Pub Date : 2025-01-13DOI: 10.1016/j.devcel.2024.12.031
Qianying Guo, Fanqing Xu, Shi Song, Siming Kong, Fan Zhai, Yuwen Xiu, Dandan Liu, Ming Li, Ying Lian, Ling Ding, Qian Liu, Ming Yang, Zhengrong Du, Nan Wang, Chuan Long, Xiaomeng Wang, Yuqian Wang, Zhiqiang Yan, Jie Qiao, Liying Yan, Peng Yuan
Cleavage-stage arrest in human embryos substantially limits the success rate of infertility treatment, with maternal-to-zygotic transition (MZT) abnormalities being a potential contributor. However, the underlying mechanisms and regulators remain unclear. Here, by performing allelic transcriptome analysis on human preimplantation embryos, we accurately quantified MZT progression by allelic ratio and identified a fraction of 8-cell embryos, at the appropriate developmental time point and exhibiting normal morphology, were in transcriptionally arrested status. Furthermore, we identified PAIRED (PRD)-like homeobox transcription factors divergent paired-related homeobox (DPRX) and arginine-fifty homeobox (ARGFX) as factors involved in MZT, whose deficiency severely impairs MZT and lineage specification and leads to aberrant retention of histone acetylation. By reversing the acetylation retention caused by DPRX and ARGFX defects, embryonic arrest can be partially rescued. Our study identifies factors involved in human MZT and elucidates the etiology underlying human cleavage-stage arrest.
{"title":"Allelic transcriptomic profiling identifies the role of PRD-like homeobox genes in human embryonic-cleavage-stage arrest","authors":"Qianying Guo, Fanqing Xu, Shi Song, Siming Kong, Fan Zhai, Yuwen Xiu, Dandan Liu, Ming Li, Ying Lian, Ling Ding, Qian Liu, Ming Yang, Zhengrong Du, Nan Wang, Chuan Long, Xiaomeng Wang, Yuqian Wang, Zhiqiang Yan, Jie Qiao, Liying Yan, Peng Yuan","doi":"10.1016/j.devcel.2024.12.031","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.031","url":null,"abstract":"Cleavage-stage arrest in human embryos substantially limits the success rate of infertility treatment, with maternal-to-zygotic transition (MZT) abnormalities being a potential contributor. However, the underlying mechanisms and regulators remain unclear. Here, by performing allelic transcriptome analysis on human preimplantation embryos, we accurately quantified MZT progression by allelic ratio and identified a fraction of 8-cell embryos, at the appropriate developmental time point and exhibiting normal morphology, were in transcriptionally arrested status. Furthermore, we identified PAIRED (PRD)-like homeobox transcription factors divergent paired-related homeobox (<em>DPRX</em>) and arginine-fifty homeobox (<em>ARGFX</em>) as factors involved in MZT, whose deficiency severely impairs MZT and lineage specification and leads to aberrant retention of histone acetylation. By reversing the acetylation retention caused by <em>DPRX</em> and <em>ARGFX</em> defects, embryonic arrest can be partially rescued. Our study identifies factors involved in human MZT and elucidates the etiology underlying human cleavage-stage arrest.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"21 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142967969","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 : 2025-01-13DOI: 10.1016/j.devcel.2024.12.032
Luciano Martín Di Fino, Muhammad Shahzad Anjam, Maarten Besten, Andriani Mentzelopoulou, Vassilis Papadakis, Nageena Zahid, Luis Alonso Baez, Nicola Trozzi, Mateusz Majda, Xuemin Ma, Thorsten Hamann, Joris Sprakel, Panagiotis N. Moschou, Richard S. Smith, Peter Marhavý
Reactivation of cell division is crucial for the regeneration of damaged tissues, which is a fundamental process across all multicellular organisms. However, the mechanisms underlying the activation of cell division in plants during regeneration remain poorly understood. Here, we show that single-cell endodermal ablation generates a transient change in the local mechanical pressure on neighboring pericycle cells to activate patterned cell division that is crucial for tissue regeneration in Arabidopsis roots. Moreover, we provide strong evidence that this process relies on the phytohormone ethylene. Thus, our results highlight a previously unrecognized role of mechano-chemical control in patterned cell division during regeneration in plants.
