The timing of flowering in plants is modulated by both carbon (C) and nitrogen (N) signaling pathways. In a previous study, we established a pivotal role of the sucrose-signaling trehalose 6-phosphate pathway in regulating flowering under N-limited short-day conditions. In this work, we show that both wild-type Arabidopsis (Arabidopsis thaliana) plants grown under N-limited conditions and knock-down plants of TREHALOSE PHOSPHATE SYNTHASE 1 induce FLOWERING LOCUS C (FLC) expression, a well-known floral repressor associated with vernalization. When exposed to an extended period of cold, a flc mutant fails to respond to N availability and flowers at the same time under N-limited and full-nutrition conditions. Our data suggest that SUCROSE NON-FERMENTING 1 RELATED KINASE 1-dependent trehalose 6-phosphate-mediated C signaling and a mechanism downstream of N signaling (likely involving NIN-LIKE PROTEIN 7) impact the expression of FLC. Collectively, our data underscore the existence of a multi-factor regulatory system in which the C and N signaling pathways jointly govern the regulation of flowering in plants.
植物的开花时间受碳（C）和氮（N）信号途径的调节。在之前的一项研究中，我们确定了蔗糖-6-磷酸三卤糖信号途径在氮限制的短日照条件下调节开花的关键作用。在这项研究中，我们发现在氮限制条件下生长的野生型拟南芥（Arabidopsis thaliana）植株和三卤糖磷酸合成酶 1 的基因敲除植株都能诱导花序抑制因子 C（FLC）的表达，FLC 是一种与春化相关的著名花序抑制因子。当暴露于较长时间的低温时，flc 突变体不能对氮的可用性做出反应，并在氮限制和全营养条件下同时开花。我们的数据表明，依赖于 6-磷酸三卤糖介导的 C 信号转导和 N 信号转导下游机制（可能涉及 NIN-LIKE PROTEIN 7）影响了 FLC 的表达。总之，我们的数据强调了多因素调控系统的存在，其中 C 信号途径和 N 信号途径共同调控植物开花。
{"title":"Carbon and nitrogen signaling regulate FLOWERING LOCUS C and impact flowering time in Arabidopsis","authors":"Vladislav Gramma, Justyna Jadwiga Olas, Vasiliki Zacharaki, Jathish Ponnu, Magdalena Musialak-Lange, Vanessa Wahl","doi":"10.1093/plphys/kiae594","DOIUrl":"https://doi.org/10.1093/plphys/kiae594","url":null,"abstract":"The timing of flowering in plants is modulated by both carbon (C) and nitrogen (N) signaling pathways. In a previous study, we established a pivotal role of the sucrose-signaling trehalose 6-phosphate pathway in regulating flowering under N-limited short-day conditions. In this work, we show that both wild-type Arabidopsis (Arabidopsis thaliana) plants grown under N-limited conditions and knock-down plants of TREHALOSE PHOSPHATE SYNTHASE 1 induce FLOWERING LOCUS C (FLC) expression, a well-known floral repressor associated with vernalization. When exposed to an extended period of cold, a flc mutant fails to respond to N availability and flowers at the same time under N-limited and full-nutrition conditions. Our data suggest that SUCROSE NON-FERMENTING 1 RELATED KINASE 1-dependent trehalose 6-phosphate-mediated C signaling and a mechanism downstream of N signaling (likely involving NIN-LIKE PROTEIN 7) impact the expression of FLC. Collectively, our data underscore the existence of a multi-factor regulatory system in which the C and N signaling pathways jointly govern the regulation of flowering in plants.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"29 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142600987","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}
Epigenetic modifications play vital roles in many biological processes. Flower senescence involves epigenetic factors that influence the chromatin state and gene expression. However, the molecular mechanism underlying the role of histone deacetylation in regulating flower senescence has not been elucidated. Here, we demonstrate that histone deacetylation is involved in flower senescence by fine-tuning reactive oxygen species (ROS) homeostasis in rose (Rosa hybrida). Our data reveal that the histone lysine deacetyltransferase RhHDA15 inhibits ROS accumulation and petal senescence by downregulating the expression of NADPH OXIDASE/RESPIRATORY BURST OXIDASE HOMOLOG (RhRboh) genes. Furthermore, the transcription factor RELATED TO ABI3/VP1 2 (RhRAV2) recruits RhHDA15 and the co-repressor TOPLESS (RhTPL) to suppress flower senescence by reducing H3 lysine 9 acetylation (H3K9ac) at the RhRbohA1/2 promoter and thus directly inhibiting precocious RhRbohA1/2 expression. Our work sheds light on an epigenetic mechanism in which histone deacetylation plays a crucial role in controlling petal senescence by precisely fine-tuning ROS homeostasis, providing insights into the regulatory network of organ senescence.
