Pub Date : 2024-08-12DOI: 10.1038/s41477-024-01758-0
Lijin Qiao, Takuya Suzaki, Pengbo Liang
Plants constantly adjust their gene expression and metabolism to thrive in diverse environments. In legume root nodules, the surprising role of zinc as an intracellular messenger links environmental changes to transcriptional control.
{"title":"Zinc sensing in nodules regulates symbiotic nitrogen fixation","authors":"Lijin Qiao, Takuya Suzaki, Pengbo Liang","doi":"10.1038/s41477-024-01758-0","DOIUrl":"10.1038/s41477-024-01758-0","url":null,"abstract":"Plants constantly adjust their gene expression and metabolism to thrive in diverse environments. In legume root nodules, the surprising role of zinc as an intracellular messenger links environmental changes to transcriptional control.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141918828","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 : 2024-08-12DOI: 10.1038/s41477-024-01742-8
Yvon Jaillais, Emmanuelle Bayer, Dominique C. Bergmann, Miguel A. Botella, Yohann Boutté, Tolga O. Bozkurt, Marie-Cecile Caillaud, Véronique Germain, Guido Grossmann, Ingo Heilmann, Piers A. Hemsley, Charlotte Kirchhelle, Alexandre Martinière, Yansong Miao, Sebastien Mongrand, Sabine Müller, Lise C. Noack, Yoshihisa Oda, Thomas Ott, Xue Pan, Roman Pleskot, Martin Potocky, Stéphanie Robert, Clara Sanchez Rodriguez, Françoise Simon-Plas, Eugenia Russinova, Daniel Van Damme, Jaimie M. Van Norman, Dolf Weijers, Shaul Yalovsky, Zhenbiao Yang, Enric Zelazny, Julien Gronnier
Biological membranes play a crucial role in actively hosting, modulating and coordinating a wide range of molecular events essential for cellular function. Membranes are organized into diverse domains giving rise to dynamic molecular patchworks. However, the very definition of membrane domains has been the subject of continuous debate. For example, in the plant field, membrane domains are often referred to as nanodomains, nanoclusters, microdomains, lipid rafts, membrane rafts, signalling platforms, foci or liquid-ordered membranes without any clear rationale. In the context of plant–microbe interactions, microdomains have sometimes been used to refer to the large area at the plant–microbe interface. Some of these terms have partially overlapping meanings at best, but they are often used interchangeably in the literature. This situation generates much confusion and limits conceptual progress. There is thus an urgent need for us as a scientific community to resolve these semantic and conceptual controversies by defining an unambiguous nomenclature of membrane domains. In this Review, experts in the field get together to provide explicit definitions of plasma membrane domains in plant systems and experimental guidelines for their study. We propose that plasma membrane domains should not be considered on the basis of their size alone but rather according to the biological system being considered, such as the local membrane environment or the entire cell. This Review aims to define an updated nomenclature for plasma membrane domains in plants. The authors are experts in this field who unite here in an effort to eliminate the ambiguities and confusion that have persisted until now.
{"title":"Guidelines for naming and studying plasma membrane domains in plants","authors":"Yvon Jaillais, Emmanuelle Bayer, Dominique C. Bergmann, Miguel A. Botella, Yohann Boutté, Tolga O. Bozkurt, Marie-Cecile Caillaud, Véronique Germain, Guido Grossmann, Ingo Heilmann, Piers A. Hemsley, Charlotte Kirchhelle, Alexandre Martinière, Yansong Miao, Sebastien Mongrand, Sabine Müller, Lise C. Noack, Yoshihisa Oda, Thomas Ott, Xue Pan, Roman Pleskot, Martin Potocky, Stéphanie Robert, Clara Sanchez Rodriguez, Françoise Simon-Plas, Eugenia Russinova, Daniel Van Damme, Jaimie M. Van Norman, Dolf Weijers, Shaul Yalovsky, Zhenbiao Yang, Enric Zelazny, Julien Gronnier","doi":"10.1038/s41477-024-01742-8","DOIUrl":"10.1038/s41477-024-01742-8","url":null,"abstract":"Biological membranes play a crucial role in actively hosting, modulating and coordinating a wide range of molecular events essential for cellular function. Membranes are organized into diverse domains giving rise to dynamic molecular patchworks. However, the very definition of membrane domains has been the subject of continuous debate. For example, in the plant field, membrane domains are often referred to as nanodomains, nanoclusters, microdomains, lipid rafts, membrane rafts, signalling platforms, foci or liquid-ordered membranes without any clear rationale. In the context of plant–microbe interactions, microdomains have sometimes been used to refer to the large area at the plant–microbe interface. Some of these terms have partially overlapping meanings at best, but they are often used interchangeably in the literature. This situation generates much confusion and limits conceptual progress. There is thus an urgent need for us as a