Pub Date : 2024-09-02Epub Date: 2024-08-06DOI: 10.1016/j.molp.2024.07.014
Hyung-Taeg Cho, Minsu Lee, Hee-Seung Choi, Kwang-Ho Maeng, Kyeonghoon Lee, Ha-Yeon Lee, Anindya Ganguly, Hoonyoung Park, Chang-Hoi Ho
Combinatorial interactions between different regulators diversify and enrich the chance of transcriptional regulation in eukaryotic cells. However, a dose-dependent functional switch of homologous transcriptional repressors has rarely been reported. Here, we show that SHY2, an auxin/indole-3-acetic acid (Aux/IAA) repressor, exhibits a dose-dependent bimodal role in auxin-sensitive root-hair growth and gene transcription in Arabidopsis, whereas other Aux/IAA homologs consistently repress the auxin responses. The co-repressor (TOPLESS [TPL])-binding affinity of a bimodal Aux/IAA was lower than that of a consistently repressing Aux/IAA. The switch of a single amino acid residue in the TPL-binding motif between the bimodal form and the consistently repressing form switched their TPL-binding affinity and transcriptional and biological roles in auxin responses. Based on these data, we propose a model whereby competition between homologous repressors with different co-repressor-binding affinities could generate a bimodal output at the transcriptional and developmental levels.
{"title":"A dose-dependent bimodal switch by homologous Aux/IAA transcriptional repressors.","authors":"Hyung-Taeg Cho, Minsu Lee, Hee-Seung Choi, Kwang-Ho Maeng, Kyeonghoon Lee, Ha-Yeon Lee, Anindya Ganguly, Hoonyoung Park, Chang-Hoi Ho","doi":"10.1016/j.molp.2024.07.014","DOIUrl":"10.1016/j.molp.2024.07.014","url":null,"abstract":"<p><p>Combinatorial interactions between different regulators diversify and enrich the chance of transcriptional regulation in eukaryotic cells. However, a dose-dependent functional switch of homologous transcriptional repressors has rarely been reported. Here, we show that SHY2, an auxin/indole-3-acetic acid (Aux/IAA) repressor, exhibits a dose-dependent bimodal role in auxin-sensitive root-hair growth and gene transcription in Arabidopsis, whereas other Aux/IAA homologs consistently repress the auxin responses. The co-repressor (TOPLESS [TPL])-binding affinity of a bimodal Aux/IAA was lower than that of a consistently repressing Aux/IAA. The switch of a single amino acid residue in the TPL-binding motif between the bimodal form and the consistently repressing form switched their TPL-binding affinity and transcriptional and biological roles in auxin responses. Based on these data, we propose a model whereby competition between homologous repressors with different co-repressor-binding affinities could generate a bimodal output at the transcriptional and developmental levels.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1407-1422"},"PeriodicalIF":17.1,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141879073","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}
Suppressor of G2 allele of skp1 (SGT1) is a highly conserved eukaryotic protein that plays a vital role in growth, development, and immunity in both animals and plants. Although some SGT1 interactors have been identified, the molecular regulatory network of SGT1 remains unclear. SGT1 serves as a co-chaperone to stabilize protein complexes such as the nucleotide-binding leucine-rich repeat (NLR) class of immune receptors, thereby positively regulating plant immunity. SGT1 has also been found to be associated with the SKP1-Cullin-F-box (SCF) E3 ubiquitin ligase complex. However, whether SGT1 targets immune repressors to coordinate plant immune activation remains elusive. In this study, we constructed a toolbox for TurboID- and split-TurboID-based proximity labeling (PL) assays in Nicotiana benthamiana and used the PL toolbox to explore the SGT1 interactome during pre- and post-immune activation. The comprehensive SGT1 interactome network we identified highlights a dynamic shift from proteins associated with plant development to those linked with plant immune responses. We found that SGT1 interacts with Necrotic Spotted Lesion 1 (NSL1), which negatively regulates salicylic acid-mediated defense by interfering with the nucleocytoplasmic trafficking of non-expressor of pathogenesis-related genes 1 (NPR1) during N NLR-mediated response to tobacco mosaic virus. SGT1 promotes the SCF-dependent degradation of NSL1 to facilitate immune activation, while salicylate-induced protein kinase-mediated phosphorylation of SGT1 further potentiates this process. Besides N NLR, NSL1 also functions in several other NLR-mediated immunity. Collectively, our study unveils the regulatory landscape of SGT1 and reveals a novel SGT1-NSL1 signaling module that orchestrates plant innate immunity.
