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The DEAD-box RNA helicase ZmRH48 is required for the splicing of multiple mitochondrial introns,mitochondrial complex biosynthesis,and seed development in maize

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Journal of Integrative plant biology 2023年第11期65卷 2456-2468页

作者： Yan-Zhuo Yang Shuo Ding Xin-Yuan Liu Chunhui Xu Feng Sun Bao-Cai Tan key laboratory of plant development and environmental adaptation biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdao 266237China

RNA helicases participate in nearly all aspects of RNA metabolism by rearranging RNAs or RNA–protein complexes in an adenosine triphosphatedependent manner.Due to the large RNA helicase families in plants,the precise roles of many RNA helicases in plant physiology and development remain to be clarified.Here,we show that mutations in maize(Zea mays)DEAD-box RNA helicase48(Zm RH48)impair the splicing of mitochondrial introns,mitochondrial complex biosynthesis,and seed development.Loss of Zm RH48 function severely arrested embryogenesis and endosperm development,leading to defective kernel formation.Zm RH48 is targeted to mitochondria,where its deficiency dramatically reduced the splicing efficiency of five cis-introns(nad5 intron 1;nad7 introns 1,2,and 3;and ccm Fc intron 1)and one trans-intron(nad2 intron 2),leading to lower levels of mitochondrial complexes I andⅢ.Zm RH48 interacts with two unique pentatricopeptide repeat(PPR)proteins,PPR-SMR1 and SPR2,which are required for the splicing of over half of all mitochondrial introns.PPR-SMR1 interacts with SPR2,and both proteins interact with P-type PPR proteins and Zm-m CSF1 to facilitate intron splicing.These results suggest that Zm RH48 is likely a component of a splicing complex and is critical for mitochondrial complex biosynthesis and seed development.

关键词： intron splicing maize mitochondria RNA helicase seed development ZmRH48

Ca^(2+)-dependent TaCCD1 cooperates with TaSAUR215 to enhance plasma membrane H^(+)-ATPase activity and alkali stress tolerance by inhibiting PP2C-mediated dephosphorylation of TaHA2 in wheat

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Molecular plant 2023年第3期16卷 571-587页

作者： Minghan Cui Yanping Li Jianhang Li Fengxiang Yin Xiangyu Chen Lumin Qin Lin Wei Guangmin Xia Shuwei Liu key laboratory of plant development and environmental adaptation biology Ministry of EducationSchool of Life ScienceShandong UniversityQingdao 266237China

Alkali stress is a major constraint for crop production in many regions of saline-alkali land.However,little is known about the mechanisms through which wheat responds to alkali stress.In this study,we identified a calcium ion-binding protein from wheat,TaCCD1,which is critical for regulating the plasma membrane(PM)H^(+)-ATPase-mediated alkali stress response.PM H+-ATPase activity is closely related to alkali tolerance in the wheat variety Shanrong 4(SR4).We found that two D-clade type 2C protein phosphatases,TaPP2C.D1 and TaPP2C.D8(TaPP2C.D1/8),negatively modulate alkali stress tolerance by dephosphorylating the penultimate threonine residue(Thr926)of TaHA2 and thereby inhibiting PM H+-ATPase activity.Alkali stress induces the expression of TaCCD1 in SR4,and TaCCD1 interacts with TaSAUR215,an early auxin-responsive protein.These responses are both dependent on calcium signaling triggered by alkali stress.TaCCD1 enhances the inhibitory effect of TaSAUR215 on TaPP2C.D1/8 activity,thereby promoting the activity of the PM H^(+)-ATPase TaHA2 and alkali stress tolerance in wheat.Functional and genetic analyses verified the effects of these genes in response to alkali stress,indicating that TaPP2C.D1/8 function downstream of TaSAUR215 and TaCCD1.Collectively,this study uncovers a new signaling pathway that regulates wheat responses to alkali stress,in which Ca^(2+)-dependent TaCCD1 cooperates with TaSAUR215 to enhance PM H+-ATPase activity and alkali stress tolerance by inhibiting TaPP2C.D1/8-mediated dephosphorylation of PM H+-ATPase TaHA2 in wheat.