scientific community to resolve these semantic and conceptual controversies by defining an unambiguous nomenclature of membrane domains. In this Review, experts in the field get together to provide explicit definitions of plasma membrane domains in plant systems and experimental guidelines for their study. We propose that plasma membrane domains should not be considered on the basis of their size alone but rather according to the biological system being considered, such as the local membrane environment or the entire cell. This Review aims to define an updated nomenclature for plasma membrane domains in plants. The authors are experts in this field who unite here in an effort to eliminate the ambiguities and confusion that have persisted until now.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141918829","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 : 2024-08-12DOI: 10.1038/s41477-024-01776-y
Raphael Trösch
{"title":"Where chloroplasts and ER meet","authors":"Raphael Trösch","doi":"10.1038/s41477-024-01776-y","DOIUrl":"10.1038/s41477-024-01776-y","url":null,"abstract":"","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141918823","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}
Scaffolding is crucial for constructing most chromosome-level genomes. The high-throughput chromatin conformation capture (Hi-C) technology has become the primary scaffolding strategy due to its convenience and cost-effectiveness. As sequencing technologies and assembly algorithms advance, constructing haplotype-resolved genomes is increasingly preferred because haplotypes can provide additional genetic information on allelic and non-allelic variations. ALLHiC is a widely used allele-aware scaffolding tool designed for this purpose. However, its dependence on chromosome-level reference genomes and a higher chromosome misassignment rate still impede the unravelling of haplotype-resolved genomes. Here we present HapHiC, a reference-independent allele-aware scaffolding tool with superior performance on chromosome assignment as well as contig ordering and orientation. In addition, we provide new insights into the challenges in allele-aware scaffolding by conducting comprehensive analyses on various adverse factors. Finally, with the help of HapHiC, we constructed the haplotype-resolved allotriploid genome for Miscanthus × giganteus, an important lignocellulosic bioenergy crop. This study uncovers key challenges in allele-aware genome scaffolding with Hi-C data. A reference-independent Hi-C scaffolder showing superior performance was developed to construct the haplotype-resolved genome of triploid Miscanthus × giganteus.
{"title":"Chromosome-level scaffolding of haplotype-resolved assemblies using Hi-C data without reference genomes","authors":"Xiaofei Zeng, Zili Yi, Xingtan Zhang, Yuhui Du, Yu Li, Zhiqing Zhou, Sijie Chen, Huijie Zhao, Sai Yang, Yibin Wang, Guoan Chen","doi":"10.1038/s41477-024-01755-3","DOIUrl":"10.1038/s41477-024-01755-3","url":null,"abstract":"Scaffolding is crucial for constructing most chromosome-level genomes. The high-throughput chromatin conformation capture (Hi-C) technology has become the primary scaffolding strategy due to its convenience and cost-effectiveness. As sequencing technologies and assembly algorithms advance, constructing haplotype-resolved genomes is increasingly preferred because haplotypes can provide additional genetic information on allelic and non-allelic variations. ALLHiC is a widely used allele-aware scaffolding tool designed for this purpose. However, its dependence on chromosome-level reference genomes and a higher chromosome misassignment rate still impede the unravelling of haplotype-resolved genomes. Here we present HapHiC, a reference-independent allele-aware scaffolding tool with superior performance on chromosome assignment as well as contig ordering and orientation. In addition, we provide new insights into the challenges in allele-aware scaffolding by conducting comprehensive analyses on various adverse factors. Finally, with the help of HapHiC, we constructed the haplotype-resolved allotriploid genome for Miscanthus × giganteus, an important lignocellulosic bioenergy crop. This study uncovers key challenges in allele-aware genome scaffolding with Hi-C data. A reference-independent Hi-C scaffolder showing superior performance was developed to construct the haplotype-resolved genome of triploid Miscanthus × giganteus.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141891850","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 : 2024-08-05DOI: 10.1038/s41477-024-01756-2
To overcome key challenges in scaffolding chromosome-level haplotypes with Hi-C data, we developed HapHiC, a Hi-C scaffolding tool that exhibits superior performance in handling haplotype-resolved assemblies without the need for reference genomes. We used HapHiC to construct the complex genome of triploid Miscanthus × giganteus.