{"title":"Proxitome profiling reveals a conserved SGT1-NSL1 signaling module that activates NLR-mediated immunity.","authors":"Dingliang Zhang, Xinxin Yang, Zhiyan Wen, Zhen Li, Xinyu Zhang, Chenchen Zhong, Jiajie She, Qianshen Zhang, He Zhang, Wenli Li, Xiaoyun Zhao, Mingliang Xu, Zhen Su, Dawei Li, Savithramma P Dinesh-Kumar, Yongliang Zhang","doi":"10.1016/j.molp.2024.07.010","DOIUrl":"10.1016/j.molp.2024.07.010","url":null,"abstract":"<p><p>Suppressor of G2 allele of skp1 (SGT1) is a highly conserved eukaryotic protein that plays a vital role in growth, development, and immunity in both animals and plants. Although some SGT1 interactors have been identified, the molecular regulatory network of SGT1 remains unclear. SGT1 serves as a co-chaperone to stabilize protein complexes such as the nucleotide-binding leucine-rich repeat (NLR) class of immune receptors, thereby positively regulating plant immunity. SGT1 has also been found to be associated with the SKP1-Cullin-F-box (SCF) E3 ubiquitin ligase complex. However, whether SGT1 targets immune repressors to coordinate plant immune activation remains elusive. In this study, we constructed a toolbox for TurboID- and split-TurboID-based proximity labeling (PL) assays in Nicotiana benthamiana and used the PL toolbox to explore the SGT1 interactome during pre- and post-immune activation. The comprehensive SGT1 interactome network we identified highlights a dynamic shift from proteins associated with plant development to those linked with plant immune responses. We found that SGT1 interacts with Necrotic Spotted Lesion 1 (NSL1), which negatively regulates salicylic acid-mediated defense by interfering with the nucleocytoplasmic trafficking of non-expressor of pathogenesis-related genes 1 (NPR1) during N NLR-mediated response to tobacco mosaic virus. SGT1 promotes the SCF-dependent degradation of NSL1 to facilitate immune activation, while salicylate-induced protein kinase-mediated phosphorylation of SGT1 further potentiates this process. Besides N NLR, NSL1 also functions in several other NLR-mediated immunity. Collectively, our study unveils the regulatory landscape of SGT1 and reveals a novel SGT1-NSL1 signaling module that orchestrates plant innate immunity.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1369-1391"},"PeriodicalIF":17.1,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141766776","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}
Under warm temperatures, plants adjust their morphologies for environmental adaption via precise gene expression regulation. However, the function and regulation of alternative polyadenylation (APA), an important fine-tuning of gene expression, remains unknown in plant thermomorphogenesis. In this study, we found that SUMOylation, a critical post-translational modification, is induced by a long-term treatment at warm temperatures via a SUMO ligase SIZ1 in Arabidopsis. Disruption of SIZ1 altered the global usage of polyadenylation signals and affected the APA dynamic of thermomorphogenesis-related genes. CPSF100, a key subunit of the CPSF complex for polyadenylation regulation, is SUMOylated by SIZ1. Importantly, we demonstrated that SUMOylation is essential for the function of CPSF100 in genome-wide polyadenylation site choice during thermomorphogenesis. Further analyses revealed that the SUMO conjugation on CPSF100 attenuates its interaction with two isoforms of its partner CPSF30, increasing the nuclear accumulation of CPSF100 for polyadenylation regulation. In summary, our study uncovers a regulatory mechanism of APA via SIZ1-mediated SUMOylation in plant thermomorphogenesis.
