-related transcription factors, including the MdNAC18.1 homologue MdNAC72 and the main regulator of JA signalling MdMYC2. Interestingly, MdNAC18.1 was capable of binding to the promoter itself containing an additional NAC recognition site that arose from the 61-bp duplication to repress its own expression, but could not bind to its own promoter without the 61-bp duplication. Thus, the <i>MdNAC18.1</i> allele with autosuppression function produces a phenotype of delayed maturity date and slower softening of fruit compared to that without autoregulation function. Our results demonstrate an autosuppression module that regulates the overall tempo of fruit ripening through fine-tuning ethylene biosynthesis.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"28 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143495836","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Characterization and functional reconstruction of a highly productive germacrene A synthase from Liriodendron chinense.
IF 10.1 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-26 DOI: 10.1111/pbi.70023
Weijia Cheng, Yao Zhi, Fangfang Chen, Xiaochun Xiao, Hui Lu, Ranjun Li, Hangzhi Zhu, Qiuxia Wang, Xueting Fang, Zhenni Xu, Zixin Deng, Tiangang Liu, Li Lu

Plants produce a large array of natural products which play important roles in flavours, fragrances and medicines. However, some high-value plant intermediate metabolites cannot be directly extracted from plants. The tulip tree (Liriodendron chinense) in the Magnoliaceae family is rich in sesquiterpenes. Upon characterizing the functions of 11 Liriodendron chinense terpene synthases, we discovered that LcTPS3 could produce high yields of (+)-germacrene A, which was shown to be a central scaffold in sesquiterpene biosynthesis. This compound can be completely transformed into β-elemene at high temperature, a broad-spectrum antitumor drug widely used in clinical treatment. By expressing LcTPS3 in a precursor-providing Saccharomyces cerevisiae chassis and with the aid of metabolic engineering, the fermentation yield of (+)-germacrene A has been achieved at 14.71 g/L. Site-directed mutagenesis experiments and molecular dynamics simulations revealed that the A280V suppresses the cyclization of substrate by influencing the conformation of the enzyme-substrate. The Y282L facilitates secondary cyclization to produce α-guaiene by shortening the distance between the catalytic residue Y531 and the substrate. These insights underscore the high plasticity of LcTPS3 and suggest that its targeted engineering could unlock the synthesis of a wider array of valuable sesquiterpenes.

{"title":"Characterization and functional reconstruction of a highly productive germacrene A synthase from Liriodendron chinense.","authors":"Weijia Cheng, Yao Zhi, Fangfang Chen, Xiaochun Xiao, Hui Lu, Ranjun Li, Hangzhi Zhu, Qiuxia Wang, Xueting Fang, Zhenni Xu, Zixin Deng, Tiangang Liu, Li Lu","doi":"10.1111/pbi.70023","DOIUrl":"https://doi.org/10.1111/pbi.70023","url":null,"abstract":"<p><p>Plants produce a large array of natural products which play important roles in flavours, fragrances and medicines. However, some high-value plant intermediate metabolites cannot be directly extracted from plants. The tulip tree (Liriodendron chinense) in the Magnoliaceae family is rich in sesquiterpenes. Upon characterizing the functions of 11 Liriodendron chinense terpene synthases, we discovered that LcTPS3 could produce high yields of (+)-germacrene A, which was shown to be a central scaffold in sesquiterpene biosynthesis. This compound can be completely transformed into β-elemene at high temperature, a broad-spectrum antitumor drug widely used in clinical treatment. By expressing LcTPS3 in a precursor-providing Saccharomyces cerevisiae chassis and with the aid of metabolic engineering, the fermentation yield of (+)-germacrene A has been achieved at 14.71 g/L. Site-directed mutagenesis experiments and molecular dynamics simulations revealed that the A280V suppresses the cyclization of substrate by influencing the conformation of the enzyme-substrate. The Y282L facilitates secondary cyclization to produce α-guaiene by shortening the distance between the catalytic residue Y531 and the substrate. These insights underscore the high plasticity of LcTPS3 and suggest that its targeted engineering could unlock the synthesis of a wider array of valuable sesquiterpenes.</p>","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":" ","pages":""},"PeriodicalIF":10.1,"publicationDate":"2025-02-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143514034","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
