Yukihisa Goto,Yasuhiro Kadota,Malick Mbengue,Jennifer D Lewis,Hidenori Matsui,Noriko Maki,Bruno Pok Man Ngou,Jan Sklenar,Paul Derbyshire,Arisa Shibata,Yasunori Ichihashi,David S Guttman,Hirofumi Nakagami,Takamasa Suzuki,Frank L H Menke,Silke Robatzek,Darrell Desveaux,Cyril Zipfel,Ken Shirasu
Plants detect pathogens using cell-surface pattern recognition receptors (PRRs) such as ELONGATION Factor-TU (EF-TU) RECEPTOR (EFR) and FLAGELLIN SENSING 2 (FLS2), which recognize bacterial EF-Tu and flagellin, respectively. These PRRs belong to the leucine-rich repeat receptor kinase (LRR-RK) family and activate the production of reactive oxygen species via the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD). The PRR-RBOHD complex is tightly regulated to prevent unwarranted or exaggerated immune responses. However, certain pathogen effectors can subvert these regulatory mechanisms, thereby suppressing plant immunity. To elucidate the intricate dynamics of the PRR-RBOHD complex, we conducted a comparative coimmunoprecipitation analysis using EFR, FLS2, and RBOHD in Arabidopsis thaliana. We identified QIAN SHOU KINASE 1 (QSK1), an LRR-RK, as a PRR-RBOHD complex-associated protein. QSK1 downregulated FLS2 and EFR abundance, functioning as a negative regulator of PRR-triggered immunity (PTI). QSK1 was targeted by the bacterial effector HopF2Pto, a mono-ADP ribosyltransferase, reducing FLS2 and EFR levels through both transcriptional and transcription-independent pathways, thereby inhibiting PTI. Furthermore, HopF2Pto transcriptionally downregulated PROSCOOP genes encoding important stress-regulated phytocytokines and their receptor MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2. Importantly, HopF2Pto requires QSK1 for its accumulation and virulence functions within plants. In summary, our results provide insights into the mechanism by which HopF2Pto employs QSK1 to desensitize plants to pathogen attack.
{"title":"The leucine-rich repeat receptor kinase QSK1 regulates PRR-RBOHD complexes targeted by the bacterial effector HopF2Pto.","authors":"Yukihisa Goto,Yasuhiro Kadota,Malick Mbengue,Jennifer D Lewis,Hidenori Matsui,Noriko Maki,Bruno Pok Man Ngou,Jan Sklenar,Paul Derbyshire,Arisa Shibata,Yasunori Ichihashi,David S Guttman,Hirofumi Nakagami,Takamasa Suzuki,Frank L H Menke,Silke Robatzek,Darrell Desveaux,Cyril Zipfel,Ken Shirasu","doi":"10.1093/plcell/koae267","DOIUrl":"https://doi.org/10.1093/plcell/koae267","url":null,"abstract":"Plants detect pathogens using cell-surface pattern recognition receptors (PRRs) such as ELONGATION Factor-TU (EF-TU) RECEPTOR (EFR) and FLAGELLIN SENSING 2 (FLS2), which recognize bacterial EF-Tu and flagellin, respectively. These PRRs belong to the leucine-rich repeat receptor kinase (LRR-RK) family and activate the production of reactive oxygen species via the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD). The PRR-RBOHD complex is tightly regulated to prevent unwarranted or exaggerated immune responses. However, certain pathogen effectors can subvert these regulatory mechanisms, thereby suppressing plant immunity. To elucidate the intricate dynamics of the PRR-RBOHD complex, we conducted a comparative coimmunoprecipitation analysis using EFR, FLS2, and RBOHD in Arabidopsis thaliana. We identified QIAN SHOU KINASE 1 (QSK1), an LRR-RK, as a PRR-RBOHD complex-associated protein. QSK1 downregulated FLS2 and EFR abundance, functioning as a negative regulator of PRR-triggered immunity (PTI). QSK1 was targeted by the bacterial effector HopF2Pto, a mono-ADP ribosyltransferase, reducing FLS2 and EFR levels through both transcriptional and transcription-independent pathways, thereby inhibiting PTI. Furthermore, HopF2Pto transcriptionally downregulated PROSCOOP genes encoding important stress-regulated phytocytokines and their receptor MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2. Importantly, HopF2Pto requires QSK1 for its accumulation and virulence functions within plants. In summary, our results provide insights into the mechanism by which HopF2Pto employs QSK1 to desensitize plants to pathogen attack.