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MdbHLH162 connects the gibberellin and jasmonic acid signals to regulate anthocyanin biosynthesis in apple

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Journal of Integrative Plant Biology 2024年第2期66卷 265-284页

作者： Jian-Ping An Rui-Rui Xu Xiao-Na Wang Xiao-Wei Zhang Chun-Xiang You Yuepeng Han Apple technology innovation center of Shandong Province College of Horticulture Science and EngineeringShandong Agricultural UniversityTai-An 271018China CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture Wuhan Botanical GardenHubei Hongshan LaboratoryThe Innovative Academy of Seed Design of Chinese Academy of SciencesWuhan 430074China College of Biology and Oceanography Weifang UniversityWeifang 261061China

Anthocyanins are secondary metabolites induced by environmental stimuli and developmental signals.The positive regulators of anthocyanin biosynthesis have been reported,whereas the anthocyanin repressors have been neglected.Although the signal transduction pathways of gibberellin(GA)and jasmonic acid(JA)and their regulation of anthocyanin biosynthesis have been investigated,the cross-talk between GA and JA and the antagonistic mechanism of regulating anthocyanin biosynthesis remain to be investigated.In this study,we identified the anthocyanin repressor MdbHLH162 in apple and revealed its molecular mechanism of regulating anthocyanin biosynthesis by integrating the GA and JA signals.MdbHLH162 exerted passive repression by interacting with MdbHLH3 and MdbHLH33,which are two recognized positive regulators of anthocyanin biosynthesis.MdbHLH162 negatively regulated anthocyanin biosynthesis by disrupting the formation of the anthocyanin-activated MdMYB1-MdbHLH3/33complexes and weakening transcriptional activation of the anthocyanin biosynthetic genes MdDFR and MdUF3GT by MdbHLH3 and MdbHLH33.The GA repressor MdRGL2a antagonized MdbHLH162-mediated inhibition of anthocyanins by sequestering MdbHLH162 from the MdbHLH162-MdbHLH3/33 complex.The JA repressors MdJAZ1 and MdJAZ2 interfered with the antagonistic regulation of MdbHLH162 by MdRGL2a by titrating the formation of the MdRGL2a-MdbHLH162 complex.Our findings reveal that MdbHLH162 integrates the GA and JA signals to negatively regulate anthocyanin biosynthesis.This study provides new information for discovering more anthocyanin biosynthesis repressors and explores the cross-talk between hormone signals.

关键词： anthocyanin biosynthesis bHLH transcription factor gibberellin jasmonic acid regulatory network transcriptional regulation

OsWRKY78 regulates panicle exsertion via gibberellin signaling pathway in rice

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Journal of Integrative Plant Biology 2024年第4期66卷 771-786页

作者： Enyang Mei Mingliang He Min Xu Jiaqi Tang Jiali Liu Yingxiang Liu Zhipeng Hong Xiufeng Li Zhenyu Wang Qingjie Guan Xiaojie Tian Qingyun Bu State Key Laboratory of Black Soils Conservation and Utilization Key Laboratory of Soybean Molecular Design BreedingNortheast Institute of Geography and AgroecologyChinese Academy of SciencesHarbin 150081China University of Chinese Academy of Sciences Beijing 100049China Key Laboratory of Saline-alkali Vegetation Ecology Restoration Northeast Forestry UniversityMinistry of EducationHarbin 150040China College of Life Science Northeast Forestry UniversityHarbin 150040China

Panicle exsertion is one of the crucial agronomic traits in rice(Oryza sativa).Shortening of panicle exsertion often leads to panicle enclosure and severely reduces seed production.gibberellin(GA)plays important roles in regulating panicle exsertion.However,the underlying mechanism and the relative regulatory network remain elusive.Here,we characterized the oswrky78 mutant showing severe panicle enclosure,and found that the defect of oswrky78 is caused by decreased bioactive GA contents.Biochemical analysis demonstrates that OsWRKY78 can directly activate GA biosynthesis and indirectly suppress GA metabolism.Moreover,we found OsWRKY78 can interact with and be phosphorylated by mitogen-activated protein kinase(MAPK)kinase OsMAPK6,and this phosphorylation can enhance OsWRKY78 stability and is necessary for its biological function.Taken together,these results not only reveal the critical function of OsWRKY78,but also reveal its mechanism via mediating crosstalk between MAPK and the GA signaling pathway in regulating panicle exsertion.