PtrVINV2 is dispensable for cellulose synthesis but essential for salt tolerance in Populus trichocarpa Torr. and Gray
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-24 DOI: 10.1111/pbi.70022
Shuang Zhang, Lina Cao, Danyang Chen, Ruhui Chang, Jiayu Cao, Qiaoyi Zhang, Yeling Qin, Guanjun Liu, Zhiru Xu
Invertase (EC.3.2.1.26), a key enzyme in sucrose breakdown, is crucial for cellulose synthesis. However, the function of the vacuolar invertase (VINV) in woody plants remains unclear. In this study, transgenic lines of Populus trichocarpa Torr. and Gray were generated to investigate the role of PtrVINV2 in wood formation and under high salinity stress. Compared to wild-type (WT), VINV activity in the developing xylem of knockout lines was reduced, resulting in a decrease in lignin content and an increase in hemicellulose content, while cellulose content remained unaffected. These changes in structural carbohydrate content were accompanied by reductions in xylem width and fibre cell wall thickness. The overexpression lines of the developing xylem exhibited opposite trends. Transcriptome analyses of developing xylem indicated that the expression level of PtrVINV2 affects the expression of genes involved in hemicellulose and lignin biosynthesis pathways, such as AXS, UAMs, HCT, COMT, CAD and peroxidases, while CesA expression remained unaffected. WGCNA analysis revealed that Potri.001G219100, Potri.009G106600 and Potri.002G081000 serve as ‘hub’ transcription factor genes within the structural/non-structural carbohydrate modules of PtrVINV2 transgenic lines, potentially involved in plant salt tolerance. Additionally, under 200 mmol/L NaCl treatment, the knockout lines exhibited increased salt sensitivity compared to WT. This increased sensitivity was accompanied by elevated activities of SOD, CAT and MDA, as well as higher sucrose content and reduced contents of glucose and fructose. The findings indicate that although PtrVINV2 is not essential for cellulose synthesis, it enhances salt tolerance in poplar and presents a promising candidate gene for breeding salt-tolerant poplar.
{"title":"PtrVINV2 is dispensable for cellulose synthesis but essential for salt tolerance in Populus trichocarpa Torr. and Gray","authors":"Shuang Zhang, Lina Cao, Danyang Chen, Ruhui Chang, Jiayu Cao, Qiaoyi Zhang, Yeling Qin, Guanjun Liu, Zhiru Xu","doi":"10.1111/pbi.70022","DOIUrl":"https://doi.org/10.1111/pbi.70022","url":null,"abstract":"Invertase (EC.3.2.1.26), a key enzyme in sucrose breakdown, is crucial for cellulose synthesis. However, the function of the vacuolar invertase (VINV) in woody plants remains unclear. In this study, transgenic lines of <i>Populus trichocarpa</i> Torr. and Gray were generated to investigate the role of <i>PtrVINV2</i> in wood formation and under high salinity stress. Compared to wild-type (WT), VINV activity in the developing xylem of knockout lines was reduced, resulting in a decrease in lignin content and an increase in hemicellulose content, while cellulose content remained unaffected. These changes in structural carbohydrate content were accompanied by reductions in xylem width and fibre cell wall thickness. The overexpression lines of the developing xylem exhibited opposite trends. Transcriptome analyses of developing xylem indicated that the expression level of <i>PtrVINV2</i> affects the expression of genes involved in hemicellulose and lignin biosynthesis pathways, such as <i>AXS</i>, <i>UAMs</i>, <i>HCT</i>, <i>COMT</i>, <i>CAD</i> and <i>peroxidases</i>, while <i>CesA</i> expression remained unaffected. WGCNA analysis revealed that <i>Potri.001G219100</i>, <i>Potri.009G106600</i> and <i>Potri.002G081000</i> serve as ‘hub’ transcription factor genes within the structural/non-structural carbohydrate modules of <i>PtrVINV2</i> transgenic lines, potentially involved in plant salt tolerance. Additionally, under 200 mmol/L NaCl treatment, the knockout lines exhibited increased salt sensitivity compared to WT. This increased sensitivity was accompanied by elevated activities of SOD, CAT and MDA, as well as higher sucrose content and reduced contents of glucose and fructose. The findings indicate that although <i>PtrVINV2</i> is not essential for cellulose synthesis, it enhances salt tolerance in poplar and presents a promising candidate gene for breeding salt-tolerant poplar.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"40 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143477871","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
