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Nitric oxide-mediated S-nitrosylation of IAA17 protein in intrinsically disordered region represses Auxin signaling

Journal of Genetics and Genomics 2023年第7期50卷 473-485页

作者： Hongwei Jing Xiaolu Yang Ryan J.Emenecker Jian Feng Jian Zhang Marcelo Rodrigues Alves de Figueiredo Patarasuda Chaisupa R.Clay Wright Alex S.Holehouse Lucia C.Strader Jianru Zuo State Key Laboratory of Plant Genomics Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijing 100101China University of Chinese Academy of Sciences Beijing 100049China Department of Biology Duke UniversityDurhamNC 27008USA Department of Neurobiology Duke University Medical CenterDurhamNC 27710USA Department of Biochemistry and Molecular Biophysics Washington University School of MedicineSt.LouisMO 63110USA Center for Biomolecular Condensates(CBC) Washington University in St.LouisSt.LouisMO 63130USA Department of Biological Systems Engineering Virginia TechBlacksburgVA 24061USA The Translational Plant Sciences Center(TPSC) Virginia TechBlacksburgVA 24061USA CAS Center for Excellence in Molecular Plant Sciences Chinese Academy of SciencesBeijing 100101China

The phytohormone Auxin plays crucial roles in nearly every aspect of plant growth and development.Auxin signaling is activated through the phytohormone-induced proteasomal degradation of the Auxin/INDOLE-3-ACETIC ACID(Aux/IAA)family of transcriptional repressors.Notably,many Auxin-modulated physiological processes are also regulated by nitric oxide(NO)that executes its biological effects predominantly through protein S-nitrosylation at specific cysteine residues.However,little is known about the molecular mechanisms in regulating the interactive NO and Auxin networks.Here,we show that NO represses Auxin signaling by inhibiting IAA17 protein degradation.NO induces the S-nitrosylation of Cys-70 located in the intrinsically disordered region of IAA17,which inhibits the TIR1-IAA17 interaction and consequently the proteasomal degradation of IAA17.The accumulation of a higher level of IAA17 attenuates Auxin response.Moreover,an IAA17^(C70W)nitrosomimetic mutation renders the accumulation of a higher level of the mutated protein,thereby causing partial resistance to Auxin and defective lateral root development.Taken together,these results suggest that S-nitrosylation of IAA17 at Cys-70 inhibits its interaction with TIR1,thereby negatively regulating Auxin signaling.This study provides unique molecular insights into the redox-based Auxin signaling in regulating plant growth and development.

关键词： Arabidopsis thaliana Auxin Aux/IAA Nitric oxide S-nitrosylation Intrinsically disordered region

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High Auxin stimulates callus through SDG8-mediated histone H3K36 methylation in Arabidopsis

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Journal of Integrative Plant Biology 2022年第12期64卷 2425-2437页

作者： Jun Ma Qiang Li Lei Zhang Sen Cai Yuanyuan Liu Juncheng Lin Rongfeng Huang Yongqiang Yu Mingzhang Wen Tongda Xu College of Life Sciences Fujian Agriculture and Forestry UniversityFuzhou 350002China Plant Synthetic Biology Center FAFU-UCR Joint Center for Horticultural Biology and MetabolomicsHaixia Institute of Science and TechnologyFujian Agriculture and Forestry UniversityFuzhou 350002China Shanghai Center for Plant Stress Biology CAS Center for Excellence in Molecular Plant SciencesChinese Academy of SciencesShanghai 201602China Basic Forestry and Proteomics Research Center Haixia Institute of Science and TechnologyFujian Agricuture and Forestry UniversityFuzhou 350002China Frontiers Science Center for Synthetic Biology(Ministry of Education) Tianin UniversityTianjin 300072China