关键词： gibberellin MAPK cascades OsWRKY78 panicle exsertion rice

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)

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

The HB40-JUB1 transcriptional regulatory network controls gibberellin homeostasis in Arabidopsis

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Molecular Plant 2022年第2期15卷 322-339页

作者： Shuchao Dong Danuse Tarkowska Mastoureh Sedaghatmehr Maryna Welsch Saurabh Gupta Bernd Mueller-Roeber Salma Balazadeh Max-Planck Institute of Molecular Plant Physiology Am Mühlenberg 114476 Potsdam-GolmGermany Institute of Biology Leiden UniversitySylviusweg 722333 BE LeidenThe Netherlands Laboratory of Growth Regulators Czech Academy of SciencesInstitute of Experimental Botany&Palacky UniversityŠlechtitelû2778371 OlomoucCzech Republic University of Potsdam Institute of Biochemistry and BiologyKarl-Liebknecht-Stra?e 24-25Haus 2014476 Potsdam-GolmGermany

The gibberellins(GAs)are phytohormones that play fundamental roles in almost every aspect of plant growth and development.Although GA biosynthetic and signaling pathways are well understood,the mechanisms that control GA homeostasis remain largely unclear in plants.Here,we demonstrate that the homeobox transcription factor(TF)HB40 of the HD-Zip family regulates GA content at two additive con-trol levels in Arabidopsis thaliana.We show that HB40 expression is induced by GA and in turn reduces the levels of endogenous bioactive GAs by simultaneously reducing GA biosynthesis and increasing GA deac-tivation.Consistently,HB40 overexpression leads to typical GA-deficiency traits,such as small rosettes,reduced plant height,delayed flowering,and male sterility.By contrast,a loss-of-function hb40 mutation enhances GA-controlled growth.Genome-wide RNA sequencing combined with molecular-genetic ana-lyses revealed that HB40 directly activates the transcription of JUNGBRUNNEN1(JJUB1),a key TF that re-presses growth by suppressing GA biosynthesis and signaling.HB40 also activates genes encoding GA 2-oxidases(GA2oxs),which are major GA-catabolic enzymes.The effect of HB40 on plant growth is ultimately mediated through the induction of nuclear growth-repressing DELLA proteins.Collectively,our results reveal the important role of the HB40-JUB1 regulatory network in controlling GA homeostasis during plant growth.

关键词： Arabidopsis growth gibberellin homeostasis transcription factor HB40 JUB1 GA 2-oxidase DELLA proteins

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

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Journal of Genetics and Genomics 2022年第8期49卷 756-765页

作者： Lichao Chen Shuhao Sun Chun-Peng Song Jian-Min Zhou Jiayang Li Jianru Zuo State Key Laboratory of Plant Genomics Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijing 100101China College of Advanced Agricultural Sciences University of Chinese Academy of SciencesBeijing 100049China CAS Center for Excellence in Molecular Plant Sciences Chinese Academy of SciencesBeijing 100101China State Key Laboratory of Crop Stress Adaptation and Improvement Collaborative Innovation Center of Crop Stress BiologyHenan UniversityKaifengHenan 475001China Hainan Yazhou Bay Seed Laboratory SanyaHainan 572025China

In response to dynamically altered environments,plants must finely coordinate the balance between growth and stress responses for their survival.However,the underpinning regulatory mechanisms remain largely elusive.The phytohormone gibberellin promotes growth via a derepression mechanism by proteasomal degradation of the DELLA transcription repressors.Conversely,the stress-induced burst of nitric oxide(NO)enhances stress tolerance,largely relying on NO-mediated S-nitrosylation,a redox-based posttranslational modification.Here,we show that S-nitrosylation of Cys-374 in the Arabidopsis RGA protein,a key member of DELLAs,inhibits its interaction with the F-box protein SLY1,thereby preventing its proteasomal degradation under salinity condition.The accumulation of RGA consequently retards growth but enhances salt tolerance.We propose that NO negatively regulates gibberellin signaling via S-nitrosylation of RGA to coordinate the balance of growth and stress responses when challenged by adverse environments.

关键词： gibberellin Nitric oxide S-nitrosylation DELLA repressors Stress responses

Histological,transcriptomic,and gene functional analyses reveal the regulatory events underlying gibberellin-induced parthenocarpy in tomato

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Horticultural Plant Journal 2024年第1期10卷 156-170页