{"title":"The histone deacetylase RhHDA15 represses petal senescence by epigenetically regulating reactive oxygen species homeostasis in rose","authors":"Meizhu Qin, Zhicheng Wu, Chengkun Zhang, Yunhe Jiang, Cai-Zhong Jiang, Xiaoming Sun, Junping Gao","doi":"10.1093/plphys/kiae612","DOIUrl":"https://doi.org/10.1093/plphys/kiae612","url":null,"abstract":"Epigenetic modifications play vital roles in many biological processes. Flower senescence involves epigenetic factors that influence the chromatin state and gene expression. However, the molecular mechanism underlying the role of histone deacetylation in regulating flower senescence has not been elucidated. Here, we demonstrate that histone deacetylation is involved in flower senescence by fine-tuning reactive oxygen species (ROS) homeostasis in rose (Rosa hybrida). Our data reveal that the histone lysine deacetyltransferase RhHDA15 inhibits ROS accumulation and petal senescence by downregulating the expression of NADPH OXIDASE/RESPIRATORY BURST OXIDASE HOMOLOG (RhRboh) genes. Furthermore, the transcription factor RELATED TO ABI3/VP1 2 (RhRAV2) recruits RhHDA15 and the co-repressor TOPLESS (RhTPL) to suppress flower senescence by reducing H3 lysine 9 acetylation (H3K9ac) at the RhRbohA1/2 promoter and thus directly inhibiting precocious RhRbohA1/2 expression. Our work sheds light on an epigenetic mechanism in which histone deacetylation plays a crucial role in controlling petal senescence by precisely fine-tuning ROS homeostasis, providing insights into the regulatory network of organ senescence.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"127 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142599534","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}
Plant fertility is fundamental to plant survival and requires the coordinated interaction of developmental pathways and signaling molecules. Nitric oxide (NO) is a small, gaseous signaling molecule that plays crucial roles in plant fertility as well as other developmental processes and stress responses. NO influences biological processes through S-nitrosation, the posttranslational modification of protein cysteines to S-nitrosocysteine (R-SNO). NO homeostasis is controlled by S-nitrosoglutathione reductase (GSNOR), which reduces S-nitrosoglutathione (GSNO), the major form of NO in cells. GSNOR mutants (hot5-2/gsnor1) have defects in female gametophyte development along with elevated levels of reactive nitrogen species and R-SNOs. To better understand the fertility defects in hot5-2, we investigated the in vivo nitrosoproteome of Arabidopsis (Arabidopsis thaliana) floral tissues coupled with quantitative proteomics of pistils. To identify protein-SNOs, we used an organomercury-based method that involves direct reaction with S-nitrosocysteine, enabling specific identification of S-nitrosocysteine–containing peptides and S-nitrosated proteins. We identified 1102 endogenously S-nitrosated proteins in floral tissues, of which 1049 were unique to hot5-2. Among the identified proteins, 728 were novel S-nitrosation targets. Notably, specific UDP-glycosyltransferases and argonaute proteins are S-nitrosated in floral tissues and differentially regulated in pistils. We also discovered S-nitrosation of subunits of the 26S proteasome together with increased abundance of proteasomal components and enhanced trypsin-like proteasomal activity in hot5-2 pistils. Our data establish a method for nitrosoprotein detection in plants, expand knowledge of the plant S-nitrosoproteome, and suggest that nitro-oxidative modification and NO homeostasis are critical to protein quality control in reproductive tissues.
