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AtVQ25 promotes salicylic acid-related leaf senescence by fine-tuning the self-repression of AtWRKY53

Journal of Integrative Plant Biology 2024年第6期66卷 1126-1147页

作者： Qi Tan Mingming Zhao Jingwei Gao Ke Li Mengwei Zhang Yunjia Li Zeting Liu Yujia Song Xiaoyue Lu Zhengge Zhu Rongcheng Lin Pengcheng Yin Chunjiang Zhou Geng Wang Ministry of Education Key Laboratory of Molecular and Cellular Biology Hebei Research Center of the Basic Discipline of Cell BiologyHebei Collaboration Innovation Center for Cell Signaling and Environmental Adaptation Hebei Key Laboratory of Molecular and Cellular Biology College of Life Sciences Hebei Normal University College of Chemical Engineering Shijiazhuang University Institute of Botany Chinese Academy of Sciences

Most mechanistic details of chronologically ordered regulation of leaf senescence are unknown.Regulatory networks centered on AtWRKY53 are crucial for orchestrating and integrating various senescence-related signals. Notably, AtWRKY53binds to its own promoter and represses transcription of AtWRKY53, but the biological significance and mechanism underlying this selfrepression remain unclear. In this study, we identified the VQ motif-containing protein AtVQ25as a cooperator of AtWRKY53. The expression level of AtVQ25 peaked at mature stage and was specifically repressed after the onset of leaf senescence. AtVQ25-overexpressing plants and atvq25 mutants displayed precocious and delayed leaf senescence, respectively. Importantly, we identified AtWRKY53 as an interacting partner of AtVQ25. We determined that interaction between AtVQ25 and AtWRKY53 prevented AtWRKY53from binding to W-box elements on the AtWRKY53promoter and thus counteracted the selfrepression of AtWRKY53. In addition, our RNA-sequencing data revealed that the AtVQ25-AtWRKY53 module is related to the salicylic acid(SA) pathway. Precocious leaf senescence and SA-induced leaf senescence in AtVQ25-overexpressing lines were inhibited by an SA pathway mutant, atsid2, and Nah G transgenic plants; AtVQ25-overexpressing/atwrky53 plants were also insensitive to SA-induced leaf senescence. Collectively, we demonstrated that AtVQ25 directly attenuates the self-repression of AtWRKY53 during the onset of leaf senescence,which is substantially helpful for understanding the timing of leaf senescence onset modulated by AtWRKY53.

关键词： AtWRKY53 leaf senescence salicylic acid transcriptional regulation VQ motif-containing proteins

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OsbZIP53 Negatively Regulates Immunity Response by Involving in Reactive Oxygen Species and salicylic acid Metabolism in Rice

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Rice science 2024年第2期31卷 190-202,I0022-I0028页

作者： WU Lijuan HAN Cong WANG Huimei HE Yuchang LIN Hai WANG Lei CHEN Chen E Zhiguo State Key Laboratory of Rice Biology and Breeding China National Rice Research InstituteHangzhou 310006China Jiangsu Key Laboratory of Crop Genetics and Physiology/Key Laboratory of Plant Functional Genomics of the Ministry of Education/Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops Agricultural College of Yangzhou UniversityYangzhou 225009China

The basic region/leucine zipper(bZIP)transcription factors play important roles in plant development and responses to abiotic and biotic stresses.OsbZIP53 regulates resistance to Magnaporthe oryzae in rice by analyzing APIP5-RNAi transgenic plants.To further investigate the biological functions of OsbZIP53,we generated osbzip53 mutants using CRISPR/Cas9 editing and also constructed OsbZIP53 over-expression transgenic plants.Comprehensive analysis of phenotypical,physiological,and transcriptional data showed that knocking-out OsbZIP53 not only improved disease resistance by inducing a hypersensitivity response in plants,but also regulated the immune response through the salicylic acid pathway.Specifically,disrupting OsbZIP53 increased H2O2 accumulation by promoting reactive oxygen species generation through up-regulation of several respiratory burst oxidase homologs(Osrboh genes)and weakened H2O2 degradation by directly targeting OsMYBS1.In addition,the growth of osbzip53 mutants was seriously impaired,while OsbZIP53 over-expression lines displayed a similar phenotype to the wild type,suggesting that OsbZIP53 has a balancing effect on rice immune response and growth.