Callus induction,which results in fate transition in plant cells,is considered as the first and key step for plant regeneration.This process can be stimulated in different tissues by a callus-inducing medium(CIM),which contains a high concentration of phytohormone Auxin.Although a few key regulators for callus induction have been identified,the multiple aspects of the regulatory mechanism driven by high levels of Auxin still need further investigation.Here,we find that high Auxin induces callus through a H3 K36 histone methylation-dependent mechanism,which requires the methyltransferase SET DOMAIN GROUP 8(SDG8).During callus induction,the increased Auxin accumulates SDG8 expression through a TIR1/AFBs-based transcriptional regulation.SDG8 then deposits H3 K36 me3 modifications on the loci of callus-related genes,including a master regulator WOX5 and the cell proliferation-related genes,such as CYCB1.1.This epigenetic regulation in turn is required for the transcriptional activation of these genes during callus formation.These findings suggest that the massive transcriptional reprogramming for cell fate transition by Auxin during callus formation requires epigenetic modifications including SDG8-mediated histone H3 K36 methylation.Our results provide insight into the coordination between Auxin signaling and epigenetic regulation during fundamental processes in plant development.

关键词： Auxin callus formation epigenetic regulation H3K36 methylation SDG8 TIR1/AFBs

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Protein post-translational modifications in Auxin signaling

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Journal of Genetics and Genomics 2024年第3期51卷 279-291页

作者： Xiankui Cui Junxia Wang Ke Li Bingsheng Lv Bingkai Hou Zhaojun Ding The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdaoShandong 266237China Shandong Academy of Grape JinanShandong 250100China College of Horticulture Qingdao Agricultural UniversityQingdaoShandong 266109China

Protein post-translational modifications(PTMs),such as ubiquitination,phosphorylation,and small ubiquitin-like modifier(SUMO)ylation,are crucial for regulating protein stability,activity,subcellular localization,and binding with cofactors.Such modifications remarkably increase the variety and complexity of proteomes,which are essential for regulating numerous cellular and physiological processes.The regulation of Auxin signaling is finely tuned in time and space to guide various plant growth and development.Accumulating evidence indicates that PTMs play critical roles in Auxin signaling regulations.Thus,a thorough and systematic review of the functions of PTMs in Auxin signal transduction will improve our profound comprehension of the regulation mechanism of Auxin signaling and Auxin-mediated various processes.This review discusses the progress of protein ubiquitination,phosphorylation,histone acetylation and methylation,SUMOylation,and S-nitrosylation in the regulation of Auxin signaling.

关键词： Arabidopsis thaliana Auxin Auxin signaling Post-translational modifications Protein regulation

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GmPIN1-mediated Auxin asymmetry regulates leaf petiole angle and plant architecture in soybean

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Journal of Integrative Plant Biology 2022年第7期64卷 1325-1338页

作者： Zhongqin Zhang Le Gao Meiyu Ke Zhen Gao Tianli Tu Laimei Huang Jiaomei Chen Yuefeng Guan Xi Huang Xu Chen Key Laboratory of Ministry of Education for Genetics Breeding and Multiple Utilization of CropsCollege of AgricultureFujian Agriculture and Forestry UniversityFuzhou 350002China Haixia Institute of Science and Technology Horticultural Plant Biology and Metabolomics CenterFujian Agriculture and Forestry UniversityFuzhou 350002China Department of Horticulture Beijing Vocational College of AgricultureBeijing 102442China College of Life Science Fujian Agriculture and Forestry UniversityFuzhou 350002China State Key Laboratory of Cellular Stress Biology School of Life SciencesXiamen UniversityXiamen 361102China