{"title":"Disrupted Nitric Oxide Homeostasis Impacts Fertility through Multiple Processes Including Protein Quality Control","authors":"Patrick Treffon, Elizabeth Vierling","doi":"10.1093/plphys/kiae609","DOIUrl":"https://doi.org/10.1093/plphys/kiae609","url":null,"abstract":"Plant fertility is fundamental to plant survival and requires the coordinated interaction of developmental pathways and signaling molecules. Nitric oxide (NO) is a small, gaseous signaling molecule that plays crucial roles in plant fertility as well as other developmental processes and stress responses. NO influences biological processes through S-nitrosation, the posttranslational modification of protein cysteines to S-nitrosocysteine (R-SNO). NO homeostasis is controlled by S-nitrosoglutathione reductase (GSNOR), which reduces S-nitrosoglutathione (GSNO), the major form of NO in cells. GSNOR mutants (hot5-2/gsnor1) have defects in female gametophyte development along with elevated levels of reactive nitrogen species and R-SNOs. To better understand the fertility defects in hot5-2, we investigated the in vivo nitrosoproteome of Arabidopsis (Arabidopsis thaliana) floral tissues coupled with quantitative proteomics of pistils. To identify protein-SNOs, we used an organomercury-based method that involves direct reaction with S-nitrosocysteine, enabling specific identification of S-nitrosocysteine–containing peptides and S-nitrosated proteins. We identified 1102 endogenously S-nitrosated proteins in floral tissues, of which 1049 were unique to hot5-2. Among the identified proteins, 728 were novel S-nitrosation targets. Notably, specific UDP-glycosyltransferases and argonaute proteins are S-nitrosated in floral tissues and differentially regulated in pistils. We also discovered S-nitrosation of subunits of the 26S proteasome together with increased abundance of proteasomal components and enhanced trypsin-like proteasomal activity in hot5-2 pistils. Our data establish a method for nitrosoprotein detection in plants, expand knowledge of the plant S-nitrosoproteome, and suggest that nitro-oxidative modification and NO homeostasis are critical to protein quality control in reproductive tissues.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"37 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142598309","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}
Guy Levin, Michael Yasmin, Oded Liran, Rawad Hanna, Oded Kleifeld, Guy Horev, Francis-André Wollman, Gadi Schuster, Wojciech J Nawrocki
Non-photochemical quenching (NPQ) mechanisms are crucial for protecting photosynthesis from photoinhibition in plants, algae, and cyanobacteria, and their modulation is a long-standing goal for improving photosynthesis and crop yields. The current work demonstrates that Chlorella ohadii, a green micro-alga that thrives in the desert under high light intensities that are fatal to many photosynthetic organisms does not perform nor require NPQ to protect photosynthesis under constant high light. Instead of dissipating excess energy, it minimizes its uptake by eliminating the photosynthetic antenna of photosystem II. In addition, it accumulates antioxidants that neutralize harmful reactive oxygen species (ROS) and increases cyclic electron flow around PSI. These NPQ-independent responses proved efficient in preventing ROS accumulation and reducing oxidative damage to proteins in high-light-grown cells.
{"title":"Processes independent of nonphotochemical quenching protect a high-light-tolerant desert alga from oxidative stress","authors":"Guy Levin, Michael Yasmin, Oded Liran, Rawad Hanna, Oded Kleifeld, Guy Horev, Francis-André Wollman, Gadi Schuster, Wojciech J Nawrocki","doi":"10.1093/plphys/kiae608","DOIUrl":"https://doi.org/10.1093/plphys/kiae608","url":null,"abstract":"Non-photochemical quenching (NPQ) mechanisms are crucial for protecting photosynthesis from photoinhibition in plants, algae, and cyanobacteria, and their modulation is a long-standing goal for improving photosynthesis and crop yields. The current work demonstrates that Chlorella ohadii, a green micro-alga that thrives in the desert under high light intensities that are fatal to many photosynthetic organisms does not perform nor require NPQ to protect photosynthesis under constant high light. Instead of dissipating excess energy, it minimizes its uptake by eliminating the photosynthetic antenna of photosystem II. In addition, it accumulates antioxidants that neutralize harmful reactive oxygen species (ROS) and increases cyclic electron flow around PSI. These NPQ-independent responses proved efficient in preventing ROS accumulation and reducing oxidative damage to proteins in high-light-grown cells.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"5 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597602","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}
Serena Flori, Jack Dickenson, Trupti Gaikwad, Isobel Cole, Nicholas Smirnoff, Katherine Helliwell, Colin Brownlee, Glen Wheeler
Diatoms are a group of silicified algae that play a major role in marine and freshwater ecosystems. Diatom chloroplasts were acquired by secondary endosymbiosis and exhibit important structural and functional differences from the primary plastids of land plants and green algae. Many functions of primary plastids, including photoacclimation and inorganic carbon acquisition, are regulated by calcium-dependent signalling processes. Calcium signalling has also been implicated in the photoprotective responses of diatoms; however, the nature of calcium elevations in diatom chloroplasts and their wider role in cell signalling remains unknown. Using genetically encoded calcium indicators, we find that the diatom Phaeodactylum tricornutum exhibits dynamic calcium elevations within the chloroplast stroma. Stromal calcium ([Ca2+]str) acts independently from the cytosol and is not elevated by stimuli that induce large cytosolic calcium ([Ca2+]cyt) elevations. In contrast, high light and exogenous hydrogen peroxide (H2O2) induce large, sustained [Ca2+]str elevations that are not replicated in the cytosol. Measurements using the fluorescent H2O2 sensor roGFP2-Oxidant Receptor Peroxidase 1 (Orp1) indicate that [Ca2+]str elevations induced by these stimuli correspond to the accumulation of H2O2 in the chloroplast. [Ca2+]str elevations were also induced by adding methyl viologen, which generates superoxide within the chloroplast, and by treatments that disrupt non-photochemical quenching (NPQ). The findings indicate that diatoms generate specific [Ca2+]str elevations in response to high light and oxidative stress that likely modulate the activity of calcium-sensitive components in photoprotection and other regulatory pathways.