关键词： OsbZIP53 hypersensitive response reactive oxygen species metabolism rice immunity salicylic acid transcription factor

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FaSnRK1a mediates salicylic acid pathways to enhance strawberry resistance to Botrytis cinerea

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Horticultural Plant Journal 2024年第1期10卷 131-144页

作者： Jingjing Luo Wenying Yu Yuansong Xiao Yafei Zhang Futian Peng State Key Laboratory of Crop Biology College of Horticulture Science and EngineeringShandong Agricultural UniversityTaianShandong 271018China

Strawberry is a major fruit crop worldwide because its nutritional and health benefits to human health,but its productivity is limited by Botrytis cinerea.Sucrose nonfermentation 1-related protein kinase 1(SnRK1)has a defense function against pathogens,but the function of SnRK1 in the defense response to B.cinerea in plants is still unclear.In this study,FaSnRK1a-OE and RNAi fruits were constructed and then inoculated with B.cinerea.The result reveals a positive role of Fa SnRK1a in the regulation of resistance to gray mold.FaSnRK1a affects SA content by regulating FaPAL1 and FaPAL2 expressions.The genes related to the SA signaling pathway(FaTGA1 and FaTGA2.1)were significantly increased/decreased in FaSnRK1a-OE or FaSnRK1a-RNAi fruit,respectively.FaSnRK1a interacted with the FaWRKY33.2 protein and negatively regulated FaWRKY33.2 expression,and FaWRKY33.2 acts as a repressor of disease resistance to B.cinerea.Finally,FaSnRK1a regulates the expression of six PR genes and the activities of antioxidant enzymes to boost defense response after B.cinerea inoculation.Our findings showed that FaSnRK1a increases the resistance of strawberry fruit to B.cinerea via SA signaling pathway and interaction with the FaWRKY33.2 transcription factor.

关键词： Strawberry B.cinerea SnRK1 salicylic acid WRKY transcription factor

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salicylic acid inhibits gibberellin signaling through receptor interactions

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Molecular Plant 2022年第11期15卷 1759-1771页

作者： Xiaodong Yu Xiaoyu Cui Chong Wu Shixi Shi Shunping Yan Hubei Hongshan Laboratory Wuhan 430070China College of Life Science and Technology Huazhong Agricultural UniversityWuhan 430070China Shenzhen Institute of Nutrition and Health Huazhong Agricultural UniversityShenzhen 518000China Shenzhen Branch Guangdong Laboratory for Lingnan Modern AgricultureShenzhen 518000China Agricultural Genomics Institute at Shenzhen Chinese Academy of Agricultural SciencesShenzhen 518000China

It is well known that plants activate defense responses at the cost of growth.However,the underlying molecular mechanisms are not well understood.The phytohormones salicylic acid(SA)and gibberellin(GA)promote defense response and growth,respectively.Here we show that SA inhibits GA signaling to repress plant growth.We found that the SA receptor NPR1 interacts with the GA receptor GID1.Further biochemical studies revealed that NPR1 functions as an adaptor of ubiquitin E3 ligase to promote the polyubiquitination and degradation of GID1,which enhances the stability of DELLA proteins,the negative regulators of GA signaling.Genetic analysis suggested that NPR1,GID1,and DELLA proteins are all required for the SA-mediated growth inhibition.Collectively,our study not only uncovers a novel regulatory mechanism of growth-defense trade-off but also reveals the interaction of hormone receptors as a new mode of hormonal crosstalk.