{"title":"SIZ1-mediated SUMOylation of CPSF100 promotes plant thermomorphogenesis by controlling alternative polyadenylation.","authors":"Zhibo Yu, Jun Wang, Cheng Zhang, Qiuna Zhan, Leqian Shi, Bing Song, Danlu Han, Jieming Jiang, Junwen Huang, Xiaolin Ou, Zhonghui Zhang, Jianbin Lai, Qingshun Quinn Li, Chengwei Yang","doi":"10.1016/j.molp.2024.07.011","DOIUrl":"10.1016/j.molp.2024.07.011","url":null,"abstract":"<p><p>Under warm temperatures, plants adjust their morphologies for environmental adaption via precise gene expression regulation. However, the function and regulation of alternative polyadenylation (APA), an important fine-tuning of gene expression, remains unknown in plant thermomorphogenesis. In this study, we found that SUMOylation, a critical post-translational modification, is induced by a long-term treatment at warm temperatures via a SUMO ligase SIZ1 in Arabidopsis. Disruption of SIZ1 altered the global usage of polyadenylation signals and affected the APA dynamic of thermomorphogenesis-related genes. CPSF100, a key subunit of the CPSF complex for polyadenylation regulation, is SUMOylated by SIZ1. Importantly, we demonstrated that SUMOylation is essential for the function of CPSF100 in genome-wide polyadenylation site choice during thermomorphogenesis. Further analyses revealed that the SUMO conjugation on CPSF100 attenuates its interaction with two isoforms of its partner CPSF30, increasing the nuclear accumulation of CPSF100 for polyadenylation regulation. In summary, our study uncovers a regulatory mechanism of APA via SIZ1-mediated SUMOylation in plant thermomorphogenesis.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1392-1406"},"PeriodicalIF":17.1,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141766778","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}
Pub Date : 2024-08-05Epub Date: 2024-06-19DOI: 10.1016/j.molp.2024.06.008
Ting Wang, Yi Zheng, Chen Xu, Yulin Deng, Xinyi Hao, Zicheng Chu, Ji Tian, Yi Wang, Xinzhong Zhang, Zhenhai Han, Ting Wu
Xenia, the phenomenon in which the pollen genotype directly affects the phenotypic characteristics of maternal tissues (i.e., fruit ripening), has applications in crop production and breeding. However, the underlying molecular mechanism has yet to be elucidated. Here, we investigated whether mobile mRNAs from the pollen affect the ripening and quality-related characteristics of the fruit using cross-pollination between distinct Malus domestica (apple) cultivars. We demonstrated that hundreds of mobile mRNAs originating from the seeds are delivered to the fruit. We found that the movement of one of these mRNAs, ACC oxidase 3 (MdACO3), is coordinated with fruit ripening. Salicylic acid treatment, which can cause plasmodesmal closure, blocks MdACO3 movement, indicating that MdACO3 transcripts may move through the plasmodesmata. To assess the role of mobile MdACO3 transcripts in apple fruit, we created MdACO3-GFP-expressing apple seeds using MdACO3-GFP-overexpressing pollen for pollination and showed that MdACO3 transcripts in the transgenic seeds move to the flesh, where they promote fruit ripening. Furthermore, we demonstrated that MdACO3 can be transported from the seeds to fruit in the fleshy-fruited species tomato and strawberry. These results underscore the potential of mobile mRNAs from seeds to influence fruit characteristics, providing an explanation for the xenia phenomenon. Notably, our findings highlight the feasibility of leveraging diverse pollen genomic resources, without resorting to genome editing, to improve fruit quality.