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142486312","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The banana (Musa spp.) peel undergoes rapid softening during ripening, leading to finger drop and a shortened shelf life. The regulatory mechanism behind this process remains to be elucidated. In this study, we confirmed the role of peel softening in banana finger drop and uncovered the underlying transcriptional regulatory network. Cell wall-related (CWR) genes were substantially upregulated in both the peel and finger drop zone during ethylene-induced ripening. Transcriptome analysis and genome-wide profiling of chromatin accessibility and transcription factor (TF) binding revealed that two key regulators of fruit ripening, Musa acuminata NAC-like, Activated by apetala3/Pistillata1 (MaNAP1) and MaMADS1, regulate CWR genes by directly binding to their promoters or by targeting other ripening-related TFs to form a hierarchical regulatory network. Notably, MaNAP1 and MaMADS1 were directly targeted by ETHYLENE INSENSITIVE3 (MaEIN3), and MaNAP1 and MaMADS1 associated with tissue-specific histone modifications, enabling them to integrate MaEIN3-mediated ethylene signaling and undergo epigenetic regulation. Overexpression of MaNAP1, MaMADS1 or other identified regulatory TFs upregulated CWR genes and promoted peel softening. Our findings unveil a MaNAP1-MaMADS1-centered regulatory cascade governing banana peel softening and finger drop, offering potential targets for enhancing banana texture and shelf life.
{"title":"The MaNAP1-MaMADS1 transcription factor module mediates ethylene-regulated peel softening and ripening in banana","authors":"Hua Li, Zhuo Chen, Wenjun Zhu, Xueting Ni, Junru Wang, Lufeng Fu, Jialin Chen, Tianpu Li, Lingxian Tang, Yingjie Yang, Fukun Zhang, Jiashui Wang, Biyan Zhou, Faxing Chen, Peitao Lü","doi":"10.1093/plcell/koae282","DOIUrl":"https://doi.org/10.1093/plcell/koae282","url":null,"abstract":"The banana (Musa spp.) peel undergoes rapid softening during ripening, leading to finger drop and a shortened shelf life. The regulatory mechanism behind this process remains to be elucidated. In this study, we confirmed the role of peel softening in banana finger drop and uncovered the underlying transcriptional regulatory network. Cell wall-related (CWR) genes were substantially upregulated in both the peel and finger drop zone during ethylene-induced ripening. Transcriptome analysis and genome-wide profiling of chromatin accessibility and transcription factor (TF) binding revealed that two key regulators of fruit ripening, Musa acuminata NAC-like, Activated by apetala3/Pistillata1 (MaNAP1) and MaMADS1, regulate CWR genes by directly binding to their promoters or by targeting other ripening-related TFs to form a hierarchical regulatory network. Notably, MaNAP1 and MaMADS1 were directly targeted by ETHYLENE INSENSITIVE3 (MaEIN3), and MaNAP1 and MaMADS1 associated with tissue-specific histone modifications, enabling them to integrate MaEIN3-mediated ethylene signaling and undergo epigenetic regulation. Overexpression of MaNAP1, MaMADS1 or other identified regulatory TFs upregulated CWR genes and promoted peel softening. Our findings unveil a MaNAP1-MaMADS1-centered regulatory cascade governing banana peel softening and finger drop, offering potential targets for enhancing banana texture and shelf life.