关键词： Triticum aestivum alkali stress resistance calcium-binding protein small auxin-up RNA plasma membrane H+-ATPase dephosphorylation

SIZ1 negatively regulates aluminum resistance by mediating the STOP1–ALMT1 pathway in Arabidopsis

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Journal of Integrative plant biology 2021年第6期63卷 1147-1160页

作者： Jiameng Xu Jiayong Zhu Jiajia Liu Junxia Wang Zhaojun Ding Huiyu Tian The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationCollege of Life SciencesShandong UniversityQingdao 266237China

Sensitive to proton rhizotoxicity 1(STOP1) functions as a crucial regulator of root growth during aluminum(Al) stress. However, how this transcription factor is regulated by Al stress to affect downstream genes expression is not well understood. To explore the underlying mechanisms of the function and regulation of STOP1, we employed a yeast two hybrid screen to identify STOP1-interacting proteins. The SUMO E3 ligase SIZ1, was found to interact with STOP1 and mainly facilitate its SUMO modification at K40 and K212 residues. Simultaneous introduction of K40 R and K212 R substitutions in STOP1 enhances its transactivation activity to upregulate the expression of aluminum-activated malate transporter 1(ALMT1)via increasing the association with mediator 16(MED16) transcriptional co-activator. Loss of function of SIZ1 causes highly increased expression of ALMT1, thus enhancing Al-induced malate exudation and Al tolerance. Also, we found that the protein level of SIZ1 is reduced in response to Al stress. Genetic evidence demonstrates that STOP1/ALMT1 is epistatic to SIZ1 in regulating root growth response to Al stress. This study suggests a mechanism about how the SIZ1–STOP1–ALMT1 signaling module is involved in root growth response to Al stress.

关键词： ALMT1 aluminum SIZ1 STOP1 SUMOylation

Gibberellin repression of axillary bud formation in Arabidopsis by modulation of DELLA-SPL9 complex activity

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Journal of Integrative plant biology 2020年第4期62卷 421-432页

作者： Qi-Qi Zhang Jia-Gang Wang Ling-Yan Wang Jun-Fang Wang Qun Wang Ping Yu Ming-Yi Bai Min Fan key laboratory of plant development and environmental adaptation biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdao 266237China

The formation of lateral branches has an important and fundamental contribution to the remarkable developmental plasticity of plants,which allows plants to alter their architecture to adapt to the challenging environment conditions.The Gibberellin(GA)phytohormones have been known to regulate the outgrowth of axillary meristems(AMs),but the specific molecular mechanisms remain unclear.Here we show that DELLA proteins regulate axillary bud formation by interacting and regulating the DNA-binding ability of SQUAMOSA-PROMOTER BINDING PROTEIN LIKE 9(SPL9),a micro RNA156-targeted squamosa promoter binding protein-like transcription factor.SPL9 participates in the initial regulation of axillary buds by repressing the expression of LATERAL SUPPRESSOR(LAS),a key regulator inthe initiation of AMs,and LAS contributes to the specific expression pattern of the GA deactivation enzyme GA2ox4,which is specifically expressed in the axils of leaves to form a low-GA cell niche in this anatomical region.Nevertheless,increasing GA levels in leaf axils by ectopically expressing the GA-biosynthesis enzyme GA20ox2 significantly impaired axillary meristem initiation.Our study demonstrates that DELLA-SPL9-LAS-GA2ox4 defines a core feedback regulatory module that spatially pattern GA content in the leaf axil and precisely control the axillary bud formation in different spatial and temporal.