关键词： salicylic acid gibberellin trade-off receptor growth inhibition

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salicylic acid biosynthesis is not from phenylalanine in Arabidopsis

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Journal of Integrative Plant Biology 2023年第4期65卷 881-887页

作者： Jie Wu Wentao Zhu Qiao Zhao Shenzhen Key Laboratory of Synthetic Genomics Guangdong Provincial Key Laboratory of Synthetic GenomicsShenzhen Institute of Synthetic BiologyShenzhen Institute of Advanced Technologythe Chinese Academy of SciencesShenzhen 518055China Department of Applied Chemistry Innovation Center of Pesticide ResearchCollege of ScienceChina Agricultural UniversityBeijing 100193China Center for Plant Biology School of Life SciencesTsinghua UniversityBeijing 100084China

The phytohormone salicylic acid(SA)regulates biotic and abiotic stress responses in plants.Two distinct biosynthetic pathways for SA have been well documented in plants:the isochorismate(IC)pathway in the chloroplast and the phenylalanine ammonia-lyase(PAL)pathway in the cytosol.However,there has been no solid evidence that the PAL pathway contributes to SA biosynthesis.Here,we report that feeding Arabidopsis thaliana with Ring-13C-labeled phenylalanine(13C6-Phe)resulted in incorporation of the13C label not into SA,but into its isomer 4-hydroxybenzoic acid(4-HBA)instead.We obtained similar results when feeding13C6-Phe to the SA-deficient ics1 ics2 mutant and the SA-hyperaccumulating mutant s3h s5h.Notably,we detected13C6-SA when13C6-benzoic acid(BA)was provided,suggesting that SA can be synthesized from BA.Furthermore,despite the substantial accumulation of SA upon pathogen infection,we did not observe incorporation of13C label from Phe into SA.We also did not detect13C6-SA in PAL-overexpressing lines in the kfb01 kfb02 kfb39 kfb50 background after being fed13C6-Phe,although endogenous PAL levels were dramatically increased.Based on these combined results,we propose that SA biosynthesis is not from Phe in Arabidopsis.These results have important implications for our understanding of the SA biosynthetic pathway in land plants.

关键词： benzoic acid IC pathway isotopic labeling PAL pathway salicylic acid

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salicylic acid Application Mitigates Oxidative Damage and Improves the Growth Performance of Barley under Drought Stress

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Phyton-International Journal of Experimental Botany 2023年第5期92卷 1513-1537页

作者： Shah Mohammad Naimul Islam Niloy Paul Md.Mezanur Rahman Md.Ashraful Haque Md.Motiar Rohman Mohammad Golam Mostofa Institute of Biotechnology and Genetic Engineering Bangabandhu Sheikh Mujibur Rahman Agricultural UniversityGazipur1706Bangladesh Institute of Genomics for Crop Abiotic Stress Tolerance Department of Plant and Soil ScienceTexas Tech UniversityLubbock79409USA Plant Breeding Division Bangladesh Agricultural Research InstituteGazipur1701Bangladesh Department of Energy Plant Research Laboratory Michigan State UniversityEast Lansing48824USA

Drought is a severe environmental constraint,causing a significant reduction in crop productivity across the world.salicylic acid(SA)is an important plant growth regulator that helps plants cope with the adverse effects induced by various abiotic stresses.The current study investigated the potential effects of SA on drought tolerance efficacy in two barley(Hordeum vulgare)genotypes,namely BARI barley 5 and BARI barley 7.Ten-day-old barley seedlings were exposed to drought stress by maintaining 7.5%soil moisture content in the absence or presence of 0.5,1.0 and 1.5 mM SA.Drought exposure led to severe damage to both genotypes,as indicated by phenotypic aberrations and reduction of dry biomass.On the other hand,the application of SA to drought-stressed plants protected both barley genotypes from the adverse effects of drought,which was reflected in the improvement of phenotypes and biomass production.SA supplementation improved relative water content and proline levels in drought-stressed barley genotypes,indicating the osmotic adjustment functions of SA under water-deficit conditions.Drought stress induced the accumulation of reactive oxygen species(ROS),such as hydrogen peroxide(H2O2)and superoxide(O_(2)•^(−)),and the lipid peroxidation product malondialdehyde(MDA)in the leaves of barley plants.Exogenous supply of SA reduced oxidative damage by restricting the accumulation of ROS through the stimulation of the activities of key antioxidant enzymes,including superoxide dismutase(SOD),peroxidase(POD),catalase(CAT),ascorbate peroxidase(APX)and glutathione peroxidase(GPX).Among the three-applied concentrations of SA,0.5 mM SA exhibited better mitigating effects against drought stress considering the phenotypic performance and biochemical data.Furthermore,BARI barley 5 showed better performance under drought stress than BARI barley 7 in the presence of SA application.Collectively,our results suggest that SA played a crucial role in improving water status and antioxidant defense strategy to protect barley plants from t

