Plants can shape their root microbiome to promote growth and nutrient uptake. PHOSPHATE STARVATION RESPONSE 2 (OsPHR2) is a central regulator of phosphate signaling in rice, but whether OsPHR2 can shape the root microbiome to promote phosphorus uptake is unclear. Here, we investigate the role of OsPHR2 in recruiting microbiota for phosphorus uptake using high-throughput sequencing and metabolite analysis. OsPHR2-overexpressing (OsPHR2 OE) rice showed 69.8% greater shoot P uptake in natural soil compared with sterilized soil under high-phosphorus (HP) conditions, but there was only a 54.8% increase in the wild-type (WT). The abundance of the family Pseudomonadaceae was significantly enriched in OsPHR2 OE roots relative to those of WT rice. Compared with the WT, OsPHR2 OE rice had a relatively higher abundance of succinic acid and methylmalonic acid, which could stimulate the growth of Pseudomonas sp. (P6). After inoculation with P6, phosphorus uptake in WT and OsPHR2 OE rice was higher than that in uninoculated rice under low-phosphorus (LP) conditions. Taken together, our results suggest that OsPHR2 can increase phosphorus use in rice through root exudate-mediated recruitment of Pseudomonas. This finding reveals a cooperative contribution of the OsPHR2-modulated root microbiome, which is important for improving phosphorus use in agriculture.
{"title":"OsPHR2-mediated recruitment of Pseudomonadaceae enhances rice phosphorus uptake.","authors":"Jianping Liu, Weifeng Xu, Qian Zhang, Wencheng Liao, Liang Li, Shu Chen, Jinyong Yang, Zhengrui Wang, Feiyun Xu","doi":"10.1016/j.xplc.2024.100930","DOIUrl":"10.1016/j.xplc.2024.100930","url":null,"abstract":"<p><p>Plants can shape their root microbiome to promote growth and nutrient uptake. PHOSPHATE STARVATION RESPONSE 2 (OsPHR2) is a central regulator of phosphate signaling in rice, but whether OsPHR2 can shape the root microbiome to promote phosphorus uptake is unclear. Here, we investigate the role of OsPHR2 in recruiting microbiota for phosphorus uptake using high-throughput sequencing and metabolite analysis. OsPHR2-overexpressing (OsPHR2 OE) rice showed 69.8% greater shoot P uptake in natural soil compared with sterilized soil under high-phosphorus (HP) conditions, but there was only a 54.8% increase in the wild-type (WT). The abundance of the family Pseudomonadaceae was significantly enriched in OsPHR2 OE roots relative to those of WT rice. Compared with the WT, OsPHR2 OE rice had a relatively higher abundance of succinic acid and methylmalonic acid, which could stimulate the growth of Pseudomonas sp. (P6). After inoculation with P6, phosphorus uptake in WT and OsPHR2 OE rice was higher than that in uninoculated rice under low-phosphorus (LP) conditions. Taken together, our results suggest that OsPHR2 can increase phosphorus use in rice through root exudate-mediated recruitment of Pseudomonas. This finding reveals a cooperative contribution of the OsPHR2-modulated root microbiome, which is important for improving phosphorus use in agriculture.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369732/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140867562","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-12Epub Date: 2024-05-08DOI: 10.1016/j.xplc.2024.100942
Zeng-Yuan Wu, Mark A Chapman, Jie Liu, Richard I Milne, Ying Zhao, Ya-Huang Luo, Guang-Fu Zhu, Marc W Cadotte, Ming-Bao Luan, Peng-Zhen Fan, Alex K Monro, Zhi-Peng Li, Richard T Corlett, De-Zhu Li
Feralization is an important evolutionary process, but the mechanisms behind it remain poorly understood. Here, we use the ancient fiber crop ramie (Boehmeria nivea (L.) Gaudich.) as a model to investigate genomic changes associated with both domestication and feralization. We first produced a chromosome-scale de novo genome assembly of feral ramie and investigated structural variations between feral and domesticated ramie genomes. Next, we gathered 915 accessions from 23 countries, comprising cultivars, major landraces, feral populations, and the wild progenitor. Based on whole-genome resequencing of these accessions, we constructed the most comprehensive ramie genomic variation map to date. Phylogenetic, demographic, and admixture signal detection analyses indicated that feral ramie is of exoferal or exo-endo origin, i.e., descended from hybridization between domesticated ramie and the wild progenitor or ancient landraces. Feral ramie has higher genetic diversity than wild or domesticated ramie, and genomic regions affected by natural selection during feralization differ from those under selection during domestication. Ecological analyses showed that feral and domesticated ramie have similar ecological niches that differ substantially from the niche of the wild progenitor, and three environmental variables are associated with habitat-specific adaptation in feral ramie. These findings advance our understanding of feralization, providing a scientific basis for the excavation of new crop germplasm resources and offering novel insights into the evolution of feralization in nature.