{"title":"Cellular damage triggers mechano-chemical control of cell wall dynamics and patterned cell divisions in plant healing","authors":"Luciano Martín Di Fino, Muhammad Shahzad Anjam, Maarten Besten, Andriani Mentzelopoulou, Vassilis Papadakis, Nageena Zahid, Luis Alonso Baez, Nicola Trozzi, Mateusz Majda, Xuemin Ma, Thorsten Hamann, Joris Sprakel, Panagiotis N. Moschou, Richard S. Smith, Peter Marhavý","doi":"10.1016/j.devcel.2024.12.032","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.032","url":null,"abstract":"Reactivation of cell division is crucial for the regeneration of damaged tissues, which is a fundamental process across all multicellular organisms. However, the mechanisms underlying the activation of cell division in plants during regeneration remain poorly understood. Here, we show that single-cell endodermal ablation generates a transient change in the local mechanical pressure on neighboring pericycle cells to activate patterned cell division that is crucial for tissue regeneration in <em>Arabidopsis</em> roots. Moreover, we provide strong evidence that this process relies on the phytohormone ethylene. Thus, our results highlight a previously unrecognized role of mechano-chemical control in patterned cell division during regeneration in plants.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"21 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142967966","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 : 2025-01-13DOI: 10.1016/j.devcel.2024.12.033
Zhihua Song, Qing Yang, Biying Dong, Shengjie Wang, Jingyi Xue, Ni Liu, Xiaomiao Zhou, Na Li, Abhaya M. Dandekar, Lailiang Cheng, Dong Meng, Yujie Fu
Sorbitol, a main photosynthate and transport carbohydrate in all tree fruit species in Rosaceae, acts as a signal controlling resistance against Alternaria (A.) alternata in apple by altering the expression of the MdNLR16 resistance gene via the MdWRKY79 transcription factor. However, it is not known if N6-methyladenosine (m6A) methylation of the mRNAs of these genes participates in the process. Here, we found that decreased sorbitol synthesis in apple leaves leads to a transcriptome-wide reduction in the m6A modification, with fewer transcripts containing two or more methylation sites. We identified two methyltransferases, MdVIR1 and MdVIR2, that respond to sorbitol and A. alternata inoculation and positively control resistance to A. alternata. MdVIR1 and MdVIR2 act on MdWRKY79 and MdNLR16 mRNAs, and the resulting m6A modification stabilizes their mRNAs and improves translation efficiency. These data identify that m6A modification through MdVIR1 and MdVIR2 methyltransferases is essential for sorbitol-controlled resistance to A. alternata.