Crop breeding during the Green Revolution resulted in high yields largely due to the creation of plants with semi-dwarf architectures that could tolerate high-density planting.Although semi-dwarf varieties have been developed in rice,wheat and maize,none was reported in soybean(Glycine max),and few genes controlling plant architecture have been characterized in soybean.Here,we demonstrate that the Auxin efflux transporter PINFORMED1(GmPIN1),which determines polar Auxin transport,regulates the leaf petiole angle in soybean.CRISPR-Cas9-induced Gmpin1abc and Gmpin1bc multiple mutants displayed a compact architecture with a smaller petiole angle than wildtype plants.GmPIN1 transcripts and Auxin were distributed asymmetrically in the petiole base,with high levels of GmPIN1a/c transcript and Auxin in the lower cells,which resulted in asymmetric cell expansion.By contrast,the(iso)flavonoid content was greater in the upper petiole cells than in the lower cells.Our results suggest that(iso)flavonoids inhibit GmPIN1a/c expression to regulate the petiole angle.Overall,our study demonstrates that a signal cascade that integrates(iso)flavonoid biosynthesis,GmPIN1a/c expression,Auxin accumulation,and cell expansion in an asymmetric manner creates a desirable petiole curvature in soybean.This study provides a genetic resource for improving soybean plant architecture.

关键词： Auxin flavonoid GmPIN1 peangle angle soybean

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A feedback regulation between ARF7-mediated Auxin signaling and Auxin homeostasis involving MES17 affects plant gravitropism

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Journal of Integrative Plant Biology 2022年第7期64卷 1339-1351页

作者： Feng Zhang Cuiling Li Xingzhen Qu Jiajia Liu Zipeng Yu Junxia Wang Jiayong Zhu Yongqiang Yu Zhaojun Ding The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationCollege of Life SciencesShandong UniversityQingdao 266237China Horticulture Biology and Metabolomics Center Haixia Institute of Science and TechnologyFujian Agriculture and Forestry UniversityFuzhou 350002China

Gravitropism is an essential adaptive response of land plants.Asymmetric Auxin gradients across plant organs,interpreted by multiple Auxin signaling components including Auxin RESPONSE FACTOR7(ARF7),trigger differential growth and bending response.However,how this fundamental process is strictly maintained in nature remains unclear.Here,we report that gravity stimulates the transcription of METHYL ESTERASE17(MES17)along the lower side of the hypocotyl via ARF7-dependent Auxin signaling.The asymmetric distribution of MES17,a methyltransferase that converts Auxin from its inactive form methyl indole-3-acetic acid ester(MeI AA)to its biologically active form free-IAA,enhanced the gradient of active Auxin across the hypocotyl,which in turn reversely amplified the asymmetric Auxin responses and differential growth that shape gravitropic bending.Taken together,our findings reveal the novel role of MES17-mediated Auxin homeostasis in gravitropic responses and identify an ARF7-triggered feedback mechanism that reinforces the asymmetric distribution of active Auxin and strictly controls gravitropism in plants.

关键词： ARF7 Auxin gravitropism homeostasis MES17

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SlBEL11 regulates flavonoid biosynthesis,thus fine-tuning Auxin efflux to prevent premature fruit drop in tomato

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Journal of Integrative Plant Biology 2024年第4期66卷 749-770页

作者： Xiufen Dong Xianfeng Liu Lina Cheng Ruizhen Li Siqi Ge Sai Wang Yue Cai Yang Liu Sida Meng Cai-Zhong Jiang Chun-Lin Shi Tianlai Li Daqi Fu Mingfang Qi Tao Xu College of Horticulture Shenyang Agricultural UniversityShenyang 110866China Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang Province College of Horticulture ScienceZhejiang A&F UniversityHangzhou 311300China Key Laboratory for Quality and Safety Control of Subtropical Fruits and Vegetables Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang ProvinceMinistry of Agriculture and Rural AffairsCollege of Horticulture ScienceZhejiang A&F UniversityHangzhou 311300China Key Laboratory of Protected Horticulture of Ministry of Education Shenyang 110866China Crops Pathology and Genetic Research Unit United States Department of Agriculture Agricultural Research ServiceWashingtonDC 20250USA Department of Plant Sciences University of CaliforniaDavisCA 95616USA ANGENOVO Oslo 0753Norway Laboratory of Fruit Biology College of Food Science and Nutritional EngineeringChina Agricultural UniversityBeijing 100083China