关键词： Antioxidant defense barley drought stress plant growth reactive oxygen species salicylic acid

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UBP12/UBP13-mediated deubiquitination of salicylic acid receptor NPR3 suppresses plant immunity

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Molecular Plant 2023年第1期16卷 232-244页

作者： Yu Zhou Su-Hyun Park Nam-Hai Chua Temasek Life Sciences Laboratory National University of Singapore1 Research LinkSingapore 117604Singapore Disruptive&Sustainable Technologies for Agricultural Precision Singapore-MIT Alliance for Research and Technology1 CREATE WaySingapore 138602Singapore

salicylic acid(SA),a defense hormone produced after pathogen challenge,is critical for plant immunity.Arabidopsis NONEXPRESSER OF PR GENES 1(NPR1)and its paralogs NPR3 and NPR4 can bind SA and mediate SA signal transduction.NPR1 functions as a transcriptional co-activator to promote defense gene expression,whereas NPR3 and NPR4 have been shown to function as negative regulators in the SA signaling pathway.Although the mechanism about NPR1 regulation has been well studied,how NPR3/NPR4 proteins are regulated in immune responses remains largely unknown.Here,we show that the stability of NPR3/NPR4 is enhanced by SA.In the absence of pathogen challenge,NPR3/NPR4 are unstable and degraded by the 26S proteasome,whereas the increase in cellular SA levels upon pathogen infection suppresses NPR3/NPR4 degradation.We found that UBP12 and UBP13,two homologous deubiquitinases from a ubiquitin-specific protease subfamily,negatively regulate plant immunity by promoting NPR3/NPR4 stability.Our genetic results further showed that UBP12/UBP13-mediated immunity suppression is partially dependent on NPR3/NPR4 functions.By interacting with NPR3 in the nucleus in an SA-dependent manner,UBP12 and UBP13 remove ubiquitin from polyubiquitinated NPR3 to protect it from being degraded.The stabilization of NPR3/NPR4 promoted by UBP12/UBP13 is essential for negative regulation of basal and SA-induced immunity.

关键词： plant immunity salicylic acid NPR3 UBP12/UBP13

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The origin and evolution of salicylic acid signaling and biosynthesis in plants

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Molecular Plant 2023年第1期16卷 245-259页

作者： Xianqing Jia Long Wang Hongyu Zhao Yibo Zhang Zhixiang Chen Lei Xu Keke Yi Key Laboratory of Plant Nutrition and Fertilizer Ministry of Agriculture and Rural AffairsInstitute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijing 100081China Department of Botany and Plant Pathology Center for Plant BiologyPurdue UniversityWest LafayetteIN 47907-2054USA

salicylic acid(SA)plays a pivotal role in plant response to biotic and abiotic stress.Several core SA signaling regulators and key proteins in SA biosynthesis have been well characterized.However,much remains unknown about the origin,evolution,and early diversification of core elements in plant SA signaling and biosynthesis.In this study,we identified 10 core protein families in SA signaling and biosynthesis across green plant lineages.We found that the key SA signaling receptors,the nonexpresser of pathogenesis-related(NPR)proteins,originated in the most recent common ancestor(MRCA)of land plants and formed divergent groups in the ancestor of seed plants.However,key transcription factors for SA signaling,TGACG motif-binding proteins(TGAs),originated in the MRCA of streptophytes,arguing for the stepwise evolution of core SA signaling in plants.Different from the assembly of the core SA signaling pathway in the ancestor of seed plants,SA exists extensively in green plants,including chlorophytes and streptophyte algae.However,the full isochorismate synthase(ICS)-based SA synthesis pathway was first assembled in the MRCA of land plants.We further revealed that the ancient abnormal inflorescence meristem 1(AIM1)-basedβ-oxidation pathway is crucial for the biosynthesis of SA in chlorophyte algae,and this biosynthesis pathway may have facilitated the adaptation of early-diverging green algae to the high-light-intensity environment on land.Taken together,our findings provide significant insights into the early evolution and diversification of plant SA signaling and biosynthesis pathways,highlighting a crucial role of SA in stress tolerance during plant terrestrialization.