{"title":"Nanopore RNA direct sequencing identifies that m6A modification is essential for sorbitol-controlled resistance to Alternaria alternata in apple","authors":"Zhihua Song, Qing Yang, Biying Dong, Shengjie Wang, Jingyi Xue, Ni Liu, Xiaomiao Zhou, Na Li, Abhaya M. Dandekar, Lailiang Cheng, Dong Meng, Yujie Fu","doi":"10.1016/j.devcel.2024.12.033","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.033","url":null,"abstract":"Sorbitol, a main photosynthate and transport carbohydrate in all tree fruit species in Rosaceae, acts as a signal controlling resistance against <em>Alternaria (A.) alternata</em> in apple by altering the expression of the <em>MdNLR</em>16 resistance gene via the MdWRKY79 transcription factor. However, it is not known if <em>N</em><sup>6</sup>-methyladenosine (m<sup>6</sup>A) methylation of the mRNAs of these genes participates in the process. Here, we found that decreased sorbitol synthesis in apple leaves leads to a transcriptome-wide reduction in the m<sup>6</sup>A modification, with fewer transcripts containing two or more methylation sites. We identified two methyltransferases, <em>MdVIR1</em> and <em>MdVIR2</em>, that respond to sorbitol and <em>A. alternata</em> inoculation and positively control resistance to <em>A. alternata</em>. MdVIR1 and MdVIR2 act on <em>MdWRKY79</em> and <em>MdNLR16</em> mRNAs, and the resulting m<sup>6</sup>A modification stabilizes their mRNAs and improves translation efficiency. These data identify that m<sup>6</sup>A modification through MdVIR1 and MdVIR2 methyltransferases is essential for sorbitol-controlled resistance to <em>A. alternata</em>.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"47 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142967968","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}
N6-methyladenosine (m6A) RNA modification and its effectors control various plant developmental processes, yet whether and how these effectors are transcriptionally controlled to confer functional specificity so far remain elusive. Herein, we show that a rice C2H2 zinc-finger protein, OsZAF, specifically activates the expression of OsFIP37 encoding a core component of the m6A methyltransferase complex during microsporogenesis in rice anthers. OsFIP37, in turn, facilitates m6A modification and stabilization of an auxin biosynthesis gene OsYUCCA3 to promote auxin biosynthesis in anthers. This elevates auxin levels coinciding with upregulation of an auxin response factor OsARF12 that positively controls OsZAF, thus creating a positive feedback circuit whereby OsFIP37 is continuously activated for local auxin production. Our findings suggest that OsZAF-dependent feedback regulation of m6A modification is integral to local auxin biosynthesis and signaling in anthers, which facilitates the timely generation of auxin maxima required for male meiosis in rice.
{"title":"Feedback regulation of m6A modification creates local auxin maxima essential for rice microsporogenesis","authors":"Peng Cheng, Hu Zhao, Songyao Zhang, Zhanxiang Zong, Chengxiang Li, Luchang Ming, Weibo Xie, Hao Yu","doi":"10.1016/j.devcel.2024.12.034","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.034","url":null,"abstract":"<em>N</em><sup>6</sup>-methyladenosine (m<sup>6</sup>A) RNA modification and its effectors control various plant developmental processes, yet whether and how these effectors are transcriptionally controlled to confer functional specificity so far remain elusive. Herein, we show that a rice C2H2 zinc-finger protein, OsZAF, specifically activates the expression of <em>OsFIP37</em> encoding a core component of the m<sup>6</sup>A methyltransferase complex during microsporogenesis in rice anthers. OsFIP37, in turn, facilitates m<sup>6</sup>A modification and stabilization of an auxin biosynthesis gene <em>OsYUCCA3</em> to promote auxin biosynthesis in anthers. This elevates auxin levels coinciding with upregulation of an auxin response factor <em>OsARF12</em> that positively controls <em>OsZAF</em>, thus creating a positive feedback circuit whereby <em>OsFIP37</em> is continuously activated for local auxin production. Our findings suggest that OsZAF-dependent feedback regulation of m<sup>6</sup>A modification is integral to local auxin biosynthesis and signaling in anthers, which facilitates the timely generation of auxin maxima required for male meiosis in rice.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"204 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142967967","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 : 2025-01-10DOI: 10.1016/j.devcel.2024.12.028
Yaqiong Liu, Xianzhong Lau, Prabhakaran Munusamy, Carlos M. Abascal Sherwell Sanchez, Daniel Snell, Mahesh Sangrithi
Female primordial germ cells (PGCs) undergo X chromosome reactivation (XCR) during genome-wide reprogramming. XCR kinetics and dynamics are poorly understood at a molecular level. Here, we apply single-cell RNA sequencing and chromatin profiling on germ cells from F1 mouse embryos, performing a precise appraisal of XCR spanning from migratory-stage PGCs to gonadal germ cells. Establishment of germ cell sexual dimorphism and X chromosome dosage compensation states in vivo are temporally linked to XCR. Allele-specific analysis evidence that the reactivating X chromosome is minimally active in embryonic day (E)9.5 female PGCs, reactivates gradually, and reaches parity to the active X chromosome in E16.5 oogonia. While Xist is repressed from E10.5 onward, epigenetic memory of X inactivation persists from self-sustained polycomb repressive complex 2 (PRC2) activity. The reactivating X is asymmetrically enriched for histone 3-lysine-27-trimethylation (H3K27me3) at E13.5, which is later reversed, permitting germline gene expression. Our findings relate XCR with PRC2 function in promoting female meiosis.