{"title":"Diatoms exhibit dynamic chloroplast calcium signals in response to high light and oxidative stress","authors":"Serena Flori, Jack Dickenson, Trupti Gaikwad, Isobel Cole, Nicholas Smirnoff, Katherine Helliwell, Colin Brownlee, Glen Wheeler","doi":"10.1093/plphys/kiae591","DOIUrl":"https://doi.org/10.1093/plphys/kiae591","url":null,"abstract":"Diatoms are a group of silicified algae that play a major role in marine and freshwater ecosystems. Diatom chloroplasts were acquired by secondary endosymbiosis and exhibit important structural and functional differences from the primary plastids of land plants and green algae. Many functions of primary plastids, including photoacclimation and inorganic carbon acquisition, are regulated by calcium-dependent signalling processes. Calcium signalling has also been implicated in the photoprotective responses of diatoms; however, the nature of calcium elevations in diatom chloroplasts and their wider role in cell signalling remains unknown. Using genetically encoded calcium indicators, we find that the diatom Phaeodactylum tricornutum exhibits dynamic calcium elevations within the chloroplast stroma. Stromal calcium ([Ca2+]str) acts independently from the cytosol and is not elevated by stimuli that induce large cytosolic calcium ([Ca2+]cyt) elevations. In contrast, high light and exogenous hydrogen peroxide (H2O2) induce large, sustained [Ca2+]str elevations that are not replicated in the cytosol. Measurements using the fluorescent H2O2 sensor roGFP2-Oxidant Receptor Peroxidase 1 (Orp1) indicate that [Ca2+]str elevations induced by these stimuli correspond to the accumulation of H2O2 in the chloroplast. [Ca2+]str elevations were also induced by adding methyl viologen, which generates superoxide within the chloroplast, and by treatments that disrupt non-photochemical quenching (NPQ). The findings indicate that diatoms generate specific [Ca2+]str elevations in response to high light and oxidative stress that likely modulate the activity of calcium-sensitive components in photoprotection and other regulatory pathways.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"13 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597552","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}
Jiaxin Yang, Xiayang Lu, Suying Hu, Xiaozeng Yang, Xiaoyan Cao
MicroRNAs (miRNAs) are non-coding endogenous single-stranded RNAs that regulate target gene expression by reducing their transcription and translation. Several miRNAs in plants function in secondary metabolism. The dried root of Scutellaria baicalensis Georgi is a traditional Chinese medicine that contains flavonoids (baicalin, wogonoside, and baicalein) as its main active ingredients. Although the S. baicalensis genome sequence has been published, information regarding its miRNAs is lacking. In this study, 12 small RNA libraries of different S. baicalensis tissues were compiled, including roots, stems, leaves, and flowers. A total of 129 miRNAs were identified, including 99 miRNAs from 27 miRNA families and 30 predicted miRNAs. Furthermore, 46 reliable target genes of 15 miRNA families were revealed using psRNAtarget and confirmed by degradome sequencing. It was speculated that the microRNA858 (miR858)–SbMYB47 module might be involved in flavonoid biosynthesis. Transient assays in Nicotiana benthamiana leaves indicated that miR858 targets SbMYB47 and suppresses its expression. Artificial miRNA-mediated knockdown of miR858 and overexpression of SbMYB47 significantly increased the flavonoid content in S. baicalensis hairy roots, while SbMYB47 knockdown inhibited flavonoid accumulation. Yeast one-hybrid and dual-luciferase assays indicated that SbMYB47 directly binds to and activates the S. baicalensis phenylalanine ammonia-lyase 3 (SbPAL-3) and flavone synthase II (SbFNSⅡ-2) promoters. Our findings reveal the link between the miR858–SbMYB47 module and flavonoid biosynthesis, providing a potential strategy for the production of flavonoids with important pharmacological activities through metabolic engineering.