{"title":"Movement of ACC oxidase 3 mRNA from seeds to flesh promotes fruit ripening in apple.","authors":"Ting Wang, Yi Zheng, Chen Xu, Yulin Deng, Xinyi Hao, Zicheng Chu, Ji Tian, Yi Wang, Xinzhong Zhang, Zhenhai Han, Ting Wu","doi":"10.1016/j.molp.2024.06.008","DOIUrl":"10.1016/j.molp.2024.06.008","url":null,"abstract":"<p><p>Xenia, the phenomenon in which the pollen genotype directly affects the phenotypic characteristics of maternal tissues (i.e., fruit ripening), has applications in crop production and breeding. However, the underlying molecular mechanism has yet to be elucidated. Here, we investigated whether mobile mRNAs from the pollen affect the ripening and quality-related characteristics of the fruit using cross-pollination between distinct Malus domestica (apple) cultivars. We demonstrated that hundreds of mobile mRNAs originating from the seeds are delivered to the fruit. We found that the movement of one of these mRNAs, ACC oxidase 3 (MdACO3), is coordinated with fruit ripening. Salicylic acid treatment, which can cause plasmodesmal closure, blocks MdACO3 movement, indicating that MdACO3 transcripts may move through the plasmodesmata. To assess the role of mobile MdACO3 transcripts in apple fruit, we created MdACO3-GFP-expressing apple seeds using MdACO3-GFP-overexpressing pollen for pollination and showed that MdACO3 transcripts in the transgenic seeds move to the flesh, where they promote fruit ripening. Furthermore, we demonstrated that MdACO3 can be transported from the seeds to fruit in the fleshy-fruited species tomato and strawberry. These results underscore the potential of mobile mRNAs from seeds to influence fruit characteristics, providing an explanation for the xenia phenomenon. Notably, our findings highlight the feasibility of leveraging diverse pollen genomic resources, without resorting to genome editing, to improve fruit quality.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1221-1235"},"PeriodicalIF":17.1,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141432352","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}
Pub Date : 2024-08-05Epub Date: 2024-07-11DOI: 10.1016/j.molp.2024.07.004
Josh Strable, Alejandro Aragón-Raygoza
{"title":"Development and maintenance of the ligular region of maize leaves.","authors":"Josh Strable, Alejandro Aragón-Raygoza","doi":"10.1016/j.molp.2024.07.004","DOIUrl":"10.1016/j.molp.2024.07.004","url":null,"abstract":"","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1175-1177"},"PeriodicalIF":17.1,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141600788","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}
Pub Date : 2024-08-05Epub Date: 2024-06-17DOI: 10.1016/j.molp.2024.06.006
Pedro de Los Reyes, Gloria Serrano-Bueno, Francisco J Romero-Campero, He Gao, Jose M Romero, Federico Valverde
Plants are sessile organisms that have acquired highly plastic developmental strategies to adapt to the environment. Among these processes, the floral transition is essential to ensure reproductive success and is finely regulated by several internal and external genetic networks. The photoperiodic pathway, which controls plant response to day length, is one of the most important pathways controlling flowering. In Arabidopsis photoperiodic flowering, CONSTANS (CO) is the central gene activating the expression of the florigen FLOWERING LOCUS T (FT) in the leaves at the end of a long day. The circadian clock strongly regulates CO expression. However, to date, no evidence has been reported regarding a feedback loop from the photoperiod pathway back to the circadian clock. Using transcriptional networks, we have identified relevant network motifs regulating the interplay between the circadian clock and the photoperiod pathway. Gene expression, chromatin immunoprecipitation experiments, and phenotypic analysis allowed us to elucidate the role of CO over the circadian clock. Plants with altered CO expression showed a different internal clock period, measured by daily leaf rhythmic movements. We showed that CO upregulates the expression of key genes related to the circadian clock, such as CCA1, LHY, PRR5, and GI, at the end of a long day by binding to specific sites on their promoters. Moreover, a high number of PRR5-repressed target genes are upregulated by CO, and this could explain the phase transition promoted by CO. The CO-PRR5 complex interacts with the bZIP transcription factor HY5 and helps to localize the complex in the promoters of clock genes. Taken together, our results indicate that there may be a feedback loop in which CO communicates back to the circadian clock, providing seasonal information to the circadian system.