{"title":"Single-cell RNA-seq identifies protracted mouse germline X chromosome reactivation dynamics directed by a PRC2-dependent mechanism","authors":"Yaqiong Liu, Xianzhong Lau, Prabhakaran Munusamy, Carlos M. Abascal Sherwell Sanchez, Daniel Snell, Mahesh Sangrithi","doi":"10.1016/j.devcel.2024.12.028","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.028","url":null,"abstract":"Female primordial germ cells (PGCs) undergo X chromosome reactivation (XCR) during genome-wide reprogramming. XCR kinetics and dynamics are poorly understood at a molecular level. Here, we apply single-cell RNA sequencing and chromatin profiling on germ cells from <em>F</em><sub><em>1</em></sub> mouse embryos, performing a precise appraisal of XCR spanning from migratory-stage PGCs to gonadal germ cells. Establishment of germ cell sexual dimorphism and X chromosome dosage compensation states <em>in vivo</em> are temporally linked to XCR. Allele-specific analysis evidence that the reactivating X chromosome is minimally active in embryonic day (E)9.5 female PGCs, reactivates gradually, and reaches parity to the active X chromosome in E16.5 oogonia. While <em>Xist</em> is repressed from E10.5 onward, epigenetic memory of X inactivation persists from self-sustained <em>polycomb repressive complex 2</em> (PRC2) activity. The reactivating X is asymmetrically enriched for histone 3-lysine-27-trimethylation (H3K27me3) at E13.5, which is later reversed, permitting germline gene expression. Our findings relate XCR with PRC2 function in promoting female meiosis.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"24 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142939563","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 : 2025-01-10DOI: 10.1016/j.devcel.2024.12.035
Ying Cao, Ruolan Qian, Ruilian Yao, Quan Zheng, Chen Yang, Xupeng Yang, Shuyi Ji, Linmen Zhang, Shujie Zhan, Yiping Wang, Tianshi Wang, Hui Wang, Chun-Ming Wong, Shengxian Yuan, Christopher Heeschen, Qiang Gao, René Bernards, Wenxin Qin, Cun Wang
Intervening in mitochondrial oxidative phosphorylation (OXPHOS) has emerged as a potential therapeutic strategy for certain types of cancers. Employing kinome-based CRISPR screen, we find that knockout of dual-specificity tyrosine phosphorylation-regulated kinase 1A (DYRK1A) synergizes with OXPHOS inhibitor IACS-010759 in liver cancer cells. Targeting DYRK1A combined with OXPHOS inhibitors activates TGF-β signaling, which is crucial for OXPHOS-inhibition-triggered cell death. Mechanistically, upregulation of glutamine transporter solute carrier family 1 member 5 (SLC1A5) transcription compensates for the increased glutamine requirement upon OXPHOS inhibition. DYRK1A directly phosphorylates SMAD3 Thr132, thereby suppressing the negative impact of TGF-β signaling on transcription of SLC1A5, leading to intrinsic resistance of liver cancer cells to OXPHOS inhibition. Moreover, we demonstrate the therapeutic efficacy of IACS-010759 in combination with DYRK1A inhibition in multiple liver cancer models, including xenografts, patient-derived xenografts, and spontaneous tumor model. Our study elucidates how the DYRK1A-TGF-β signaling axis controls the response of tumor cells to OXPHOS inhibition and provides valuable insights into targeting OXPHOS for liver cancer therapy.