Auxin regulates flower and fruit abscission,but how developmental signals mediate Auxin transport in abscission remains unclear.Here,we reveal the role of the transcription factor BEL1-LIKE HOMEODOMAIN11(SlBEL11)in regulating Auxin transport during abscission in tomato(Solanum lycopersicum).SlBEL11 is highly expressed in the fruit abscission zone,and its expression increases during fruit development.Knockdown of SlBEL11 expression by RNA interference(RNAi)caused premature fruit drop at the breaker(Br)and 3d post-breaker(Br+3)stages of fruit development.Transcriptome and metabolome analysis of SlBEL11-RNAi lines revealed impaired flavonoid biosynthesis and decreased levels of most flavonoids,especially quercetin,which functions as an Auxin transport inhibitor.This suggested that SlBEL11 prevents premature fruit abscission by modulating Auxin efflux from fruits,which is crucial for the formation of an Auxin response gradient.Indeed,quercetin treatment suppressed premature fruit drop in SlBEL11-RNAi plants.DNA affinity purification sequencing(DAP-seq)analysis indicated that SlBEL11 induced expression of the transcription factor gene SlMYB111 by directly binding to its promoter.Chromatin immunoprecipitation-quantitative polymerase chain reaction and electrophoretic mobility shift assay showed that S.lycopersicum MYELOBLASTOSIS VIRAL ONCOGENE HOMOLOG111(SlMYB111)induces the expression of the core flavonoid biosynthesis genes SlCHS1,SlCHI,SlF3H,and SlFLS by directly binding to their promoters.Our findings suggest that the SlBEL11-SlMYB111 module modulates flavonoid biosynthesis to fine-tune Auxin efflux from fruits and thus maintain an Auxin response gradient in the pedicel,thereby preventing premature fruit drop.

关键词： abscission Auxin flavonoid SlBEL11 tomato

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Transmembrane kinase 1-mediated Auxin signal regulates membrane-associated clathrin in Arabidopsis roots

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Journal of Integrative Plant Biology 2023年第1期65卷 82-99页

作者： Yutong Wang Xu Yan Mei Xu Weiyang Qi Chunjie Shi Xiaohong Li Jiaqi Ma Dan Tian Jianxin Shou Haijun Wu Jianwei Pan Bo Li Chao Wang Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations School of Life Sciences Lanzhou UniversityLanzhou 730000 China College of Life Sciences Shaoxing University Shaoxing 312000 China

Clathrin-mediated endocytosis(CME)is the major endocytic pathway in eukaryotic cells that directly regulates abundance of plasma membrane proteins.Clathrin triskelia are composed of clathrin heavy chains(CHCs)and light chains(CLCs),and the phytohormone Auxin differentially regulates membraneassociated CLCs and CHCs,modulating the endocytosis and therefore the distribution of Auxin efflux transporter PIN-FORMED2(PIN2).However,the molecular mechanisms by which Auxin regulates clathrin are still poorly understood.Transmembrane kinase(TMKs)family proteins are considered to contribute to Auxin signaling and plant development;it remains unclear whether they are involved in PIN transport by CME.We assessed TMKs involvement in the regulation of clathrin by Auxin,using genetic,pharmacological,and cytological approaches including live-cell imaging and immunofluorescence.In tmk1 mutant seedlings,Auxin failed to rapidly regulate abundance of both CHC and CLC and to inhibit PIN2 endocytosis,leading to an impaired asymmetric distribution of PIN2 and therefore Auxin.Furthermore,TMK3 and TMK4 were shown not to be involved in regulation of clathrin by Auxin.In summary,TMK1 is essential for Auxin-regulated clathrin recruitment and CME.TMK1therefore plays a critical role in the establishment of an asymmetric distribution of PIN2 and an Auxin gradient during root gravitropism.