{"title":"Genomic variation, environmental adaptation, and feralization in ramie, an ancient fiber crop.","authors":"Zeng-Yuan Wu, Mark A Chapman, Jie Liu, Richard I Milne, Ying Zhao, Ya-Huang Luo, Guang-Fu Zhu, Marc W Cadotte, Ming-Bao Luan, Peng-Zhen Fan, Alex K Monro, Zhi-Peng Li, Richard T Corlett, De-Zhu Li","doi":"10.1016/j.xplc.2024.100942","DOIUrl":"10.1016/j.xplc.2024.100942","url":null,"abstract":"<p><p>Feralization is an important evolutionary process, but the mechanisms behind it remain poorly understood. Here, we use the ancient fiber crop ramie (Boehmeria nivea (L.) Gaudich.) as a model to investigate genomic changes associated with both domestication and feralization. We first produced a chromosome-scale de novo genome assembly of feral ramie and investigated structural variations between feral and domesticated ramie genomes. Next, we gathered 915 accessions from 23 countries, comprising cultivars, major landraces, feral populations, and the wild progenitor. Based on whole-genome resequencing of these accessions, we constructed the most comprehensive ramie genomic variation map to date. Phylogenetic, demographic, and admixture signal detection analyses indicated that feral ramie is of exoferal or exo-endo origin, i.e., descended from hybridization between domesticated ramie and the wild progenitor or ancient landraces. Feral ramie has higher genetic diversity than wild or domesticated ramie, and genomic regions affected by natural selection during feralization differ from those under selection during domestication. Ecological analyses showed that feral and domesticated ramie have similar ecological niches that differ substantially from the niche of the wild progenitor, and three environmental variables are associated with habitat-specific adaptation in feral ramie. These findings advance our understanding of feralization, providing a scientific basis for the excavation of new crop germplasm resources and offering novel insights into the evolution of feralization in nature.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369781/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140892823","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
In angiosperms, the pollen tube enters the receptive synergid cell, where it ruptures to release its cytoplasm along with two sperm cells. This interaction is complex, and the exact signal transducers that trigger the bursting of pollen tubes are not well understood. In this study, we identify three homologous receptor-like cytoplasmic kinases (RLCKs) expressed in pollen tubes of Arabidopsis, Delayed Burst 1/2/3 (DEB1/2/3), which play a crucial role in this process. These genes produce proteins localized on the plasma membrane, and their knockout causes delayed pollen tube burst and entrance of additional pollen tubes into the embryo sac due to fertilization recovery. We show that DEBs interact with the Ca2+ pump ACA9, influencing the dynamics of cytoplasmic Ca2+ in pollen tubes through phosphorylation. These results highlight the importance of DEBs as key signal transducers and the critical function of the DEB-ACA9 axis in timely pollen tube burst in synergids.