{"title":"DYRK1A-TGF-β signaling axis determines sensitivity to OXPHOS inhibition in hepatocellular carcinoma","authors":"Ying Cao, Ruolan Qian, Ruilian Yao, Quan Zheng, Chen Yang, Xupeng Yang, Shuyi Ji, Linmen Zhang, Shujie Zhan, Yiping Wang, Tianshi Wang, Hui Wang, Chun-Ming Wong, Shengxian Yuan, Christopher Heeschen, Qiang Gao, René Bernards, Wenxin Qin, Cun Wang","doi":"10.1016/j.devcel.2024.12.035","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.035","url":null,"abstract":"Intervening in mitochondrial oxidative phosphorylation (OXPHOS) has emerged as a potential therapeutic strategy for certain types of cancers. Employing kinome-based CRISPR screen, we find that knockout of dual-specificity tyrosine phosphorylation-regulated kinase 1A (DYRK1A) synergizes with OXPHOS inhibitor IACS-010759 in liver cancer cells. Targeting DYRK1A combined with OXPHOS inhibitors activates TGF-β signaling, which is crucial for OXPHOS-inhibition-triggered cell death. Mechanistically, upregulation of glutamine transporter solute carrier family 1 member 5 (SLC1A5) transcription compensates for the increased glutamine requirement upon OXPHOS inhibition. DYRK1A directly phosphorylates SMAD3 Thr132, thereby suppressing the negative impact of TGF-β signaling on transcription of SLC1A5, leading to intrinsic resistance of liver cancer cells to OXPHOS inhibition. Moreover, we demonstrate the therapeutic efficacy of IACS-010759 in combination with DYRK1A inhibition in multiple liver cancer models, including xenografts, patient-derived xenografts, and spontaneous tumor model. Our study elucidates how the DYRK1A-TGF-β signaling axis controls the response of tumor cells to OXPHOS inhibition and provides valuable insights into targeting OXPHOS for liver cancer therapy.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"24 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142939568","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 : 2025-01-10DOI: 10.1016/j.devcel.2024.12.030
Ying Yang, Carmel Grace McCullough, Lucas Seninge, Lihao Guo, Woo-Joo Kwon, Yongchun Zhang, Nancy Yanzhe Li, Sadhana Gaddam, Cory Pan, Hanson Zhen, Jessica Torkelson, Ian A. Glass, Gregory W. Charville, Jianwen Que, Joshua M. Stuart, Hongxu Ding, Anthony E. Oro
Human pluripotent stem cell-derived tissue engineering offers great promise for designer cell-based personalized therapeutics, but harnessing such potential requires a deeper understanding of tissue-level interactions. We previously developed a cell replacement manufacturing method for ectoderm-derived skin epithelium. However, it remains challenging to manufacture the endoderm-derived esophageal epithelium despite possessing a similar stratified epithelial structure. Here, we employ single-cell and spatial technologies to generate a spatiotemporal multi-omics cell census for human esophageal development. We identify the cellular diversity, dynamics, and signal communications for the developing esophageal epithelium and stroma. Using Manatee, a machine-learning algorithm, we prioritize the combinations of candidate human developmental signals for in vitro derivation of esophageal basal cells. Functional validation of Manatee predictions leads to a clinically compatible system for manufacturing human esophageal mucosa.