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142448347","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plants bearing double flowers have long been cultivated as ornamental plants. Hose-in-hose flowers, bearing 2-whorled corolla tubes in whorls 1 and 2, are uncommon but recur in Sinningia (Gesnerioideae, Gesneriaceae). In this study, we selected 15 hose-in-hose cultivars as materials to explore the underlying molecular and genetic mechanisms of this floral architecture. We found that they originated from different hybridization events within the Dircaea clade. Three B-class MADS-box genes were globally expressed in all floral whorls, but only GLOBOSA1 (GLO1) has accumulated a dominant mutation, i.e., the insertion of a hAT-like miniature inverted-repeat transposable element (MITE) into its promoter, that co-segregated with the hose-in-hose phenotype. In addition, all 15 hose-in-hose cultivars contained the same dominant GLO1 allele. Transient gene expression assays confirmed the role of this MITE insertion in up-regulating the promoter activity of GLO1 by providing several cis-regulatory elements. Genetic transformation in heterologous Chirita pumila (Didymocarpoideae, Gesneriaceae) verified that this dominant GLO1 allele is sufficient to confer the hose-in-hose phenotype. We further demonstrated that both the GLO1 allele and the hAT-like MITE descended from wild S. cardinalis with single flowers. This study highlights the significance of wide hybridization in frequent gains of the dominant GLO1 allele and thereafter repeated occurrence of hose-in-hose flowers in Sinningia.
长期以来,重瓣花卉一直被作为观赏植物栽培。管中花在第 1 轮和第 2 轮中有 2 轮花冠筒,这种花并不常见,但在茜草科(Gesnerioideae,Gesneriaceae)中经常出现。在本研究中,我们选择了 15 个软管花栽培品种作为材料,以探索这种花结构的分子和遗传机制。我们发现,它们起源于 Dircaea 支系内不同的杂交事件。三个 B 级 MADS-box 基因在所有花轮中均有全局表达,但只有 GLOBOSA1(GLO1)积累了一个显性突变,即在其启动子中插入了一个类似 hAT 的微型倒位重复转座元件(MITE),该突变与软管花表型共存。此外,所有 15 个软管栽培品种都含有相同的显性 GLO1 等位基因。瞬时基因表达测定证实了 MITE 插入通过提供几个顺式调控元件在上调 GLO1 启动子活性方面的作用。在异源 Chirita pumila(Didymocarpoideae,Gesneriaceae)中进行的遗传转化验证了这一显性 GLO1 等位基因足以赋予软管中软管的表型。我们进一步证明,GLO1 等位基因和 hAT 样 MITE 都是从单花野生 S. cardinalis 传下来的。这项研究强调了广泛杂交在频繁获得显性 GLO1 等位基因以及此后在僧帽蕨(Sinningia)中反复出现软管花的过程中的重要性。
{"title":"A single dominant GLOBOSA allele accounts for repeated origins of hose-in-hose flowers in Sinningia (Gesneriaceae)","authors":"Xia Yang, Qi Liu, Miao-Miao Wang, Xiao-Ya Wang, Meng-Qi Han, Fang-Pu Liu, Tian-Feng Lü, Jing Liu, Yin-Zheng Wang","doi":"10.1093/plcell/koae283","DOIUrl":"https://doi.org/10.1093/plcell/koae283","url":null,"abstract":"Plants bearing double flowers have long been cultivated as ornamental plants. Hose-in-hose flowers, bearing 2-whorled corolla tubes in whorls 1 and 2, are uncommon but recur in Sinningia (Gesnerioideae, Gesneriaceae). In this study, we selected 15 hose-in-hose cultivars as materials to explore the underlying molecular and genetic mechanisms of this floral architecture. We found that they originated from different hybridization events within the Dircaea clade. Three B-class MADS-box genes were globally expressed in all floral whorls, but only GLOBOSA1 (GLO1) has accumulated a dominant mutation, i.e., the insertion of a hAT-like miniature inverted-repeat transposable element (MITE) into its promoter, that co-segregated with the hose-in-hose phenotype. In addition, all 15 hose-in-hose cultivars contained the same dominant GLO1 allele. Transient gene expression assays confirmed the role of this MITE insertion in up-regulating the promoter activity of GLO1 by providing several cis-regulatory elements. Genetic transformation in heterologous Chirita pumila (Didymocarpoideae, Gesneriaceae) verified that this dominant GLO1 allele is sufficient to confer the hose-in-hose phenotype. We further demonstrated that both the GLO1 allele and the hAT-like MITE descended from wild S. cardinalis with single flowers. This study highlights the significance of wide hybridization in frequent gains of the dominant GLO1 allele and thereafter repeated occurrence of hose-in-hose flowers in Sinningia.