CmPPR4 gene controls drought resilience in melon ecotypes
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-22 DOI: 10.1111/pbi.70019
Yuelin Xia, Mingze Xu, Qinrong Yang, Yutong Zhang, Qinhui Shen, Haoshun Zhao, Kejia Zhang, Yiqing Meng, Asmat Batool, Yongming Bo, Rongrong Jin, Hong Cao, Zhongyuan Hu, Jinghua Yang, Mingfang Zhang, Xiaolong Lyu
Global climate change has rendered drought stress an increasing threat to sustainable crop production. Melon (Cucumis melo) crop is widely cultivated worldwide, and has been classified into two subspecies C. melo ssp. melo and C. melo ssp. agrestis with greater drought tolerance variation. However, the genetic basis for the difference in drought resilience between two subspecies ecotypes remains unclear. In this study, we constructed an F8 recombinant inbred lines (RILs) population generated by crossing drought-tolerant C. melo ssp. melo with drought-sensitive C. melo ssp. agrestis and identified a CmPPR4 gene that encoded a pentatricopeptide repeat (PPR) protein highly associated with drought tolerance. A single nucleotide polymorphism (SNP) variation in CmPPR4 resulted in a nonsynonymous mutation, leading to reduced drought resilience in C. melo ssp. agrestis. The geographical distribution of CmPPR4 genotypes among 297 melon accessions closely parallels global annual precipitation patterns. Furthermore, the diminished drought tolerant capacity in RNA silencing seedlings and enhanced drought tolerance in overexpression lines further confirmed CmPPR4 as a crucial regulator of drought tolerance in melon. Collectively, our findings provide new insights into the crucial role of CmPPR4 in regulating drought tolerance of melon ecotypes, promoting molecular breeding of water-saving and drought-resilient melon cultivars.
全球气候变化使干旱压力对可持续作物生产的威胁日益严重。甜瓜(Cucumis melo)是世界上广泛种植的作物,被分为两个亚种 C. melo ssp.然而,两个亚种生态型抗旱性差异的遗传基础仍不清楚。在本研究中,我们构建了一个由耐旱甜瓜与对干旱敏感的甜瓜杂交产生的 F8 重组近交系(RILs)群体,并鉴定了一个 CmPPR4 基因,该基因编码一种与耐旱性高度相关的五肽重复(PPR)蛋白。CmPPR4 基因的单核苷酸多态性(SNP)变异导致了非同义突变,从而降低了西甜瓜的抗旱能力。297 个甜瓜品种中 CmPPR4 基因型的地理分布与全球年降水量模式密切相关。此外,RNA 沉默幼苗的抗旱能力减弱,而过表达株系的抗旱能力增强,进一步证实了 CmPPR4 是甜瓜抗旱能力的关键调控因子。总之,我们的研究结果为了解 CmPPR4 在调节甜瓜生态型耐旱性中的关键作用提供了新的视角,促进了节水抗旱甜瓜栽培品种的分子育种。
{"title":"CmPPR4 gene controls drought resilience in melon ecotypes","authors":"Yuelin Xia, Mingze Xu, Qinrong Yang, Yutong Zhang, Qinhui Shen, Haoshun Zhao, Kejia Zhang, Yiqing Meng, Asmat Batool, Yongming Bo, Rongrong Jin, Hong Cao, Zhongyuan Hu, Jinghua Yang, Mingfang Zhang, Xiaolong Lyu","doi":"10.1111/pbi.70019","DOIUrl":"https://doi.org/10.1111/pbi.70019","url":null,"abstract":"Global climate change has rendered drought stress an increasing threat to sustainable crop production. Melon (<i>Cucumis melo</i>) crop is widely cultivated worldwide, and has been classified into two subspecies <i>C. melo</i> ssp. <i>melo</i> and <i>C. melo</i> ssp. <i>agrestis</i> with greater drought tolerance variation. However, the genetic basis for the difference in drought resilience between two subspecies ecotypes remains unclear. In this study, we constructed an F<sub>8</sub> recombinant inbred lines (RILs) population generated by crossing drought-tolerant <i>C. melo</i> ssp. <i>melo</i> with drought-sensitive <i>C. melo</i> ssp. <i>agrestis</i> and identified a <i>CmPPR4</i> gene that encoded a pentatricopeptide repeat (PPR) protein highly associated with drought tolerance. A single nucleotide polymorphism (SNP) variation in <i>CmPPR4</i> resulted in a nonsynonymous mutation, leading to reduced drought resilience in <i>C. melo</i> ssp. <i>agrestis.</i> The geographical distribution of <i>CmPPR4</i> genotypes among 297 melon accessions closely parallels global annual precipitation patterns. Furthermore, the diminished drought tolerant capacity in RNA silencing seedlings and enhanced drought tolerance in overexpression lines further confirmed <i>CmPPR4</i> as a crucial regulator of drought tolerance in melon. Collectively, our findings provide new insights into the crucial role of <i>CmPPR4</i> in regulating drought tolerance of melon ecotypes, promoting molecular breeding of water-saving and drought-resilient melon cultivars.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"23 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143470480","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