{"title":"Pollen-expressed RLCKs control pollen tube burst.","authors":"Yin-Jiao Xu, Ting Luo, Peng-Min Zhou, Wei-Qi Wang, Wei-Cai Yang, Hong-Ju Li","doi":"10.1016/j.xplc.2024.100934","DOIUrl":"10.1016/j.xplc.2024.100934","url":null,"abstract":"<p><p>In angiosperms, the pollen tube enters the receptive synergid cell, where it ruptures to release its cytoplasm along with two sperm cells. This interaction is complex, and the exact signal transducers that trigger the bursting of pollen tubes are not well understood. In this study, we identify three homologous receptor-like cytoplasmic kinases (RLCKs) expressed in pollen tubes of Arabidopsis, Delayed Burst 1/2/3 (DEB1/2/3), which play a crucial role in this process. These genes produce proteins localized on the plasma membrane, and their knockout causes delayed pollen tube burst and entrance of additional pollen tubes into the embryo sac due to fertilization recovery. We show that DEBs interact with the Ca<sup>2+</sup> pump ACA9, influencing the dynamics of cytoplasmic Ca<sup>2+</sup> in pollen tubes through phosphorylation. These results highlight the importance of DEBs as key signal transducers and the critical function of the DEB-ACA9 axis in timely pollen tube burst in synergids.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369774/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140867212","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-12Epub Date: 2024-05-24DOI: 10.1016/j.xplc.2024.100979
Yuanyuan Cui, Yanning Su, Jianxin Bian, Xue Han, Haosong Guo, Zhiyuan Yang, Yijun Chen, Lihui Li, Tianyu Li, Xing Wang Deng, Xiaoqin Liu
Peanut (Arachis hypogaea L.) is an important leguminous oil and economic crop that produces flowers aboveground and fruits belowground. Subterranean fruit-pod development, which significantly affects peanut production, involves complex molecular mechanisms that likely require the coordinated regulation of multiple genes in different tissues. To investigate the molecular mechanisms that underlie peanut fruit-pod development, we characterized the anatomical features of early fruit-pod development and integrated single-nucleus RNA-sequencing (snRNA-seq) and single-nucleus assay for transposase-accessible chromatin with sequencing (snATAC-seq) data at the single-cell level. We identified distinct cell types, such as meristem, embryo, vascular tissue, cuticular layer, and stele cells within the shell wall. These specific cell types were used to examine potential molecular changes unique to each cell type during pivotal stages of fruit-pod development. snRNA-seq analyses of differentially expressed genes revealed cell-type-specific insights that were not previously obtainable from transcriptome analyses of bulk RNA. For instance, we identified MADS-box genes that contributes to the formation of parenchyma cells and gravity-related genes that are present in the vascular cells, indicating an essential role for the vascular cells in peg gravitropism. Overall, our single-nucleus analysis provides comprehensive and novel information on specific cell types, gene expression, and chromatin accessibility during the early stages of fruit-pod development. This information will enhance our understanding of the mechanisms that underlie fruit-pod development in peanut and contribute to efforts aimed at improving peanut production.
{"title":"Single-nucleus RNA and ATAC sequencing analyses provide molecular insights into early pod development of peanut fruit.","authors":"Yuanyuan Cui, Yanning Su, Jianxin Bian, Xue Han, Haosong Guo, Zhiyuan Yang, Yijun Chen, Lihui Li, Tianyu Li, Xing Wang Deng, Xiaoqin Liu","doi":"10.1016/j.xplc.2024.100979","DOIUrl":"10.1016/j.xplc.2024.100979","url":null,"abstract":"<p><p>Peanut (Arachis hypogaea L.) is an important leguminous oil and economic crop that produces flowers aboveground and fruits belowground. Subterranean fruit-pod development, which significantly affects peanut production, involves complex molecular mechanisms that likely require the coordinated regulation of multiple genes in different tissues. To investigate the molecular mechanisms that underlie peanut fruit-pod development, we characterized the anatomical features of early fruit-pod development and integrated single-nucleus RNA-sequencing (snRNA-seq) and single-nucleus assay for transposase-accessible chromatin with sequencing (snATAC-seq) data at the single-cell level. We identified distinct cell types, such as meristem, embryo, vascular tissue, cuticular layer, and stele cells within the shell wall. These specific cell types were used to examine potential molecular changes