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142448086","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Small but mighty: OsKANADI1 and OsYABBY5 regulate plant stature by tuning GA metabolism in rice.","authors":"Christian Damian Lorenzo","doi":"10.1093/plcell/koae274","DOIUrl":"https://doi.org/10.1093/plcell/koae274","url":null,"abstract":"","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142447943","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Oxygenic photosynthesis generates the initial energy source that fuels nearly all life on Earth. At the heart of the process are the photosystems, which are pigment binding multi-protein complexes that catalyse the first step of photochemical conversion of light energy into chemical energy. Here, we investigate the molecular evolution of the plastid-encoded photosystem subunits at single-residue resolution across 773 angiosperm species. We show that despite an extremely high level of conservation, 7% of residues in the photosystems, spanning all photosystem subunits, exhibit hallmarks of adaptive evolution. Through in silico modelling of these adaptive substitutions, we uncover the impact of these changes on the predicted properties of the photosystems, focussing on their effects on co-factor binding and inter-subunit interface formation. By analyzing these cohorts of changes, we reveal that evolution has repeatedly altered the interaction between photosystem II and its D1 subunit in a manner that is predicted to reduce the energetic barrier for D1 turnover and photosystem repair. Together, these results provide insight into the trajectory of photosystem adaptation during angiosperm evolution.
{"title":"Widespread adaptive evolution in angiosperm photosystems provides insight into the evolution of photosystem II repair","authors":"Elizabeth H J Robbins, Steven Kelly","doi":"10.1093/plcell/koae281","DOIUrl":"https://doi.org/10.1093/plcell/koae281","url":null,"abstract":"Oxygenic photosynthesis generates the initial energy source that fuels nearly all life on Earth. At the heart of the process are the photosystems, which are pigment binding multi-protein complexes that catalyse the first step of photochemical conversion of light energy into chemical energy. Here, we investigate the molecular evolution of the plastid-encoded photosystem subunits at single-residue resolution across 773 angiosperm species. We show that despite an extremely high level of conservation, 7% of residues in the photosystems, spanning all photosystem subunits, exhibit hallmarks of adaptive evolution. Through in silico modelling of these adaptive substitutions, we uncover the impact of these changes on the predicted properties of the photosystems, focussing on their effects on co-factor binding and inter-subunit interface formation. By analyzing these cohorts of changes, we reveal that evolution has repeatedly altered the interaction between photosystem II and its D1 subunit in a manner that is predicted to reduce the energetic barrier for D1 turnover and photosystem repair. Together, these results provide insight into the trajectory of photosystem adaptation during angiosperm evolution.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142440183","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Anirban Baral, Delphine Gendre, Bibek Aryal, Louise Fougère, Luciano Martin Di Fino, Chihiro Ohori, Bernadette Sztojka, Tomohiro Uemura, Takashi Ueda, Peter Marhavý, Yohann Boutté, Rishikesh P Bhalerao
The trans-Golgi network (TGN), a key compartment in endomembrane trafficking, participates in both secretion to and endocytosis from the plasma membrane. Consequently, the TGN plays a key role in plant growth and development. Understanding how proteins are sorted for secretion or endocytic recycling at the TGN is critical for elucidating mechanisms of plant development. We previously showed that the protein ECHIDNA is essential for phytohormonal control of hypocotyl bending because it mediates secretion of cell wall components and the auxin influx carrier AUXIN RESISTANT 1 (AUX1) from the TGN. Despite the critical role of ECHIDNA in TGN-mediated trafficking, its mode of action remains unknown in Arabidopsis (Arabidopsis thaliana). We therefore performed a suppressor screen on the ech mutant. Here, we report the identification of TGN-localized TYPHON 1 (TPN1) and TPN2 proteins. A single amino acid change in either TPN protein causes dominant suppression of the ech mutant’s defects in growth and AUX1 secretion, while also restoring wild-type-like ethylene-responsive hypocotyl bending. Importantly, genetic and cell biological evidence shows that TPN1 acts through RAS-ASSOCIATED BINDING H1b (RABH1b), a TGN localized RAB-GTPase. These results provide insights into ECHIDNA-mediated secretory trafficking of cell wall and auxin carriers at the TGN, as well as its role in controlling plant growth.