关键词： Arabidopsis Auxin clathrin endocytosis PIN2 transmembrane kinase1(TMK1)

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The SlTPL3–SlWUS module regulates multi-locule formation in tomato by modulating Auxin and gibberellin levels in the shoot apical meristem

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Journal of Integrative Plant Biology 2022年第11期64卷 2150-2167页

作者： Shiwei Song Binbin Huang Zanlin Pan Qiuxiang Zhong Yinghua Yang Da Chen Lisha Zhu Guojian Hu Mi He Caiyu Wu Mohammed Zouine Riyuan Chen Mondher Bouzayen Yanwei Hao Key Laboratory of Horticultural Crop Biology and Germplasm Innovation in South China Ministry of AgricultureCollege of HorticultureSouth China Agricultural UniversityGuangzhou 510642China Laboratory of Genomics and Biotechnology of Fruits INRAToulouse INPUniversity of ToulouseCastanet Tolosan F‐31326France

Malformed fruits depreciate a plant’s market value.In tomato(Solanum lycopersicum),fruit malformation is associated with the multi-locule trait,which involves genes regulating shoot apical meristem(SAM)development.The expression pattern of TOPLESS3(SITPL3)throughout SAM development prompted us to investigate its functional significance via RNA interference(RNAi)and clustered regularly interspaced short palindromic repeats/CRISPR-associated nuclease 9(Cas9)-mediated gene editing.Lower SITPL3 transcript levels resulted in larger fruits with more locules and larger SAMs at the 5 d after germination(DAG5)stage.Differentially expressed genes in the SAM of wild-type(WT)and SITPL3-RNAi plants,identified by transcriptome deep sequencing(RNA-seq),were enriched in the gibberellin(GA)biosynthesis and plant hormone signaling pathways.Moreover,exogenous Auxin and paclobutrazol treatments rescued the multi-locule phenotype,indicating that SITPL3 affects SAM size by mediating Auxin and GA levels in the SAM.Furthermore,SITPL3 interacted with WUSCHEL(SIWUS),which plays an important role in SAM size maintenance.We conducted RNA-seq and DNA affinity purification followed by sequencing(DAP-seq)analyses to identify the genes regulated by SITPL3 and SIWUS in the SAM and to determine how they regulate SAM size.We detected24 overlapping genes regulated by SITPL3 and SIWUS and harboring an SIWUS-binding motif in their promoters.Furthermore,functional annotation revealed a notable enrichment for functions in Auxin transport,Auxin signal transduction,and GA biosynthesis.Dual-luciferase assays also revealed that SITPL3 enhances SIWUS-mediated regulation(repression and activation)of SIPIN3 and SIGA2 ox4 transcription,indicating that the SITPL3-SIWUS module regulates SAM size by mediating Auxin distribution and GA levels,and perturbations of this module result in enlarged SAM.These results provide novel insights into the molecular mechanism of SAM maintenance and locule formation in tomato and highlight the SITPL3-SIWUS module as a key regula

关键词： Auxin gibberellin locule number shoot apical meristem(SAM) TOPLESS3(Sl TPL3)

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The unconventional prefoldin RPB5 interactor mediates the gravitropic response by modulating cytoskeleton organization and Auxin transport in Arabidopsis

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Journal of Integrative Plant Biology 2022年第10期64卷 1916-1934页

作者： Yi Yang Fang Liu Le Liu Mingyue Zhu Jinfeng Yuan Yan‐Xia Mai Jun‐Jie Zou Jie Le Yonghong Wang Klaus Palme Xugang Li Yong Wang Long Wang State Key Laboratory of Crop Biology College of Life SciencesShandong Agricultural UniversityDaizong Street 61Tai'an 271018China Shandong Provincial Key Laboratory of Biophysics Institute of BiophysicsDezhou UniversityDezhou 253023China Sino‐German Joint Research Center on Agricultural Biology College of Life SciencesShandong Agricultural UniversityDaizong Street 61Tai'an 271018China Faculty of Biology Institute of Biology II/Molecular Plant PhysiologyAlbert‐Ludwigs‐University of FreiburgSchänzlestrasse 1Freiburg D‐79104Germany National Key Laboratory of Plant Molecular Genetics(NKLPMG) CAS Center for Excellence in Molecular Plant SciencesInstitute of Plant Physiology and Ecology(SIPPE)Chinese Academy of Sciences(CAS)Shanghai 200032China Biotechnology Research Institute Chinese Academy of Agricultural SciencesBeijing 100081China Key Laboratory of Plant Molecular Physiology CAS Center for Excellence in Molecular Plant SciencesInstitute of BotanyChinese Academy of SciencesBeijing 100093China University of Chinese Academy of Sciences Beijing 100049China