unique to each cell type during pivotal stages of fruit-pod development. snRNA-seq analyses of differentially expressed genes revealed cell-type-specific insights that were not previously obtainable from transcriptome analyses of bulk RNA. For instance, we identified MADS-box genes that contributes to the formation of parenchyma cells and gravity-related genes that are present in the vascular cells, indicating an essential role for the vascular cells in peg gravitropism. Overall, our single-nucleus analysis provides comprehensive and novel information on specific cell types, gene expression, and chromatin accessibility during the early stages of fruit-pod development. This information will enhance our understanding of the mechanisms that underlie fruit-pod development in peanut and contribute to efforts aimed at improving peanut production.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369777/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141093329","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-12DOI: 10.1016/j.xplc.2024.101047
Fuqiu Wang, Sijia Liang, Guanying Wang, Tianyu Hu, Chunyang Fu, Qiongqiong Wang, Zhongping Xu, Yibo Fan, Lianlian Che, Ling Min, Bo Li, Lu Long, Wei Gao, Xianlong Zhang, Shuangxia Jin
Calcium-dependent protein kinases (CDPKs) act as key signal transduction enzymes in plants, especially in response to diverse stresses, including herbivory. In this study, a comprehensive analysis of the CDPK gene family in upland cotton revealed that GhCPKs are widely expressed in multiple cotton tissues and respond positively to various biotic and abiotic stresses. We developed a strategy for screening insect-resistance genes from a CRISPR-Cas9 mutant library of GhCPKs. The library was created using 246 single-guide RNAs targeting the GhCPK gene family to generate 518 independent T0 plants. The average target-gene coverage was 86.18%, the genome editing rate was 89.49%, and the editing heritability was 82%. An insect bioassay in the field led to identification of 14 GhCPK mutants that are resistant or susceptible to insects. The mutant that showed the clearest insect resistance, cpk33/74 (in which the homologous genes GhCPK33 and GhCPK74 were knocked out), was selected for further study. Oral secretions from Spodoptera litura induced a rapid influx of Ca2+ in cpk33/74 leaves, resulting in a significant increase in jasmonic acid content. S-adenosylmethionine synthase is an important protein involved in plant stress response, and protein interaction experiments provided evidence for interactions of GhCPK33 and GhCPK74 with GhSAMS1 and GhSAM2. In addition, virus-induced gene silencing of GhSAMS1 and GhSAM2 in cotton impaired defense against S. litura. This study demonstrates an effective strategy for constructing a mutant library of a gene family in a polyploid plant species and offers valuable insights into the role of CDPKs in the interaction between plants and herbivorous insects.
{"title":"CRISPR-Cas9-mediated construction of a cotton CDPK mutant library for identification of insect-resistance genes.","authors":"Fuqiu Wang, Sijia Liang, Guanying Wang, Tianyu Hu, Chunyang Fu, Qiongqiong Wang, Zhongping Xu, Yibo Fan, Lianlian Che, Ling Min, Bo Li, Lu Long, Wei Gao, Xianlong Zhang, Shuangxia Jin","doi":"10.1016/j.xplc.2024.101047","DOIUrl":"10.1016/j.xplc.2024.101047","url":null,"abstract":"<p><p>Calcium-dependent protein kinases (CDPKs) act as key signal transduction enzymes in plants, especially in response to diverse stresses, including herbivory. In this study, a comprehensive analysis of the CDPK gene family in upland cotton revealed that GhCPKs are widely expressed in multiple cotton tissues and respond positively to various biotic and abiotic stresses. We developed a strategy for screening insect-resistance genes from a CRISPR-Cas9 mutant library of GhCPKs. The library was created using 246 single-guide RNAs targeting the GhCPK gene family to generate 518 independent T0 plants. The average target-gene coverage was 86.18%, the genome editing rate was 89.49%, and the editing heritability was 82%. An insect bioassay in the field led to identification of 14 GhCPK mutants that are resistant or susceptible to insects. The mutant that showed the clearest insect resistance, cpk33/74 (in which the homologous genes GhCPK33 and GhCPK74 were knocked out), was selected for further study. Oral secretions from Spodoptera litura induced a rapid influx of Ca<sup>2+</sup> in cpk33/74 leaves, resulting in a significant increase in jasmonic acid content. S-adenosylmethionine synthase is an important protein involved in plant stress response, and protein interaction experiments provided evidence for interactions of GhCPK33 and GhCPK74 with GhSAMS1 and GhSAM2. In addition, virus-induced gene silencing of GhSAMS1 and GhSAM2 in cotton impaired defense against S. litura. This study demonstrates an effective strategy for constructing a mutant library of a gene family in a polyploid plant species and offers valuable insights into the role of CDPKs in the interaction between plants and herbivorous insects.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141977169","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 : 2024-08-12Epub Date: 2024-04-30DOI: 10.1016/j.xplc.2024.100938