{"title":"Achieving de novo scaffolding of chromosome-level haplotypes using Hi-C data","authors":"","doi":"10.1038/s41477-024-01756-2","DOIUrl":"10.1038/s41477-024-01756-2","url":null,"abstract":"To overcome key challenges in scaffolding chromosome-level haplotypes with Hi-C data, we developed HapHiC, a Hi-C scaffolding tool that exhibits superior performance in handling haplotype-resolved assemblies without the need for reference genomes. We used HapHiC to construct the complex genome of triploid Miscanthus × giganteus.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141893813","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}
In angiosperms, epigenetic profiles for genomic imprinting are established before fertilization. However, the causal relationships between epigenetic modifications and imprinted expression are not fully understood. In this study, we classified ‘persistent’ and ‘stage-specific’ imprinted genes on the basis of time-course transcriptome analysis in rice (Oryza sativa) endosperm and compared them to epigenetic modifications at a single time point. While the levels of epigenetic modifications are relatively low in stage-specific imprinted genes, they are considerably higher in persistent imprinted genes. Overall trends revealed that the maternal alleles of maternally expressed imprinted genes are activated by DNA demethylation, while the maternal alleles of paternally expressed imprinted genes with gene body methylation (gbM) are silenced by DNA demethylation and H3K27me3 deposition, and these regions are associated with an enriched motif related to Tc/Mar-Stowaway. Our findings provide insight into the stability of genomic imprinting and the potential variations associated with endosperm development, different cell types and parental genotypes. Time-course analysis of rice imprinted genes revealed persistent and stage-specific imprinted genes. These two classes showed differences in the degree of epigenetic status and biased expression in a temporal and spatial manner in the endosperm.
{"title":"Multilayered epigenetic control of persistent and stage-specific imprinted genes in rice endosperm","authors":"Kaoru Tonosaki, Daichi Susaki, Hatsune Morinaka, Akemi Ono, Hiroki Nagata, Hiroyasu Furuumi, Ken-Ichi Nonomura, Yutaka Sato, Keiko Sugimoto, Luca Comai, Katsunori Hatakeyama, Taiji Kawakatsu, Tetsu Kinoshita","doi":"10.1038/s41477-024-01754-4","DOIUrl":"10.1038/s41477-024-01754-4","url":null,"abstract":"In angiosperms, epigenetic profiles for genomic imprinting are established before fertilization. However, the causal relationships between epigenetic modifications and imprinted expression are not fully understood. In this study, we classified ‘persistent’ and ‘stage-specific’ imprinted genes on the basis of time-course transcriptome analysis in rice (Oryza sativa) endosperm and compared them to epigenetic modifications at a single time point. While the levels of epigenetic modifications are relatively low in stage-specific imprinted genes, they are considerably higher in persistent imprinted genes. Overall trends revealed that the maternal alleles of maternally expressed imprinted genes are activated by DNA demethylation, while the maternal alleles of paternally expressed imprinted genes with gene body methylation (gbM) are silenced by DNA demethylation and H3K27me3 deposition, and these regions are associated with an enriched motif related to Tc/Mar-Stowaway. Our findings provide insight into the stability of genomic imprinting and the potential variations associated with endosperm development, different cell types and parental genotypes. Time-course analysis of rice imprinted genes revealed persistent and stage-specific imprinted genes. These two classes showed differences in the degree of epigenetic status and biased expression in a temporal and spatial manner in the endosperm.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-07-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141794605","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 : 2024-07-30DOI: 10.1038/s41477-024-01741-9
Bayley R. McDonald, Colette L. Picard, Ian M. Brabb, Marina I. Savenkova, Robert J. Schmitz, Steven E. Jacobsen, Sascha H. Duttke
Unstable transcripts have emerged as markers of active enhancers in vertebrates and shown to be involved in many cellular processes and medical disorders. However, their prevalence and role in plants is largely unexplored. Here, we comprehensively captured all actively initiating (nascent) transcripts across diverse crops and other plants using capped small (cs)RNA sequencing. We discovered that unstable transcripts are rare in plants, unlike in vertebrates, and when present, often originate from promoters. In addition, many ‘distal’ elements in plants initiate tissue-specific stable transcripts and are likely bona fide promoters of as-yet-unannotated genes or non-coding RNAs, cautioning against using reference genome annotations to infer putative enhancer sites. To investigate enhancer function, we integrated data from self-transcribing active regulatory region (STARR) sequencing. We found that annotated promoters and other regions that initiate stable transcripts, but not those marked by unstable or bidirectional unstable transcripts, showed stronger enhancer activity in this assay. Our findings underscore the blurred line between promoters and enhancers and suggest that cis-regulatory elements can encompass diverse structures and mechanisms in eukaryotes, including humans. Unstable transcripts like enhancer RNAs are common in vertebrates. McDonald et al. show that such unstable transcripts are rare in plants and that promoters can function as potent enhancers, suggesting diverse cis-regulatory mechanisms in eukaryotes.