Gravity-induced root curvature involves the asymmetric distribution of the phytohormone Auxin.This response depends on the concerted activities of the Auxin transporters such as PIN-FORMED(PIN)proteins for Auxin efflux and Auxin RESISTANT 1(AUX1)for Auxin influx.However,how the Auxin gradient is established remains elusive.Here we identified a new mutant with a short root,strong Auxin distribution in the lateral root cap and an impaired gravitropic response.The causal gene encoded an Arabidopsis homolog of the human unconventional prefoldin RPB5 interactor(URI).At URI interacted with prefoldin 2(PFD2)and PFD6,twoβ-type PFD members that modulate actin and tubulin patterning in roots.The Auxin reporter DR5_(rev):GFP showed that asymmetric Auxin redistribution after gravistimulation is disordered in aturi-1 root tips.Treatment with the endomembrane protein trafficking inhibitor brefeldin A indicated that recycling of the Auxin transporter PIN2 is disrupted in aturi-1 roots as well as in pfd mutants.We propose that At URI cooperates with PFDs to recycle PIN2and modulate Auxin distribution.

关键词： Arabidopsis Auxin cytoskeleton PIN2 prefoldin(PFD) unconventional prefoldin RPB5 interactor(URI)

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The regeneration factors ERF114 and ERF115 regulate Auxin-mediated lateral root development in response to mechanical cues

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Molecular Plant 2022年第10期15卷 1543-1557页

作者： Balkan Canher Fien Lanssens Ai Zhang Anchal Bisht Shamik Mazumdar Jefri Heyman Sebastian Wolf Charles W.Melnyk Lieven De Veylder Department of Plant Biotechnology and Bioinformatics Ghent UniversityGhent B-9052Belgium VIB Center for Plant Systems Biology Ghent B-9052Belgium Department of Plant Biology Linnean Center for Plant BiologySwedish University of Agricultural SciencesAlmas alle 575651 UppsalaSweden Department of Plant Biochemistry Center for Plant Molecular Biology(ZMBP)University of Tubingen72076 TubingenGermany

Plants show an unparalleled regenerative capacity,allowing them to survive severe stress conditions,such as injury,herbivory attack,and harsh weather conditions.This potential not only replenishes tissues and restores damaged organs but can also give rise to whole plant bodies.Despite the intertwined nature of development and regeneration,common upstream cues and signaling mechanisms are largely unknown.Here,we demonstrate that in addition to being activators of regeneration,ETHYLENE RESPONSE FACTOR 114(ERF114)and ERF115 govern developmental growth in the absence of wounding or injury.Increased ERF114 and ERF115 activity enhances Auxin sensitivity,which is correlated with enhanced xylem maturation and lateral root formation,whereas their knockout results in a decrease in lateral roots.Moreover,we provide evidence that mechanical cues contribute to ERF114 and ERF115 expression in correlation with BZR1-mediated brassinosteroid signaling under both regenerative and developmental conditions.Antagonistically,cell wall integrity surveillance via mechanosensory FERONIA signaling suppresses their expression under both conditions.Taken together,our data suggest a molecular framework in which cell wall signals and mechanical strains regulate organ development and regenerative responses via ERF114-and ERF115-mediated Auxin signaling.

关键词： lateral root ERF114 mechanical stress cell wall integrity FERONIA Auxin

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