Yiwen Cao, Zegang Han, Zhiyuan Zhang, Lu He, Chujun Huang, Jinwen Chen, Fan Dai, Lisha Xuan, Sunyi Yan, Zhanfeng Si, Yan Hu, Tianzhen Zhang
Seeds play a crucial role in plant reproduction, making it essential to identify genes that affect seed development. In this study, we focused on UDP-glucosyltransferase 71C4 (UGT71C4) in cotton, a member of the glycosyltransferase family that shapes seed width and length, thereby influencing seed index and seed cotton yield. Overexpression of UGT71C4 results in seed enlargement owing to its glycosyltransferase activity on flavonoids, which redirects metabolic flux from lignin to flavonoid metabolism. This shift promotes cell proliferation in the ovule via accumulation of flavonoid glycosides, significantly enhancing seed cotton yield and increasing the seed index from 10.66 g to 11.91 g. By contrast, knockout of UGT71C4 leads to smaller seeds through activation of the lignin metabolism pathway and redirection of metabolic flux back to lignin synthesis. This redirection leads to increased ectopic lignin deposition in the ovule, inhibiting ovule growth and development, and alters yield components, increasing the lint percentage from 41.42% to 43.40% and reducing the seed index from 10.66 g to 8.60 g. Our research sheds new light on seed size development and reveals potential pathways for enhancing seed yield.
{"title":"UDP-glucosyltransferase 71C4 controls the flux of phenylpropanoid metabolism to shape cotton seed development.","authors":"Yiwen Cao, Zegang Han, Zhiyuan Zhang, Lu He, Chujun Huang, Jinwen Chen, Fan Dai, Lisha Xuan, Sunyi Yan, Zhanfeng Si, Yan Hu, Tianzhen Zhang","doi":"10.1016/j.xplc.2024.100938","DOIUrl":"10.1016/j.xplc.2024.100938","url":null,"abstract":"<p><p>Seeds play a crucial role in plant reproduction, making it essential to identify genes that affect seed development. In this study, we focused on UDP-glucosyltransferase 71C4 (UGT71C4) in cotton, a member of the glycosyltransferase family that shapes seed width and length, thereby influencing seed index and seed cotton yield. Overexpression of UGT71C4 results in seed enlargement owing to its glycosyltransferase activity on flavonoids, which redirects metabolic flux from lignin to flavonoid metabolism. This shift promotes cell proliferation in the ovule via accumulation of flavonoid glycosides, significantly enhancing seed cotton yield and increasing the seed index from 10.66 g to 11.91 g. By contrast, knockout of UGT71C4 leads to smaller seeds through activation of the lignin metabolism pathway and redirection of metabolic flux back to lignin synthesis. This redirection leads to increased ectopic lignin deposition in the ovule, inhibiting ovule growth and development, and alters yield components, increasing the lint percentage from 41.42% to 43.40% and reducing the seed index from 10.66 g to 8.60 g. Our research sheds new light on seed size development and reveals potential pathways for enhancing seed yield.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369780/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140871127","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-12Epub Date: 2024-05-22DOI: 10.1016/j.xplc.2024.100978
Ershang Han, Zhenxing Geng, Yue Qin, Yuewei Wang, Shisong Ma
Single-cell RNA-sequencing datasets of Arabidopsis roots have been generated, but related comprehensive gene co-expression network analyses are lacking. We conducted a single-cell gene co-expression network analysis with publicly available scRNA-seq datasets of Arabidopsis roots using a SingleCellGGM algorithm. The analysis identified 149 gene co-expression modules, which we considered to be gene expression programs (GEPs). By examining their spatiotemporal expression, we identified GEPs specifically expressed in major root cell types along their developmental trajectories. These GEPs define gene programs regulating root cell development at different stages and are enriched with relevant developmental