{"title":"TYPHON proteins are RAB-dependent mediators of the trans-Golgi network secretory pathway","authors":"Anirban Baral, Delphine Gendre, Bibek Aryal, Louise Fougère, Luciano Martin Di Fino, Chihiro Ohori, Bernadette Sztojka, Tomohiro Uemura, Takashi Ueda, Peter Marhavý, Yohann Boutté, Rishikesh P Bhalerao","doi":"10.1093/plcell/koae280","DOIUrl":"https://doi.org/10.1093/plcell/koae280","url":null,"abstract":"The trans-Golgi network (TGN), a key compartment in endomembrane trafficking, participates in both secretion to and endocytosis from the plasma membrane. Consequently, the TGN plays a key role in plant growth and development. Understanding how proteins are sorted for secretion or endocytic recycling at the TGN is critical for elucidating mechanisms of plant development. We previously showed that the protein ECHIDNA is essential for phytohormonal control of hypocotyl bending because it mediates secretion of cell wall components and the auxin influx carrier AUXIN RESISTANT 1 (AUX1) from the TGN. Despite the critical role of ECHIDNA in TGN-mediated trafficking, its mode of action remains unknown in Arabidopsis (Arabidopsis thaliana). We therefore performed a suppressor screen on the ech mutant. Here, we report the identification of TGN-localized TYPHON 1 (TPN1) and TPN2 proteins. A single amino acid change in either TPN protein causes dominant suppression of the ech mutant’s defects in growth and AUX1 secretion, while also restoring wild-type-like ethylene-responsive hypocotyl bending. Importantly, genetic and cell biological evidence shows that TPN1 acts through RAS-ASSOCIATED BINDING H1b (RABH1b), a TGN localized RAB-GTPase. These results provide insights into ECHIDNA-mediated secretory trafficking of cell wall and auxin carriers at the TGN, as well as its role in controlling plant growth.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142440182","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Xingxiang Chen, Kui Liu, Tingting Luo, Baolei Zhang, Jinyu Yu, Dan Ma, Xiaoqian Sun, Huawei Zheng, Boning Xin, Jixing Xia
In response to variable environments, rice (Oryza sativa) roots have developed lignified and suberized diffusion barriers at the endodermis to permit selective nutrient uptake for optimal growth. Here, we demonstrate that endodermal suberization and non-localized lignification are redundantly regulated by four MYB transcription factors: OsMYB39a, OsMYB41, OsMYB92a, and OsMYB92b. These transcription factors function downstream of the OsMYB36a/b/c, CASPARIAN STRIP INTEGRITY FACTOR (OsCIF)–SCHENGEN3 (OsSGN3), and stress-inducible signaling pathways in rice. Knockout of all four MYB genes resulted in the complete absence of endodermal suberin lamellae (SL) and almost no lignin deposition between the Casparian strip and the cortex-facing lignified band at cell corners under all conditions examined. In contrast, endodermis-specific overexpression of any of these MYB genes was sufficient to induce strong endodermal suberization and non-localized lignification near the root tip. Furthermore, OsMYB92a-overexpressing lines showed an altered ionomic profile and enhanced salinity tolerance. Transcriptome analysis identified 152 downstream genes regulated by OsMYB39a/41/92a/92b, including the key SL formation gene OsCYP86A1 and other genes involved in endodermal lignification and suberization under normal and stress conditions. Our results provide important insights into the molecular mechanisms underlying suberization and non-localized lignification at the root endodermis and their physiological significance in ion homeostasis and acclimation to environmental stress.