植物是一种无柄生物,具有高度可塑性的发育策略,以适应环境。在这些过程中,花期转换对确保繁殖成功至关重要,并受到多个内部和外部遗传网络的精细调控。控制植物对昼长反应的光周期途径是控制开花的最重要途径之一。在拟南芥的光周期开花过程中,CONSTANS(CO)是一个核心基因,它能在长日照结束时激活叶片中花粉基因 FLOWERING LOCUS T(FT)的表达。昼夜节律强烈调节 CO 的表达。然而,迄今为止,还没有关于从光周期途径反馈回昼夜节律钟的证据。利用转录网络,我们确定了调控昼夜节律钟与光周期途径之间相互作用的相关网络模式。通过基因表达、染色质免疫沉淀实验和表型分析,我们阐明了 CO 对昼夜节律钟的作用。CO表达改变的植物表现出不同的内部时钟周期,这是由每日叶片节律性运动测量的。我们的研究表明,CO 可以通过与 CCA1、LHY、PRR5 和 GI 等昼夜节律相关的关键基因启动子上的特定位点结合,在漫长的一天结束时激活这些基因。此外,大量受 PRR5 抑制的靶基因被 CO 上调,这也可以解释 CO 促进相位转换的原因。CO-PRR5 复合物与 bZIP 转录因子 HY5 相互作用,有助于将复合物定位在时钟基因的启动子上。我们的研究结果表明,一氧化碳可能与昼夜节律钟之间存在反馈回路,为昼夜节律系统提供季节信息。
{"title":"CONSTANS alters the circadian clock in Arabidopsis thaliana.","authors":"Pedro de Los Reyes, Gloria Serrano-Bueno, Francisco J Romero-Campero, He Gao, Jose M Romero, Federico Valverde","doi":"10.1016/j.molp.2024.06.006","DOIUrl":"10.1016/j.molp.2024.06.006","url":null,"abstract":"<p><p>Plants are sessile organisms that have acquired highly plastic developmental strategies to adapt to the environment. Among these processes, the floral transition is essential to ensure reproductive success and is finely regulated by several internal and external genetic networks. The photoperiodic pathway, which controls plant response to day length, is one of the most important pathways controlling flowering. In Arabidopsis photoperiodic flowering, CONSTANS (CO) is the central gene activating the expression of the florigen FLOWERING LOCUS T (FT) in the leaves at the end of a long day. The circadian clock strongly regulates CO expression. However, to date, no evidence has been reported regarding a feedback loop from the photoperiod pathway back to the circadian clock. Using transcriptional networks, we have identified relevant network motifs regulating the interplay between the circadian clock and the photoperiod pathway. Gene expression, chromatin immunoprecipitation experiments, and phenotypic analysis allowed us to elucidate the role of CO over the circadian clock. Plants with altered CO expression showed a different internal clock period, measured by daily leaf rhythmic movements. We showed that CO upregulates the expression of key genes related to the circadian clock, such as CCA1, LHY, PRR5, and GI, at the end of a long day by binding to specific sites on their promoters. Moreover, a high number of PRR5-repressed target genes are upregulated by CO, and this could explain the phase transition promoted by CO. The CO-PRR5 complex interacts with the bZIP transcription factor HY5 and helps to localize the complex in the promoters of clock genes. Taken together, our results indicate that there may be a feedback loop in which CO communicates back to the circadian clock, providing seasonal information to the circadian system.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":" ","pages":"1204-1220"},"PeriodicalIF":17.1,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141419953","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}