regulators. As examples, a GEP specific for the quiescent center (QC) contains 20 genes regulating QC and stem cell niche homeostasis, and four GEPs are expressed in sieve elements (SEs) from early to late developmental stages, with the early-stage GEP containing 17 known SE developmental regulators. We also identified GEPs for metabolic pathways with cell-type-specific expression, suggesting the existence of cell-type-specific metabolism in roots. Using the GEPs, we discovered and verified a columella-specific gene, NRL27, as a regulator of the auxin-related root gravitropism response. Our analysis thus systematically reveals GEPs that regulate Arabidopsis root development and metabolism and provides ample resources for root biology studies.
{"title":"Single-cell network analysis reveals gene expression programs for Arabidopsis root development and metabolism.","authors":"Ershang Han, Zhenxing Geng, Yue Qin, Yuewei Wang, Shisong Ma","doi":"10.1016/j.xplc.2024.100978","DOIUrl":"10.1016/j.xplc.2024.100978","url":null,"abstract":"<p><p>Single-cell RNA-sequencing datasets of Arabidopsis roots have been generated, but related comprehensive gene co-expression network analyses are lacking. We conducted a single-cell gene co-expression network analysis with publicly available scRNA-seq datasets of Arabidopsis roots using a SingleCellGGM algorithm. The analysis identified 149 gene co-expression modules, which we considered to be gene expression programs (GEPs). By examining their spatiotemporal expression, we identified GEPs specifically expressed in major root cell types along their developmental trajectories. These GEPs define gene programs regulating root cell development at different stages and are enriched with relevant developmental regulators. As examples, a GEP specific for the quiescent center (QC) contains 20 genes regulating QC and stem cell niche homeostasis, and four GEPs are expressed in sieve elements (SEs) from early to late developmental stages, with the early-stage GEP containing 17 known SE developmental regulators. We also identified GEPs for metabolic pathways with cell-type-specific expression, suggesting the existence of cell-type-specific metabolism in roots. Using the GEPs, we discovered and verified a columella-specific gene, NRL27, as a regulator of the auxin-related root gravitropism response. Our analysis thus systematically reveals GEPs that regulate Arabidopsis root development and metabolism and provides ample resources for root biology studies.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369779/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141088801","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-12Epub Date: 2024-03-16DOI: 10.1016/j.xplc.2024.100882
Xiaotong Liu, Daisuke Igarashi, Rachel A Hillmer, Thomas Stoddard, You Lu, Kenichi Tsuda, Chad L Myers, Fumiaki Katagiri
Rapid plant immune responses in the appropriate cells are needed for effective defense against pathogens. Although transcriptome analysis is often used to describe overall immune responses, collection of transcriptome data with sufficient resolution in both space and time is challenging. We reanalyzed public Arabidopsis time-course transcriptome data obtained after low-dose inoculation with a Pseudomonas syringae strain expressing the effector AvrRpt2, which induces effector-triggered immunity in Arabidopsis. Double-peak time-course patterns are prevalent among thousands of upregulated genes. We implemented a multi-compartment modeling approach to decompose the double-peak pattern into two single-peak patterns for each gene. The decomposed peaks reveal an "echoing" pattern: the peak times of the first and second peaks correlate well across most upregulated genes. We demonstrated that the two peaks likely represent responses of two distinct cell populations that respond either cell autonomously or indirectly to AvrRpt2. Thus, the peak decomposition has extracted spatial information from the time-course data. The echoing pattern also indicates a conserved transcriptome response with different initiation times between the two cell populations despite different elicitor types. A gene set highly overlapping with the conserved gene set is also upregulated with similar kinetics during pattern-triggered immunity. Activation of a WRKY network via different entry-point WRKYs can explain the similar but not identical transcriptome responses elicited by different elicitor types. We discuss potential benefits of the properties of the WRKY activation network as an immune signaling network in light of pressure from rapidly evolving pathogens.