{"title":"Four MYB transcription factors regulate suberization and non-localized lignification at the root endodermis in rice","authors":"Xingxiang Chen, Kui Liu, Tingting Luo, Baolei Zhang, Jinyu Yu, Dan Ma, Xiaoqian Sun, Huawei Zheng, Boning Xin, Jixing Xia","doi":"10.1093/plcell/koae278","DOIUrl":"https://doi.org/10.1093/plcell/koae278","url":null,"abstract":"In response to variable environments, rice (Oryza sativa) roots have developed lignified and suberized diffusion barriers at the endodermis to permit selective nutrient uptake for optimal growth. Here, we demonstrate that endodermal suberization and non-localized lignification are redundantly regulated by four MYB transcription factors: OsMYB39a, OsMYB41, OsMYB92a, and OsMYB92b. These transcription factors function downstream of the OsMYB36a/b/c, CASPARIAN STRIP INTEGRITY FACTOR (OsCIF)–SCHENGEN3 (OsSGN3), and stress-inducible signaling pathways in rice. Knockout of all four MYB genes resulted in the complete absence of endodermal suberin lamellae (SL) and almost no lignin deposition between the Casparian strip and the cortex-facing lignified band at cell corners under all conditions examined. In contrast, endodermis-specific overexpression of any of these MYB genes was sufficient to induce strong endodermal suberization and non-localized lignification near the root tip. Furthermore, OsMYB92a-overexpressing lines showed an altered ionomic profile and enhanced salinity tolerance. Transcriptome analysis identified 152 downstream genes regulated by OsMYB39a/41/92a/92b, including the key SL formation gene OsCYP86A1 and other genes involved in endodermal lignification and suberization under normal and stress conditions. Our results provide important insights into the molecular mechanisms underlying suberization and non-localized lignification at the root endodermis and their physiological significance in ion homeostasis and acclimation to environmental stress.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142440180","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Chuanfeng Ju, Laiba Javed, Yanjun Fang, Yuqing Zhao, Chenyu Cao, Yuan Deng, Yaqi Gao, Lv Sun, Cun Wang
Hydrotropism facilitates the orientation of plant roots towards regions of elevated water potential, enabling them to absorb adequate water. Although calcium signaling plays a crucial role in plant response to water tracking, the exact regulatory mechanisms remain a mystery. Here, we employed the Arabidopsis (Arabidopsis thaliana) hydrotropism-specific protein MIZU-KUSSEI1 (MIZ1) as bait and found that calcium-dependent protein kinases4/5/6/11 (CPK4/5/6/11) interacted with MIZ1 in vitro and in vivo. The cpk4/5/6/11 mutant exhibited increased sensitivity to water potential and enhanced root tip curvature. Furthermore, CPK4/5/6/11 primarily phosphorylated MIZ1 at Ser14/36 residues. Additionally, CPK-mediated phosphorylation of MIZ1 relieved its inhibitory effect on the activity of the endoplasmic reticulum–localized Ca2+ pump ECA1, altering the balance between cytoplasmic Ca2+ inflow and outflow, thereby negatively regulating the hydrotropic growth of plants. Overall, our findings unveil the molecular mechanisms by which the CPK4/5/6/11-MIZ1 module functions in regulating plant hydrotropism responses and provide a theoretical foundation for enhancing plant water use efficiency and promoting sustainable agriculture.