{"title":"microRNA858 represses the transcription factor gene SbMYB47 and regulates flavonoid biosynthesis in Scutellaria baicalensis","authors":"Jiaxin Yang, Xiayang Lu, Suying Hu, Xiaozeng Yang, Xiaoyan Cao","doi":"10.1093/plphys/kiae607","DOIUrl":"https://doi.org/10.1093/plphys/kiae607","url":null,"abstract":"MicroRNAs (miRNAs) are non-coding endogenous single-stranded RNAs that regulate target gene expression by reducing their transcription and translation. Several miRNAs in plants function in secondary metabolism. The dried root of Scutellaria baicalensis Georgi is a traditional Chinese medicine that contains flavonoids (baicalin, wogonoside, and baicalein) as its main active ingredients. Although the S. baicalensis genome sequence has been published, information regarding its miRNAs is lacking. In this study, 12 small RNA libraries of different S. baicalensis tissues were compiled, including roots, stems, leaves, and flowers. A total of 129 miRNAs were identified, including 99 miRNAs from 27 miRNA families and 30 predicted miRNAs. Furthermore, 46 reliable target genes of 15 miRNA families were revealed using psRNAtarget and confirmed by degradome sequencing. It was speculated that the microRNA858 (miR858)–SbMYB47 module might be involved in flavonoid biosynthesis. Transient assays in Nicotiana benthamiana leaves indicated that miR858 targets SbMYB47 and suppresses its expression. Artificial miRNA-mediated knockdown of miR858 and overexpression of SbMYB47 significantly increased the flavonoid content in S. baicalensis hairy roots, while SbMYB47 knockdown inhibited flavonoid accumulation. Yeast one-hybrid and dual-luciferase assays indicated that SbMYB47 directly binds to and activates the S. baicalensis phenylalanine ammonia-lyase 3 (SbPAL-3) and flavone synthase II (SbFNSⅡ-2) promoters. Our findings reveal the link between the miR858–SbMYB47 module and flavonoid biosynthesis, providing a potential strategy for the production of flavonoids with important pharmacological activities through metabolic engineering.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"147 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597600","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}
Wenting Liang, Ángel M Zamarreño, Salvador Torres-Montilla, Antonio de la Torre, Jean Chrisologue Totozafy, Takuya Kaji, Minoru Ueda, Massimiliano Corso, José M García-Mina, Roberto Solano, Andrea Chini
Jasmonates are important phytohormones that regulate plant tolerance to biotic and abiotic stresses, and developmental processes. Distinct jasmonates in different plant lineages activate a conserved signalling pathway that mediates these responses: dinor-12-oxo-phytodienoic acid (dn-OPDA) isomers in bryophytes and lycophytes, and JA-Ile in most vascular plants. In many cases, the final responses triggered by these phytohormones depend on the accumulation of specialized metabolites. To identify compounds regulated by the dn-OPDA pathway in the liverwort Marchantia polymorpha, untargeted metabolomic analyses were carried out in response to wounding, a stress that activates the dn-OPDA pathway. A previously unreported group of molecules was identified from these analyses: dn-OPDA-amino acid conjugates (dn-OPDA-aas). Their accumulation after wounding and herbivory was confirmed by targeted metabolic profiling in Marchantia and in all species in which we previously detected dn-iso-OPDA. Mutants in GRETCHEN-HAGEN 3A (MpGH3A) failed to accumulate dn-OPDA-aa conjugates and showed a constitutive activation of the OPDA pathway and increased resistance to herbivory. Our results show that dn-iso-OPDA bioactivity is reduced by amino acid conjugation. Therefore, jasmonate conjugation in land plants plays dichotomous roles: jasmonic acid (JA) conjugation with isoleucine (Ile) produces the bioactive JA-Ile in tracheophytes, whereas conjugation of dn-iso-OPDA with different amino acids deactivates the phytohormone in bryophytes and lycophytes.