{"title":"Decomposition of dynamic transcriptomic responses during effector-triggered immunity reveals conserved responses in two distinct plant cell populations.","authors":"Xiaotong Liu, Daisuke Igarashi, Rachel A Hillmer, Thomas Stoddard, You Lu, Kenichi Tsuda, Chad L Myers, Fumiaki Katagiri","doi":"10.1016/j.xplc.2024.100882","DOIUrl":"10.1016/j.xplc.2024.100882","url":null,"abstract":"<p><p>Rapid plant immune responses in the appropriate cells are needed for effective defense against pathogens. Although transcriptome analysis is often used to describe overall immune responses, collection of transcriptome data with sufficient resolution in both space and time is challenging. We reanalyzed public Arabidopsis time-course transcriptome data obtained after low-dose inoculation with a Pseudomonas syringae strain expressing the effector AvrRpt2, which induces effector-triggered immunity in Arabidopsis. Double-peak time-course patterns are prevalent among thousands of upregulated genes. We implemented a multi-compartment modeling approach to decompose the double-peak pattern into two single-peak patterns for each gene. The decomposed peaks reveal an \"echoing\" pattern: the peak times of the first and second peaks correlate well across most upregulated genes. We demonstrated that the two peaks likely represent responses of two distinct cell populations that respond either cell autonomously or indirectly to AvrRpt2. Thus, the peak decomposition has extracted spatial information from the time-course data. The echoing pattern also indicates a conserved transcriptome response with different initiation times between the two cell populations despite different elicitor types. A gene set highly overlapping with the conserved gene set is also upregulated with similar kinetics during pattern-triggered immunity. Activation of a WRKY network via different entry-point WRKYs can explain the similar but not identical transcriptome responses elicited by different elicitor types. We discuss potential benefits of the properties of the WRKY activation network as an immune signaling network in light of pressure from rapidly evolving pathogens.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369737/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140133167","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-03DOI: 10.1016/j.xplc.2024.101045
Xiaxia Zhang, Jingxia Wu, Zhaosheng Kong
The legume-rhizobium symbiosis represents the most important system for terrestrial biological nitrogen fixation on land. Efficient nitrogen fixation during this symbiosis depends on successful rhizobial infection and complete endosymbiosis, which are achieved by complex cellular events including cell-wall remodeling, cytoskeletal reorganizations, and extensive membrane expansion and trafficking. In this review, we explore the dynamic remodeling of the plant-specific cell wall-membrane system-cytoskeleton (WMC) continuum during symbiotic nitrogen fixation. We focus on key processes linked to efficient nitrogen fixation, including rhizobial uptake, infection thread formation and elongation, rhizobial droplet release, cytoplasmic bridge formation, and rhizobial endosymbiosis. Additionally, we discuss the advanced techniques for investigating the cellular basis of root-nodule symbiosis and provide insights into the unsolved mysteries of robust symbiotic nitrogen fixation.