关键词： salicylic acid SA signaling SA biosynthesis plant evolution high irradiance

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Brassinosteroids enhance salicylic acid-mediated immune responses by inhibiting BIN2 phosphorylation of clade I TGA transcription factors in Arabidopsis

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Molecular Plant 2022年第6期15卷 991-1007页

作者： Yeong-Woo Kim Ji-Hyun Youn Jeehee Roh Jeong-Mok Kim Seong-Ki Kim Tae-Wuk Kim Department of Life Science Hanyang UniversitySeoul 04763Republic of Korea Department of Life Science Chung-Ang UniversitySeoul 06973Republic of Korea Research Institute for Convergence of Basic Science Hanyang UniversitySeoul 04763Republic of Korea Hanyang Institute of Bioscience and Biotechnology Hanyang UniversitySeoul 04763Republic of Korea

salicylic acid (SA) plays an important role in plant immune response, including resistance to pathogens and systemic acquired resistance. Two major components, NONEXPRESSOR OF PATHOGENESIS-RELATED GENES (NPRs) and TGACG motif-binding transcription factors (TGAs), are known to mediate SA signaling, which might also be orchestrated by other hormonal and environmental changes. Nevertheless, the molecular and functional interactions between SA signaling components and other cellular signaling pathways remain poorly understood. Here we showed that the steroid plant hormone brassinosteroid (BR) promotes SA responses by inactivating BR-INSENSITIVE 2 (BIN2), which inhibits the redox-sensitive clade I TGAs in Arabidopsis. We found that both BR and the BIN2 inhibitor bikinin synergistically increase SA-mediated physiological responses, such as resistance to Pst DC3000. Our genetic and biochemical analyses indicated that BIN2 functionally interacts with TGA1 and TGA4, but not with other TGAs. We further demonstrated that BIN2 phosphorylates Ser-202 of TGA4, resulting in the suppression of the redox-dependent interaction between TGA4 and NPR1 as well as destabilization of TGA4. Consistently, transgenic Arabidopsis overexpressing TGA4-YFP with a S202A mutation displayed enhanced SA responses compared to the wild-type TGA4-YFP plants. Taken together, these results suggest a novel crosstalk mechanism by which BR signaling coordinates the SA responses mediated by redox-sensitive clade I TGAs.

关键词： brassinosteroid salicylic acid immune responses BIN2 clade I TGA

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Preparation and MRI performances of core-shell structural PEG salicylic acid-gadolinium composite nanoparticles

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Journal of Rare Earths 2022年第7期40卷 1098-1105页

作者： Jia Zhang Zhiyan Lin Minzhi Zhao Weibing Xu Fang Nian College of Science Gansu Agricultural UniversityLanzhou 730000China Clinical Medical College Gansu University of Chinese MedicineLanzhou 730000China

Gadolinium(Ⅲ)-based T_(1) contrast agents have been widely used in clinical MRI.In this study,salicylic acid-gadolinium chelate was prepared via directly coordination reaction of gadolinium ion and salicylic acid.Then,three polyethylene glycols with different molecular weight were modified on the surface of salicylic acid-gadolinium by simple chemical coupling to construct three core-shell structural Gd based composites.The scanning electron microscopy(SEM)and transmission electron microscopy(TEM)characterization results show that the composite is a spherical particle with a diameter of about 100-200 nm.The longitudinal relaxation rate r_(1) of the Gal-PEG-2000 is 11.097(mmol/L)^(-1)/s,and the ratio of r_(2)/r_(1) is as low as 2.53.The composite shows good liver and intestines MRI performances after being used in in vivo imaging,showing a good prospect of biological application.

关键词： Gadolinium salicylic acid Polyethylene glycols Core-shell structural MRI contrast agent Rare earths

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