{"title":"A spatiotemporal and machine-learning platform facilitates the manufacturing of hPSC-derived esophageal mucosa","authors":"Ying Yang, Carmel Grace McCullough, Lucas Seninge, Lihao Guo, Woo-Joo Kwon, Yongchun Zhang, Nancy Yanzhe Li, Sadhana Gaddam, Cory Pan, Hanson Zhen, Jessica Torkelson, Ian A. Glass, Gregory W. Charville, Jianwen Que, Joshua M. Stuart, Hongxu Ding, Anthony E. Oro","doi":"10.1016/j.devcel.2024.12.030","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.030","url":null,"abstract":"Human pluripotent stem cell-derived tissue engineering offers great promise for designer cell-based personalized therapeutics, but harnessing such potential requires a deeper understanding of tissue-level interactions. We previously developed a cell replacement manufacturing method for ectoderm-derived skin epithelium. However, it remains challenging to manufacture the endoderm-derived esophageal epithelium despite possessing a similar stratified epithelial structure. Here, we employ single-cell and spatial technologies to generate a spatiotemporal multi-omics cell census for human esophageal development. We identify the cellular diversity, dynamics, and signal communications for the developing esophageal epithelium and stroma. Using Manatee, a machine-learning algorithm, we prioritize the combinations of candidate human developmental signals for <em>in vitro</em> derivation of esophageal basal cells. Functional validation of Manatee predictions leads to a clinically compatible system for manufacturing human esophageal mucosa.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"28 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142939570","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 : 2025-01-09DOI: 10.1016/j.devcel.2024.12.022
Daniel Liesner, Guillaume G. Cossard, Min Zheng, Olivier Godfroy, Josué Barrera-Redondo, Fabian B. Haas, Susana M. Coelho
In many multicellular organisms, sexual development is not determined by XX/XY or ZW/ZZ systems but by U/V sex chromosomes. In U/V systems, sex determination occurs in the haploid phase, with U chromosomes in females and V chromosomes in males. Here, we explore several male, female, and partially sex-reversed male lines of giant kelp to decipher how U/V sex chromosomes and autosomes initiate male versus female development. We identify a key set of genes on the sex chromosomes involved in triggering sexual development and characterize autosomal effector genes underlying sexual differentiation. We show that male, but not female, development involves large-scale transcriptome reorganization with pervasive enrichment in regulatory genes, faster evolutionary rates, and high species-specificity of male-biased genes. Our observations imply that a female-like phenotype is the “ground state”, which is complemented by the presence of a U-chromosome but overridden by a dominant male developmental program triggered by the V-chromosome.
{"title":"Developmental pathways underlying sexual differentiation in the U/V sex chromosome system of giant kelp","authors":"Daniel Liesner, Guillaume G. Cossard, Min Zheng, Olivier Godfroy, Josué Barrera-Redondo, Fabian B. Haas, Susana M. Coelho","doi":"10.1016/j.devcel.2024.12.022","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.022","url":null,"abstract":"In many multicellular organisms, sexual development is not determined by XX/XY or ZW/ZZ systems but by U/V sex chromosomes. In U/V systems, sex determination occurs in the haploid phase, with U chromosomes in females and V chromosomes in males. Here, we explore several male, female, and partially sex-reversed male lines of giant kelp to decipher how U/V sex chromosomes and autosomes initiate male versus female development. We identify a key set of genes on the sex chromosomes involved in triggering sexual development and characterize autosomal effector genes underlying sexual differentiation. We show that male, but not female, development involves large-scale transcriptome reorganization with pervasive enrichment in regulatory genes, faster evolutionary rates, and high species-specificity of male-biased genes. Our observations imply that a female-like phenotype is the “ground state”, which is complemented by the presence of a U-chromosome but overridden by a dominant male developmental program triggered by the V-chromosome.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"28 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142937020","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 : 2025-01-09DOI: 10.1016/j.devcel.2024.12.025
Charlotte N. Miller, Sean Jarrell-Hurtado, Manisha V. Haag, Y. Sara Ye, Mathew Simenc, Paloma Alvarez-Maldonado, Sara Behnami, Ling Zhang, Joseph Swift, Ashot Papikian, Jingting Yu, Kelly Colt, Joseph R. Ecker, Todd P. Michael, Julie A. Law, Wolfgang Busch
The periderm provides a protective barrier in many seed plant species. The development of the suberized phellem, which forms the outermost layer of this important tissue, has become a trait of interest for enhancing both plant resilience to stresses and plant-mediated CO2 sequestration in soils. Despite its importance, very few genes driving phellem development are known. Employing single-nuclei sequencing, we have generated an expression census capturing the complete developmental progression of Arabidopsis root phellem cells, from their progenitor cell type, the pericycle, through to their maturation. With this, we identify a whole suite of genes underlying this process, including MYB67, which we show has a role in phellem cell maturation. Our expression census and functional discoveries represent a resource, expanding our comprehension of secondary growth in plants. These data can be used to fuel discoveries and engineering efforts relevant to plant resilience and climate change.