{"title":"dn-OPDA conjugation with amino acids inhibits its phytohormone bioactivity in Marchantia polymorpha","authors":"Wenting Liang, Ángel M Zamarreño, Salvador Torres-Montilla, Antonio de la Torre, Jean Chrisologue Totozafy, Takuya Kaji, Minoru Ueda, Massimiliano Corso, José M García-Mina, Roberto Solano, Andrea Chini","doi":"10.1093/plphys/kiae610","DOIUrl":"https://doi.org/10.1093/plphys/kiae610","url":null,"abstract":"Jasmonates are important phytohormones that regulate plant tolerance to biotic and abiotic stresses, and developmental processes. Distinct jasmonates in different plant lineages activate a conserved signalling pathway that mediates these responses: dinor-12-oxo-phytodienoic acid (dn-OPDA) isomers in bryophytes and lycophytes, and JA-Ile in most vascular plants. In many cases, the final responses triggered by these phytohormones depend on the accumulation of specialized metabolites. To identify compounds regulated by the dn-OPDA pathway in the liverwort Marchantia polymorpha, untargeted metabolomic analyses were carried out in response to wounding, a stress that activates the dn-OPDA pathway. A previously unreported group of molecules was identified from these analyses: dn-OPDA-amino acid conjugates (dn-OPDA-aas). Their accumulation after wounding and herbivory was confirmed by targeted metabolic profiling in Marchantia and in all species in which we previously detected dn-iso-OPDA. Mutants in GRETCHEN-HAGEN 3A (MpGH3A) failed to accumulate dn-OPDA-aa conjugates and showed a constitutive activation of the OPDA pathway and increased resistance to herbivory. Our results show that dn-iso-OPDA bioactivity is reduced by amino acid conjugation. Therefore, jasmonate conjugation in land plants plays dichotomous roles: jasmonic acid (JA) conjugation with isoleucine (Ile) produces the bioactive JA-Ile in tracheophytes, whereas conjugation of dn-iso-OPDA with different amino acids deactivates the phytohormone in bryophytes and lycophytes.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"14 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597607","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}
J -F Trontin, M D Sow, A Delaunay, I Modesto, C Teyssier, I Reymond, F Canlet, N Boizot, C Le Metté, A Gibert, C Chaparro, C Daviaud, J Tost, C Miguel, M -A Lelu-Walter, S Maury
Embryogenesis is a brief but potentially critical phase in the tree life cycle for adaptive phenotypic plasticity. Using somatic embryogenesis in maritime pine (Pinus pinaster Ait.), we found that temperature during the maturation phase affects embryo development and post-embryonic tree growth for up to three years. We examined whether this somatic stress memory could stem from temperature- and/or development-induced changes in DNA methylation. For this, we developed a 200 Mb custom sequence capture bisulfite analysis of genes and promoters to identify differentially methylated cytosines (DMCs) between temperature treatments (18, 23, and 28°C) and developmental stages (immature and cotyledonary embryos, shoot apical meristem of 2-year-old plants) and investigate if these differences can be mitotically transmitted from embryonic to post-embryonic development (epigenetic memory). We revealed a high prevalence of temperature-induced DMCs in genes (8-14%) compared to promoters (less than 1%) in all 3 cytosine contexts. Developmental DMCs showed a comparable pattern but only in the CG context and with a strong trend towards hypomethylation, particularly in the promoters. A high percentage of DMCs induced by developmental transitions were found memorized in genes (up to 45-50%) and promoters (up to 90%). In contrast, temperature-induced memory was lower and confined to genes after both embryonic (up to 14%) and post-embryonic development (up to 8%). Using stringent criteria, we identified ten genes involved in defense responses and adaptation, embryo development, and chromatin regulation that are candidates for the establishment of a persistent epigenetic memory of temperature sensed during embryo maturation in maritime pine. Here, we provide evidence that DNA methylation marks established during the embryonic phase are transmitted to the post-embryonic plant development phase.
{"title":"Epigenetic memory of temperature sensed during somatic embryo maturation in 2-year-old maritime pine trees","authors":"J -F Trontin, M D Sow, A Delaunay, I Modesto, C Teyssier, I Reymond, F Canlet, N Boizot, C Le Metté, A Gibert, C Chaparro, C Daviaud, J Tost, C Miguel, M -A Lelu-Walter, S Maury","doi":"10.1093/plphys/kiae600","DOIUrl":"https://doi.org/10.1093/plphys/kiae600","url":null,"abstract":"Embryogenesis is a brief but potentially critical phase in the tree life cycle for adaptive phenotypic plasticity. Using somatic embryogenesis in maritime pine (Pinus pinaster Ait.), we found that temperature during the maturation phase affects embryo development and post-embryonic tree growth for up to three years. We examined whether this somatic stress memory could stem from temperature- and/or development-induced changes in DNA methylation. For this, we developed a 200 Mb custom sequence capture bisulfite analysis of genes and promoters to identify differentially methylated cytosines (DMCs) between temperature treatments (18, 23, and 28°C) and developmental stages (immature and cotyledonary embryos, shoot apical meristem of 2-year-old plants) and investigate if these differences can be mitotically transmitted from embryonic to post-embryonic development (epigenetic memory). We revealed a high prevalence of temperature-induced DMCs in genes (8-14%) compared to promoters (less than 1%) in all 3 cytosine contexts. Developmental DMCs showed a comparable pattern but only in the CG context and with a strong trend towards hypomethylation, particularly in the promoters. A high percentage of DMCs induced by developmental transitions were found memorized in genes (up to 45-50%) and promoters (up to 90%). In contrast, temperature-induced memory was lower and confined to genes after both embryonic (up to 14%) and post-embryonic development (up to 8%). Using stringent criteria, we identified ten genes involved in defense responses and adaptation, embryo development, and chromatin regulation that are candidates for the establishment of a persistent epigenetic memory of temperature sensed during embryo maturation in maritime pine. Here, we provide evidence that DNA methylation marks established during the embryonic phase are transmitted to the post-embryonic plant development phase.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"62 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597608","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}