A system genetics analysis uncovers the regulatory variants controlling drought response in wheat
IF 13.8 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Pub Date : 2025-02-20 DOI: 10.1111/pbi.14605
Bin Chen, Yuling Liu, Yanyan Yang, Qiannan Wang, Shumin Li, Fangfang Li, Linying Du, Peiyin Zhang, Xuemin Wang, Shuangxing Zhang, Xiaoke Zhang, Zhensheng Kang, Xiaojie Wang, Hude Mao
Plants activate a variable response to drought stress by modulating transcription of key genes. However, our knowledge of genetic variations governing gene expression in response to drought stress remains limited in natural germplasm. Here, we performed a comprehensive analysis of the transcriptional variability of 200 wheat accessions in response to drought stress by using a systems genetics approach integrating pan-transcriptome, co-expression networks, transcriptome-wide association study (TWAS), and expression quantitative trait loci (eQTLs) mapping. We identified 1621 genes and eight co-expression modules significantly correlated with wheat drought tolerance. We also defined 620 664 and 654 798 independent eQTLs associated with the expression of 17 429 and 18 080 eGenes under normal and drought stress conditions. Focusing on dynamic regulatory variants, we further identified 572 eQTL hotspots and constructed transcription factors governed drought-responsive network by the XGBoost model. Subsequently, by combining with genome-wide association study (GWAS), we uncovered a 369-bp insertion variant in the TaKCS3 promoter containing multiple cis-regulatory elements recognized by eQTL hotspot-associated transcription factors that enhance its transcription. Further functional analysis indicated that elevating TaKCS3 expression affects cuticular wax composition to reduce water loss during drought stress, and thereby increase drought tolerance. This study sheds light on the genome-wide genetic variants that influence dynamic transcriptional changes during drought stress and provides a valuable resource for the mining of drought-tolerant genes in the future.
{"title":"A system genetics analysis uncovers the regulatory variants controlling drought response in wheat","authors":"Bin Chen, Yuling Liu, Yanyan Yang, Qiannan Wang, Shumin Li, Fangfang Li, Linying Du, Peiyin Zhang, Xuemin Wang, Shuangxing Zhang, Xiaoke Zhang, Zhensheng Kang, Xiaojie Wang, Hude Mao","doi":"10.1111/pbi.14605","DOIUrl":"https://doi.org/10.1111/pbi.14605","url":null,"abstract":"Plants activate a variable response to drought stress by modulating transcription of key genes. However, our knowledge of genetic variations governing gene expression in response to drought stress remains limited in natural germplasm. Here, we performed a comprehensive analysis of the transcriptional variability of 200 wheat accessions in response to drought stress by using a systems genetics approach integrating pan-transcriptome, co-expression networks, transcriptome-wide association study (TWAS), and expression quantitative trait loci (eQTLs) mapping. We identified 1621 genes and eight co-expression modules significantly correlated with wheat drought tolerance. We also defined 620 664 and 654 798 independent eQTLs associated with the expression of 17 429 and 18 080 eGenes under normal and drought stress conditions. Focusing on dynamic regulatory variants, we further identified 572 eQTL hotspots and constructed transcription factors governed drought-responsive network by the XGBoost model. Subsequently, by combining with genome-wide association study (GWAS), we uncovered a 369-bp insertion variant in the <i>TaKCS3</i> promoter containing multiple <i>cis</i>-regulatory elements recognized by eQTL hotspot-associated transcription factors that enhance its transcription. Further functional analysis indicated that elevating <i>TaKCS3</i> expression affects cuticular wax composition to reduce water loss during drought stress, and thereby increase drought tolerance. This study sheds light on the genome-wide genetic variants that influence dynamic transcriptional changes during drought stress and provides a valuable resource for the mining of drought-tolerant genes in the future.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"2 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2025-02-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143462434","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
期刊
Plant Biotechnology Journal
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