关键词： SPL9 impaired spatially

Auxin signaling:Research advances over the past 30 years

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Journal of Integrative plant biology 2022年第2期64卷 371-392页

作者： Zipeng Yu Feng Zhang JiříFriml Zhaojun Ding The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdao266237 China Institute of Science and Technology(IST) Klosterneuburg3400 Austria

Auxin,one of the first identified and most widely studied phytohormones,has been and will remain a hot topic in plant biology.After more than a century of passionate exploration,the mysteries of its synthesis,transport,signaling,and metabolism have largely been unlocked.Due to the rapid development of new technologies,new methods,and new genetic materials,the study of auxin has entered the fast lane over the past 30 years.Here,we highlight advances in understanding auxin signaling,including auxin perception,rapid auxin responses,TRANSPORT INHIBITOR RESPONSE 1 and AUXIN SIGNALING F-boxes(TIR1/AFBs)-mediated transcriptional and non-transcriptional branches,and the epigenetic regulation of auxin signaling.We also focus on feedback inhibition mechanisms that prevent the over-amplification of auxin signals.In addition,we cover the TRANSMEMBRANE KINASE-mediated non-canonical signaling,which converges with TIR1/AFBs-mediated transcriptional regulation to coordinate plant growth and development.The identification of additional auxin signaling components and their regulation will continue to open new avenues of research in this field,leading to an increasingly deeper,more comprehensive understanding of how auxin signals are interpreted at the cellular level to regulate plant growth and development.

关键词： acid growth auxin perception epigenetic regulation non-transcriptional auxin signaling rapid auxin response root growth inhibition TIR1/AFB-mediated auxin signaling

NAC1 regulates root ground tissue maturation by coordinating with the SCR/SHR-CYCD6;1 module in Arabidopsis

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Molecular plant 2023年第4期16卷 709-725页

作者： Chuantian Xie Cuiling Li Fengxia Wang Feng Zhang Jiajia Liu Junxia Wang Xiansheng Zhang Xiangpei Kong Zhaojun Ding The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationCollege of Life SciencesShandong UniversityQingdao Shandong266237China National key laboratory of Crop biology College of Life SciencesShandong Agricultural UniversityTaianShandong 271018China

Precise spatiotemporal control of the timing and extent of asymmetric cell divisions(AcDs)is essential for plant development.In the Arabidopsis root,ground tissue maturation involves an additional AcD of the endo-dermis that maintains the inner cell layer as the endodermis and generates the middle cortex to the outside.Through regulation of the cell cycle regulator CYCLIND6;1(CYCD6;1),the transcription factors SCARECROW(SCR)and SHORT-ROOT(SHR)play critical roles in this process.In the present study,we found that loss of function of NAC1,a NAC transcription factor family gene,causes markedly increased periclinal cell divisions in the root endodermis.Importantly,NAC1 directly represses the transcription of CYCD6;1 by recruiting the co-repressor TOPLESS(TPL),creating a fine-tuned mechanism to maintain proper root ground tissue patterning by limiting production of middle cortex cells.Biochemical and genetic analyses further showed that NAC1 physically interacts with SCR and SHR to restrict excessive periclinal cell divisions in the endo-dermis during root middle cortex formation.Although NAC1-TPL is recruited to the CYCD6;1 promoter and represses its transcription in an SCR-dependent manner,NAC1 and SHR antagonize each other to regu-late the expression of CYCD6;1.Collectively,our study provides mechanistic insights into how the NAC1-TPL module integrates with the master transcriptional regulators SCR and SHR to control root ground tissue patterning by fine-tuning spatiotemporal expression of CYCD6;1 in Arabidopsis.

关键词： root,NAC1,SCR,SHR,TOPLESS,CYCD6 1

Botrytis cinerea-induced F-box protein 1 enhances disease resistance by inhibiting JAO/JOX-mediated jasmonic acid catabolism in Arabidopsis

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Molecular plant 2024年第2期17卷 297-311页

作者： Min Zhang Weiwei Li Tingyu Zhang Yueyan Liu Lijing Liu The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdao 266237China