{"title":"Enhancers associated with unstable RNAs are rare in plants","authors":"Bayley R. McDonald, Colette L. Picard, Ian M. Brabb, Marina I. Savenkova, Robert J. Schmitz, Steven E. Jacobsen, Sascha H. Duttke","doi":"10.1038/s41477-024-01741-9","DOIUrl":"10.1038/s41477-024-01741-9","url":null,"abstract":"Unstable transcripts have emerged as markers of active enhancers in vertebrates and shown to be involved in many cellular processes and medical disorders. However, their prevalence and role in plants is largely unexplored. Here, we comprehensively captured all actively initiating (nascent) transcripts across diverse crops and other plants using capped small (cs)RNA sequencing. We discovered that unstable transcripts are rare in plants, unlike in vertebrates, and when present, often originate from promoters. In addition, many ‘distal’ elements in plants initiate tissue-specific stable transcripts and are likely bona fide promoters of as-yet-unannotated genes or non-coding RNAs, cautioning against using reference genome annotations to infer putative enhancer sites. To investigate enhancer function, we integrated data from self-transcribing active regulatory region (STARR) sequencing. We found that annotated promoters and other regions that initiate stable transcripts, but not those marked by unstable or bidirectional unstable transcripts, showed stronger enhancer activity in this assay. Our findings underscore the blurred line between promoters and enhancers and suggest that cis-regulatory elements can encompass diverse structures and mechanisms in eukaryotes, including humans. Unstable transcripts like enhancer RNAs are common in vertebrates. McDonald et al. show that such unstable transcripts are rare in plants and that promoters can function as potent enhancers, suggesting diverse cis-regulatory mechanisms in eukaryotes.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-07-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41477-024-01741-9.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141794606","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 : 2024-07-26DOI: 10.1038/s41477-024-01747-3
Sergi Munné-Bosch, Jessyca Adelle Silva Santos
Plant invasions are becomingly increasingly common with global climate change. As a significant threat to biodiversity, appropriate management of invasive species is critical for the protection of native flora. However, many of the management strategies aimed at combating the impacts of invasive species only end up exacerbating them.
{"title":"The dramatic effects of well-intentioned but ill-designed management strategies in plant biological invasions","authors":"Sergi Munné-Bosch, Jessyca Adelle Silva Santos","doi":"10.1038/s41477-024-01747-3","DOIUrl":"10.1038/s41477-024-01747-3","url":null,"abstract":"Plant invasions are becomingly increasingly common with global climate change. As a significant threat to biodiversity, appropriate management of invasive species is critical for the protection of native flora. However, many of the management strategies aimed at combating the impacts of invasive species only end up exacerbating them.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141764282","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 : 2024-07-26DOI: 10.1038/s41477-024-01760-6
Duy-Chi Trinh, Isaty Melogno, Marjolaine Martin, Christophe Trehin, Richard S. Smith, Olivier Hamant
In most plant species, sepals—the outermost floral organs—provide a protective shield for reproductive organs. How the floral bud becomes sealed is unknown. In Arabidopsis, we identified a small region at the sepal tip that is markedly curved inward early on and remains curved even after anthesis. Through modelling and quantitative growth analysis, we find that this hook emerges from growth arrest at the tip at a stage when cortical microtubules align with growth-derived tensile stress. Depolymerizing microtubules specifically at young sepal tips hindered hook formation and resulted in open floral buds. Mutants with defective growth pattern at the tip failed to curve inwards, whereas mutants with enhanced alignment of cortical microtubules at the tip exhibited a stronger hook. We propose that floral buds are locked due to a stress-derived growth arrest event curving the sepal tip and forming a rigid hook early on during flower development. Floral buds are closed structures that protect reproductive organs. Here the authors find that differential growth prescribes transverse tensile stress and growth arrest at the sepal tip, which in turn curve it and form a rigid hook to seal the floral bud.
{"title":"Arabidopsis floral buds are locked through stress-induced sepal tip curving","authors":"Duy-Chi Trinh, Isaty Melogno, Marjolaine Martin, Christophe Trehin, Richard S. Smith, Olivier Hamant","doi":"10.1038/s41477-024-01760-6","DOIUrl":"10.1038/s41477-024-01760-6","url":null,"abstract":"In most plant species, sepals—the outermost floral organs—provide a protective shield for reproductive organs. How the floral bud becomes sealed is unknown. In Arabidopsis, we identified a small region at the sepal tip that is markedly curved inward early on and remains curved even after anthesis. Through modelling and quantitative growth analysis, we find that this hook emerges from growth arrest at the tip at a stage when cortical microtubules align with growth-derived tensile stress. Depolymerizing microtubules specifically at young sepal tips hindered hook formation and resulted in open floral buds. Mutants with defective growth pattern at the tip failed to curve inwards, whereas mutants with enhanced alignment of cortical microtubules at the tip exhibited a stronger hook. We propose that floral buds are locked due to a stress-derived growth arrest event curving the sepal tip and forming a rigid hook early on during flower development. Floral buds are closed structures that protect reproductive organs. Here the authors find that differential growth prescribes transverse tensile stress and growth arrest at the sepal tip, which in turn curve it and form a rigid hook to seal the floral bud.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8,"publicationDate":"2024-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141764313","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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