{"title":"Cellular basis of legume-rhizobium symbiosis.","authors":"Xiaxia Zhang, Jingxia Wu, Zhaosheng Kong","doi":"10.1016/j.xplc.2024.101045","DOIUrl":"10.1016/j.xplc.2024.101045","url":null,"abstract":"<p><p>The legume-rhizobium symbiosis represents the most important system for terrestrial biological nitrogen fixation on land. Efficient nitrogen fixation during this symbiosis depends on successful rhizobial infection and complete endosymbiosis, which are achieved by complex cellular events including cell-wall remodeling, cytoskeletal reorganizations, and extensive membrane expansion and trafficking. In this review, we explore the dynamic remodeling of the plant-specific cell wall-membrane system-cytoskeleton (WMC) continuum during symbiotic nitrogen fixation. We focus on key processes linked to efficient nitrogen fixation, including rhizobial uptake, infection thread formation and elongation, rhizobial droplet release, cytoplasmic bridge formation, and rhizobial endosymbiosis. Additionally, we discuss the advanced techniques for investigating the cellular basis of root-nodule symbiosis and provide insights into the unsolved mysteries of robust symbiotic nitrogen fixation.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-08-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141890882","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 : 2024-07-31DOI: 10.1016/j.xplc.2024.101043
Li Yang, Bo Wang, Duanmu Zhao, Xuechun Li, Yifei Qin, Ning Ouyang, Zhili Xiao, Zhibing Zhang, Gad Galili, Jiayang Li, Hadas Peled-Zehavi, Jian Wu
N6-methyladenosine (m6A) is a prevalent internal post-transcriptional modification in eukaryotic RNAs executed by m6A-binding proteins known as "readers." Our previous research demonstrated that the Arabidopsis m6A reader ECT2 positively regulates transcript levels of the proteasome regulator PTRE1 and several 20S proteasome subunits, thereby enhancing 26S proteasome activity. However, mechanism underlying the selective recognition of m6A targets by readers, such as ECT2, remains elusive. In this study, we further demonstrate that ECT2 physically interacts with PTRE1 and several 20S proteasome subunits. This interaction, which occurs on the ribosome, involves the N terminus of PTRE1, suggesting that ECT2 might bind to the nascent PTRE1 polypeptide. Deleting ECT2's protein interaction domain impairs its mRNA-binding ability, whereas mutations in the m6A-RNA-binding site do not affect protein-protein interactions. Moreover, introducing a novel protein-binding domain into ECT2 increases transcript levels of proteins interacting with this domain. Our findings indicate that interaction with the PTRE1 protein enhances ECT2's binding to PTRE1 m6A mRNAs during translation, thereby regulating PTRE1 mRNA levels.
{"title":"Selective recognition of PTRE1 transcripts mediated by protein-protein interaction between the m<sup>6</sup>A reader ECT2 and PTRE1.","authors":"Li Yang, Bo Wang, Duanmu Zhao, Xuechun Li, Yifei Qin, Ning Ouyang, Zhili Xiao, Zhibing Zhang, Gad Galili, Jiayang Li, Hadas Peled-Zehavi, Jian Wu","doi":"10.1016/j.xplc.2024.101043","DOIUrl":"10.1016/j.xplc.2024.101043","url":null,"abstract":"<p><p>N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) is a prevalent internal post-transcriptional modification in eukaryotic RNAs executed by m<sup>6</sup>A-binding proteins known as \"readers.\" Our previous research demonstrated that the Arabidopsis m<sup>6</sup>A reader ECT2 positively regulates transcript levels of the proteasome regulator PTRE1 and several 20S proteasome subunits, thereby enhancing 26S proteasome activity. However, mechanism underlying the selective recognition of m<sup>6</sup>A targets by readers, such as ECT2, remains elusive. In this study, we further demonstrate that ECT2 physically interacts with PTRE1 and several 20S proteasome subunits. This interaction, which occurs on the ribosome, involves the N terminus of PTRE1, suggesting that ECT2 might bind to the nascent PTRE1 polypeptide. Deleting ECT2's protein interaction domain impairs its mRNA-binding ability, whereas mutations in the m<sup>6</sup>A-RNA-binding site do not affect protein-protein interactions. Moreover, introducing a novel protein-binding domain into ECT2 increases transcript levels of proteins interacting with this domain. Our findings indicate that interaction with the PTRE1 protein enhances ECT2's binding to PTRE1 m<sup>6</sup>A mRNAs during translation, thereby regulating PTRE1 mRNA levels.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":null,"pages":null},"PeriodicalIF":9.4,"publicationDate":"2024-07-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141876706","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}