作者： Shaobo Niu Yu He Siwei Yan Zhengliang Sun Run Cai Yan Zhang Shaanxi Engineering Research Center for Vegetables College of HorticultureNorthwest A&F UniversityYanglingShaanxi 712100China

gibberellin(GA)is one of the major plant hormones that promote parthenocarpy,a highly valuable agronomic trait.Here,we demonstrated that exogenous GA3application triggered the formation of parthenocarpic fruits with smaller size but unchanged shape in tomato(Solanum lycopersicum).These fruits exhibited a thicker pericarp,undeveloped ovules,and few jelly tissues,leading to smaller locules with empty cavities.Histological investigation showed that GA treatment produced more cell layers with larger cells in the pericarp,suggesting its promotion in both cell division and expansion.Transcriptomic analyses between GA-3and mock-treated unpollinated ovaries/fruits identified a large number of differentially expressed genes related to hormones,cell division,cell expansion,and transcription factors,implying that they coordinately regulated parthenocarpy conferred by GA.In particular,the downregulation of five reported repressors of tomato parthenocarpy,including two auxin signaling components,AUXIN RESPONSE FACTOR5(SlARF5)and Sl ARF7,and three MADS-box genes,TOMATO APETALA3(TAP3),TOMATO PISTILLATA(TPI),and AGAMOUS-LIKE6(SlAGL6),after GA treatment might play a key role in this process.Furthermore,we found that the knockdown of a GA signaling factor SlMYB33,which was depressed by GA treatment,induced parthenocarpic fruit set in tomato,an effect that might have been achieved by enhancing GA biosynthesis and decreasing the expression of some repressors of tomato parthenocarpy.Thus,our results provide a basis for understanding the regulatory mechanism of GA in tomato parthenocarpy.

关键词： Tomato gibberellin Parthenocarpy Histology Transcriptome SlMYB33

gibberellin promotes cambium reestablishment during secondary vascular tissue regeneration after girdling in an auxin-dependent manner in Populus

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Journal of Integrative Plant Biology 2024年第1期66卷 86-102页

作者： Yufei Zhang Lingyan Wang Yuexin Wu Donghui Wang Xin‐Qiang He State Key Laboratory of Protein and Plant Gene Research School of Life SciencesPeking UniversityBeijing 100871China

Secondary vascular tissue(SVT)development and regeneration are regulated by phytohormones.In this study,we used an in vitro SVT regeneration system to demonstrate that gibberellin(GA)treatment significantly promotes auxin-induced cambium reestablishment.Altering GA content by overexpressing or knocking down ent-kaurene synthase(KS)affected secondary growth and SVT regeneration in poplar.The poplar DELLA gene GIBBERELLIC ACID INSENSITIVE(PtoGAI)is expressed in a specific pattern during secondary growth and cambium regeneration after girdling.Overexpression of PtoGAI disrupted poplar growth and inhibited cambium regeneration,and the inhibition of cambium regeneration could be partially restored by GA application.Further analysis of the PtaDR5:GUS transgenic plants,the localization of PIN-FORMED 1(PIN1)and the expression of auxin-related genes found that an additional GA treatment could enhance the auxin response as well as the expression of PIN1,which mediates auxin transport during SVT regeneration.Taken together,these findings suggest that GA promotes cambium regeneration by stimulating auxin signal transduction.

关键词： auxin cambium gibberellin Populus secondary vascular tissue regeneration

gibberellin in tomato:metabolism,signaling and role in drought responses

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Molecular Horticulture 2021年第1期1卷 19-30页

作者： Hagai Shohat Natanella Illouz Eliaz David Weiss Institute of Plant Sciences and Genetics in Agriculture The Hebrew University of JerusalemP.O.Box 1276100 RehovotIsrael Plant Biology Laboratory The Salk Institute for Biological StudiesLa JollaCA 92037USA

The growth-promoting hormone gibberellin(GA)regulates numerous developmental processes throughout the plant life cycle.It also affects plant response to biotic and abiotic stresses.GA metabolism and signaling in tomato(Solanum lycopersicum)have been studied in the last three decades and major components of the pathways were characterized.These include major biosynthesis and catabolism enzymes and signaling components,such as the three GA receptors gibberellin INSENSITIVE DWARF 1(GID1)and DELLA protein PROCERA(PRO),the central response suppressor.The role of these components in tomato plant development and response to the environment have been investigated.Cultivated tomato,similar to many other crop plants,are susceptible to water deficiency.Numerous studies on tomato response to drought have been conducted,including the possible role of GA in tomato drought resistance.Most studies showed that reduced levels or activity of GA improves drought tolerance and drought avoidance.This review aims to provide an overview on GA biosynthesis and signaling in tomato,how drought affects these pathways and how changes in GA activity affect tomato plant response to water deficiency.It also presents the potential of using the GA pathway to generate drought-tolerant tomato plants with improved performance under both irrigation and water-limited conditions.

关键词： gibberellin DELLA Abscisic acid Drought resistance Tomato Gene editing Yield