Liuyang Chu, Vivek Shrestha, Cay Christin Schäfer, Jan Niedens, George W Meyer, Zoe Darnell, Tyler Kling, Tobias Dürr-Mayer, Aleksej Abramov, Monika Frey, Henning Jessen, Gabriel Schaaf, Frank Hochholdinger, Agnieszka Nowak-Król, Paula McSteen, Ruthie Angelovici, Michaela S Matthes
Both deficiency and toxicity of the micronutrient boron lead to severe reductions in crop yield. Despite this agricultural importance, the molecular basis underlying boron homeostasis in plants remains unclear. To identify molecular players involved in boron homeostasis in maize (Zea mays L.), we measured boron levels in the Goodman-Buckler association panel and performed genome-wide association studies. These analyses identified a benzoxazinless (bx) gene, bx3, involved in the biosynthesis of benzoxazinoids, such as DIMBOA, which are major defense compounds in maize. Genes involved in DIMBOA biosynthesis are all located in close proximity in the genome, and benzoxazinoid biosynthesis mutants, including bx3, are all DIMBOA deficient. We determined that leaves of the bx3 mutant have a greater boron concentration than those of B73 control plants, which corresponded with enhanced leaf tip necrosis, a phenotype associated with boron toxicity. By contrast, other DIMBOA-deficient maize mutants did not show altered boron levels or the leaf tip necrosis phenotype, suggesting that boron is not associated with DIMBOA. Instead, our analyses suggest that the accumulation of boron is linked to the benzoxazinoid intermediates indolin-2-one (ION) and 3-hydroxy-ION. Therefore, our results connect boron homeostasis to the benzoxazinoid plant defense pathway through bx3 and specific intermediates, rendering the benzoxazinoid biosynthesis pathway a potential target for crop improvement under inadequate boron conditions.
{"title":"Association of the benzoxazinoid pathway with boron homeostasis in maize","authors":"Liuyang Chu, Vivek Shrestha, Cay Christin Schäfer, Jan Niedens, George W Meyer, Zoe Darnell, Tyler Kling, Tobias Dürr-Mayer, Aleksej Abramov, Monika Frey, Henning Jessen, Gabriel Schaaf, Frank Hochholdinger, Agnieszka Nowak-Król, Paula McSteen, Ruthie Angelovici, Michaela S Matthes","doi":"10.1093/plphys/kiae611","DOIUrl":"https://doi.org/10.1093/plphys/kiae611","url":null,"abstract":"Both deficiency and toxicity of the micronutrient boron lead to severe reductions in crop yield. Despite this agricultural importance, the molecular basis underlying boron homeostasis in plants remains unclear. To identify molecular players involved in boron homeostasis in maize (Zea mays L.), we measured boron levels in the Goodman-Buckler association panel and performed genome-wide association studies. These analyses identified a benzoxazinless (bx) gene, bx3, involved in the biosynthesis of benzoxazinoids, such as DIMBOA, which are major defense compounds in maize. Genes involved in DIMBOA biosynthesis are all located in close proximity in the genome, and benzoxazinoid biosynthesis mutants, including bx3, are all DIMBOA deficient. We determined that leaves of the bx3 mutant have a greater boron concentration than those of B73 control plants, which corresponded with enhanced leaf tip necrosis, a phenotype associated with boron toxicity. By contrast, other DIMBOA-deficient maize mutants did not show altered boron levels or the leaf tip necrosis phenotype, suggesting that boron is not associated with DIMBOA. Instead, our analyses suggest that the accumulation of boron is linked to the benzoxazinoid intermediates indolin-2-one (ION) and 3-hydroxy-ION. Therefore, our results connect boron homeostasis to the benzoxazinoid plant defense pathway through bx3 and specific intermediates, rendering the benzoxazinoid biosynthesis pathway a potential target for crop improvement under inadequate boron conditions.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"18 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597792","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}
Satish Namdeo Chavan, Eva Degroote, Karen De Kock, Kristof Demeestere, Tina Kyndt
Plants can transmit information to the next generation and modulate the phenotype of their offspring through epigenetic mechanisms. In this study, we demonstrate the activation of ‘intergenerational acquired resistance’ (IAR) in the progeny of rice (Oryza sativa) plants exogenously treated with dehydroascorbate (DHA). The offspring of lifelong DHA-treated plants (DHA-IAR) were significantly less susceptible to the root-knot nematode Meloidogyne graminicola and partially inherited the DHA-induced transcriptional response found in the parental plants. Phytohormone analyses on the DHA-IAR plants unveiled higher basal abscisic acid (ABA) levels and a primed induction of the jasmonic acid (JA) pathway. RNA-seq analysis on the embryonic tissues of immature seeds of DHA-treated plants revealed major shifts in the expression of genes associated with epigenetic pathways. We confirmed that DHA treatment leads to a significant but transient pattern of global DNA hypomethylation in the parental plants at 12 to 24 hours after treatment. The induction of resistance in the parental plants requires the DNA demethylase REPRESSOR OF SILENCING 1C (ROS1c) and ARGONAUTE 4 (AGO), suggesting a role for DNA demethylation and subsequent re-methylation in establishment of this phenotype. Confirming the transience of global hypomethylation upon DHA treatment, no significant change in global DNA methylation levels was observed in DHA-IAR versus naïve plants. Finally, DHA could not induce IAR in the Ros1c mutant line and in the ARGONAUTE 4 (ago4ab)-RNAi line. These data indicate that a controlled collaboration between transient DNA demethylation and remethylation underlies the induced resistance and IAR phenotypes upon DHA treatment.