{"title":"Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE4/5/6/11 negatively regulate hydrotropism via phosphorylation of MIZU-KUSSEI1","authors":"Chuanfeng Ju, Laiba Javed, Yanjun Fang, Yuqing Zhao, Chenyu Cao, Yuan Deng, Yaqi Gao, Lv Sun, Cun Wang","doi":"10.1093/plcell/koae279","DOIUrl":"https://doi.org/10.1093/plcell/koae279","url":null,"abstract":"Hydrotropism facilitates the orientation of plant roots towards regions of elevated water potential, enabling them to absorb adequate water. Although calcium signaling plays a crucial role in plant response to water tracking, the exact regulatory mechanisms remain a mystery. Here, we employed the Arabidopsis (Arabidopsis thaliana) hydrotropism-specific protein MIZU-KUSSEI1 (MIZ1) as bait and found that calcium-dependent protein kinases4/5/6/11 (CPK4/5/6/11) interacted with MIZ1 in vitro and in vivo. The cpk4/5/6/11 mutant exhibited increased sensitivity to water potential and enhanced root tip curvature. Furthermore, CPK4/5/6/11 primarily phosphorylated MIZ1 at Ser14/36 residues. Additionally, CPK-mediated phosphorylation of MIZ1 relieved its inhibitory effect on the activity of the endoplasmic reticulum–localized Ca2+ pump ECA1, altering the balance between cytoplasmic Ca2+ inflow and outflow, thereby negatively regulating the hydrotropic growth of plants. Overall, our findings unveil the molecular mechanisms by which the CPK4/5/6/11-MIZ1 module functions in regulating plant hydrotropism responses and provide a theoretical foundation for enhancing plant water use efficiency and promoting sustainable agriculture.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142440181","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Herbivore-induced wounding can elicit a defense response in plants. However, whether plants possess a surveillance system capable of detecting herbivore threats and initiating preparatory defenses before wounding occurs remains unclear. In this study, we reveal that tomato (Solanum lycopersicum) trichomes can detect and respond to the mechanical stimuli generated by herbivores. Mechanical stimuli are preferentially perceived by long trichomes, and this mechanosensation is transduced via intra-trichome communication. This communication presumably involves calcium waves, and the transduced signals activate the jasmonic acid (JA) signaling pathway in short glandular trichomes, resulting in the upregulation of the Woolly (Wo)-SlMYC1 regulatory module for terpene biosynthesis. This induced defense mechanism provides plants with an early warning system against the threat of herbivore invasion. Our findings represent a perspective on the role of multicellular trichomes in plant defense and the underlying intra-trichome communication.