{"title":"A single-nuclei transcriptome census of the Arabidopsis maturing root identifies that MYB67 controls phellem cell maturation","authors":"Charlotte N. Miller, Sean Jarrell-Hurtado, Manisha V. Haag, Y. Sara Ye, Mathew Simenc, Paloma Alvarez-Maldonado, Sara Behnami, Ling Zhang, Joseph Swift, Ashot Papikian, Jingting Yu, Kelly Colt, Joseph R. Ecker, Todd P. Michael, Julie A. Law, Wolfgang Busch","doi":"10.1016/j.devcel.2024.12.025","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.025","url":null,"abstract":"The periderm provides a protective barrier in many seed plant species. The development of the suberized phellem, which forms the outermost layer of this important tissue, has become a trait of interest for enhancing both plant resilience to stresses and plant-mediated CO<sub>2</sub> sequestration in soils. Despite its importance, very few genes driving phellem development are known. Employing single-nuclei sequencing, we have generated an expression census capturing the complete developmental progression of <em>Arabidopsis</em> root phellem cells, from their progenitor cell type, the pericycle, through to their maturation. With this, we identify a whole suite of genes underlying this process, including <em>MYB67</em>, which we show has a role in phellem cell maturation. Our expression census and functional discoveries represent a resource, expanding our comprehension of secondary growth in plants. These data can be used to fuel discoveries and engineering efforts relevant to plant resilience and climate change.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"56 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142937017","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 : 2025-01-09DOI: 10.1016/j.devcel.2024.12.023
Isidora Banjac, Martti Maimets, Ingrid H.C. Tsang, Marius Dioli, Stine Lind Hansen, Kata Krizic, Raul Bardini Bressan, Cecilia Lövkvist, Kim B. Jensen
The intestinal epithelium has a remarkably high turnover in homeostasis. It remains unresolved how this is orchestrated at the cellular level and how the behavior of stem and progenitor cells ensures tissue maintenance. To address this, we combined quantitative fate mapping in three complementary mouse models with mathematical modeling and single-cell RNA sequencing. Our integrated approach generated a spatially and temporally defined model of crypt maintenance based on two cycling populations: stem cells at the crypt-bottom and transit-amplifying (TA) cells above them. Subsequently, we validated the predictions from the mathematical model, demonstrating that fate decisions between the secretory and absorptive lineages are made within the stem cell compartment, whereas TA cell divisions contribute specifically to the absorptive lineage. These quantitative insights provide further direct evidence for crypt-bottom stem cells as the dominant driver of the intestinal epithelium replenishment.
{"title":"Fate mapping in mouse demonstrates early secretory differentiation directly from Lgr5+ intestinal stem cells","authors":"Isidora Banjac, Martti Maimets, Ingrid H.C. Tsang, Marius Dioli, Stine Lind Hansen, Kata Krizic, Raul Bardini Bressan, Cecilia Lövkvist, Kim B. Jensen","doi":"10.1016/j.devcel.2024.12.023","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.12.023","url":null,"abstract":"The intestinal epithelium has a remarkably high turnover in homeostasis. It remains unresolved how this is orchestrated at the cellular level and how the behavior of stem and progenitor cells ensures tissue maintenance. To address this, we combined quantitative fate mapping in three complementary mouse models with mathematical modeling and single-cell RNA sequencing. Our integrated approach generated a spatially and temporally defined model of crypt maintenance based on two cycling populations: stem cells at the crypt-bottom and transit-amplifying (TA) cells above them. Subsequently, we validated the predictions from the mathematical model, demonstrating that fate decisions between the secretory and absorptive lineages are made within the stem cell compartment, whereas TA cell divisions contribute specifically to the absorptive lineage. These quantitative insights provide further direct evidence for crypt-bottom stem cells as the dominant driver of the intestinal epithelium replenishment.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"20 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2025-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142939569","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}
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