植物可以通过表观遗传机制向下一代传递信息并调节其后代的表型。在这项研究中，我们证明了用脱氢抗坏血酸（DHA）外源处理的水稻（Oryza sativa）植株的后代激活了 "代际获得性抗性"（IAR）。终生接受 DHA 处理的植株的后代（DHA-IAR）对根结线虫 Meloidogyne graminicola 的易感性显著降低，并部分继承了亲本植株中发现的 DHA 诱导的转录反应。对DHA-IAR植株进行的植物激素分析揭示了较高的基础脱落酸（ABA）水平和茉莉酸（JA）途径的诱导。对 DHA 处理过的植物未成熟种子的胚胎组织进行的 RNA-seq 分析表明，与表观遗传途径相关的基因表达发生了重大变化。我们证实，DHA处理会导致亲本植物在处理后12至24小时内出现显著但短暂的全局DNA低甲基化模式。亲本植株的抗性诱导需要DNA去甲基化酶REPRESSOR OF SILENCING 1C (ROS1c) 和ARGONAUTE 4 (AGO)，这表明DNA去甲基化和随后的再甲基化在这一表型的建立中发挥作用。为了证实 DHA 处理后全局低甲基化的短暂性，在 DHA-IAR 与正常植株相比，没有观察到全局 DNA 甲基化水平的显著变化。最后，在 Ros1c 突变株系和 ARGONAUTE 4 (ago4ab)-RNAi 株系中，DHA 无法诱导 IAR。这些数据表明，瞬时 DNA 去甲基化和再甲基化之间的可控协作是 DHA 处理后诱导抗性和 IAR 表型的基础。
{"title":"ARGONAUTE4 and the DNA demethylase ROS1c mediate dehydroascorbate-induced intergenerational nematode resistance in rice","authors":"Satish Namdeo Chavan, Eva Degroote, Karen De Kock, Kristof Demeestere, Tina Kyndt","doi":"10.1093/plphys/kiae598","DOIUrl":"https://doi.org/10.1093/plphys/kiae598","url":null,"abstract":"Plants can transmit information to the next generation and modulate the phenotype of their offspring through epigenetic mechanisms. In this study, we demonstrate the activation of ‘intergenerational acquired resistance’ (IAR) in the progeny of rice (Oryza sativa) plants exogenously treated with dehydroascorbate (DHA). The offspring of lifelong DHA-treated plants (DHA-IAR) were significantly less susceptible to the root-knot nematode Meloidogyne graminicola and partially inherited the DHA-induced transcriptional response found in the parental plants. Phytohormone analyses on the DHA-IAR plants unveiled higher basal abscisic acid (ABA) levels and a primed induction of the jasmonic acid (JA) pathway. RNA-seq analysis on the embryonic tissues of immature seeds of DHA-treated plants revealed major shifts in the expression of genes associated with epigenetic pathways. We confirmed that DHA treatment leads to a significant but transient pattern of global DNA hypomethylation in the parental plants at 12 to 24 hours after treatment. The induction of resistance in the parental plants requires the DNA demethylase REPRESSOR OF SILENCING 1C (ROS1c) and ARGONAUTE 4 (AGO), suggesting a role for DNA demethylation and subsequent re-methylation in establishment of this phenotype. Confirming the transience of global hypomethylation upon DHA treatment, no significant change in global DNA methylation levels was observed in DHA-IAR versus naïve plants. Finally, DHA could not induce IAR in the Ros1c mutant line and in the ARGONAUTE 4 (ago4ab)-RNAi line. These data indicate that a controlled collaboration between transient DNA demethylation and remethylation underlies the induced resistance and IAR phenotypes upon DHA treatment.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"9 1","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-11-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597486","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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