{"title":"Different multicellular trichome types coordinate herbivore mechanosensing and defense in tomato.","authors":"Chao Sun,JinBo Wei,XinYun Gu,MinLiang Wu,Meng Li,YiXi Liu,NingKai An,KeMeng Wu,ShaSha Wu,JunQing Wu,MeiZhi Xu,JiaChen Wu,YaLing Wang,DaiYin Chao,YouJun Zhang,Shuang Wu","doi":"10.1093/plcell/koae269","DOIUrl":"https://doi.org/10.1093/plcell/koae269","url":null,"abstract":"Herbivore-induced wounding can elicit a defense response in plants. However, whether plants possess a surveillance system capable of detecting herbivore threats and initiating preparatory defenses before wounding occurs remains unclear. In this study, we reveal that tomato (Solanum lycopersicum) trichomes can detect and respond to the mechanical stimuli generated by herbivores. Mechanical stimuli are preferentially perceived by long trichomes, and this mechanosensation is transduced via intra-trichome communication. This communication presumably involves calcium waves, and the transduced signals activate the jasmonic acid (JA) signaling pathway in short glandular trichomes, resulting in the upregulation of the Woolly (Wo)-SlMYC1 regulatory module for terpene biosynthesis. This induced defense mechanism provides plants with an early warning system against the threat of herbivore invasion. Our findings represent a perspective on the role of multicellular trichomes in plant defense and the underlying intra-trichome communication.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142439559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Minjae Kim, Gabriel Lemes Jorge, Moritz Aschern, Stéphan Cuiné, Marie Bertrand, Malika Mekhalfi, Jean-Luc Putaux, Jae-Seong Yang, Jay J Thelen, Fred Beisson, Gilles Peltier, Yonghua Li-Beisson
The cell wall of plants and algae is an important cell structure that protects cells from changes in the external physical and chemical environment. This extracellular matrix, composed of polysaccharides and glycoproteins, must be constantly remodeled throughout the life cycle. However, compared to matrix polysaccharides, little is known about the mechanisms regulating the formation and degradation of matrix glycoproteins. We report here that a plant kinase belonging to the DUAL-SPECIFICITY TYROSINE PHOSPHORYLATION-REGULATED KINASE (DYRK) family present in all eukaryotes regulates cell wall degradation after mitosis of Chlamydomonas reinhardtii by inducing the expression of matrix metalloproteinases (MMPs). Without the plant DYRK kinase (DYRKP1), daughter cells cannot disassemble parental cell walls and remain trapped inside for more than 10 days. On the other hand, the DYRKP1 complementation line shows normal degradation of the parental cell wall. Transcriptomic and proteomic analyses indicate a marked down-regulation of MMP gene expression and accumulation, respectively, in the dyrkp1 mutants. The mutants deficient in MMPs retain palmelloid structures for a longer time than the background strain, like dyrkp1 mutants. Our findings show that DYRKP1, by ensuring timely MMP expression, enables the successful execution of the cell cycle. Altogether, this study provides insight into the life cycle regulation in plants and algae.
{"title":"The DYRKP1 kinase regulates cell wall degradation in Chlamydomonas by inducing matrix metalloproteinase expression","authors":"Minjae Kim, Gabriel Lemes Jorge, Moritz Aschern, Stéphan Cuiné, Marie Bertrand, Malika Mekhalfi, Jean-Luc Putaux, Jae-Seong Yang, Jay J Thelen, Fred Beisson, Gilles Peltier, Yonghua Li-Beisson","doi":"10.1093/plcell/koae271","DOIUrl":"https://doi.org/10.1093/plcell/koae271","url":null,"abstract":"The cell wall of plants and algae is an important cell structure that protects cells from changes in the external physical and chemical environment. This extracellular matrix, composed of polysaccharides and glycoproteins, must be constantly remodeled throughout the life cycle. However, compared to matrix polysaccharides, little is known about the mechanisms regulating the formation and degradation of matrix glycoproteins. We report here that a plant kinase belonging to the DUAL-SPECIFICITY TYROSINE PHOSPHORYLATION-REGULATED KINASE (DYRK) family present in all eukaryotes regulates cell wall degradation after mitosis of Chlamydomonas reinhardtii by inducing the expression of matrix metalloproteinases (MMPs). Without the plant DYRK kinase (DYRKP1), daughter cells cannot disassemble parental cell walls and remain trapped inside for more than 10 days. On the other hand, the DYRKP1 complementation line shows normal degradation of the parental cell wall. Transcriptomic and proteomic analyses indicate a marked down-regulation of MMP gene expression and accumulation, respectively, in the dyrkp1 mutants. The mutants deficient in MMPs retain palmelloid structures for a longer time than the background strain, like dyrkp1 mutants. Our findings show that DYRKP1, by ensuring timely MMP expression, enables the successful execution of the cell cycle. Altogether, this study provides insight into the life cycle regulation in plants and algae.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142440203","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}