Jasmonic acid(JA)is a crucial phytohormone that regulates plant immunity.The endogenous JA level is determined by the rates of its biosynthesis and catabolism in plants.The activation of JA biosynthesis has been well documented;however,how plants repress JA catabolism upon pathogen infection remains elusive.In this study,we identified and characterized Botrytis cinerea-induced F-box protein 1(BFP1)in Arabidopsis.The expression of BFP1 was induced by B.cinerea in a JA signaling-dependent manner,and BFP1 protein was critical for plant defense against B.cinerea and plant response to JA.In addition,BFP1 overexpression increased plant defenses against broad-spectrum pathogens without fitness costs.Further experiments demonstrated that BFP1 interacts with and mediates the ubiquitination and degrada-tion of jasmonic acid oxidases(JAOs,also known as jasmonate-induced oxygenases,JoXs),the enzymes that hydroxylate JA to 12OH-JA.Consistent with this,BFP1 affects the accumulation of JA and 12OH-JA during B.cinerea infection.Moreover,mutation of JAo2 complemented the phenotypes of the bfp1 mutant.Collectively,our results unveil a new mechanism used by plants to activate immune responses upon path-ogeninfection:suppressing JA catabolism.

关键词： plant immunity BFP1 JAO/JOXs JA catabolism ubiquitination-mediated degradation

Antiviral strategies:What can we learn from natural reservoirs?

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Journal of Integrative plant biology 2022年第10期64卷 1849-1855页

作者： Wenbo Pan Weiwei Li Lijing Liu Huawei Zhang Peking University Institute of Advanced Agricultural Sciences Weifang 261325China The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdao 266237China

Viruses cause many severe diseases in both plants and animals,urging us to explore new antiviral strategies.In their natural reservoirs,viruses live and replicate while causing mild or no symptoms.Some animals,such as bats,are the predicted natural reservoir of multiple viruses,indicating that they possess broad-spectrum antiviral capabilities.Mechanisms of host defenses against viruses are generally studied independently in plants and animals.In this article,we speculate that some antiviral strategies of natural reservoirs are conserved between kingdoms.To verify this hypothesis,we created null mutants of 10-formyltetrahydrofolate synthetase(AtTHFS),an Arabidopsis thaliana homologue of methylenetetrahydrofolate dehydrogenase,cyclohydrolase and formyltetrahydrofolate synthetase 1(MTHFD1),which encodes a positive regulator of viral replication in bats.We found that disruption of AtTHFS enhanced plant resistance to three different types of plant viruses,including the tomato spotted wilt virus(TSWV),the cucumber mosaic virus(CMV)and the beet severe curly top virus(BSCTV).These results demonstrate a novel antiviral strategy for plant breeding.We further discuss the approaches used to identify and study natural reservoirs of plant viruses,especially those hosting many viruses,and highlight the possibility of discovering new antiviral strategies from them for plant molecular breeding and antiviral therapy.

关键词： antiviral strategy antiviral therapy cropmolecular breeding natural reservoir virus

Brassinosteroid signaling and molecular crosstalk with nutrients in plants

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遗传学报:英文版 2023年第8期50卷 541-553页

作者： Chao Han Lingyan Wang Jinyang Lyu Wen Shi Lianmei Yao Min Fan Ming-Yi Bai The Key Laboratory of Plant Development and Environmental Adaptation Biology Ministry of EducationSchool of Life SciencesShandong UniversityQingdaoShandong 266237China

As sessile organisms,plants have evolved sophisticated mechanisms to optimize their growth and development in response to fluctuating nutrient levels.Brassinosteroids(BRs)are a group of plant steroid hormones that play critical roles in plant growth and developmental processes as well as plant responses to environmental stimuli.Recently,multiple molecular mechanisms have been proposed to explain the integration of BRs with different nutrient signaling processes to coordinate gene expression,metabolism,growth,and survival.Here,we review recent advances in understanding the molecular regulatory mechanisms of the BR signaling pathway and the multifaceted roles of BR in the intertwined sensing,signaling,and metabolic processes of sugar,nitrogen,phosphorus,and iron.Further understanding and exploring these BR-related processes and mechanisms will facilitate advances in crop breeding for higher resource efficiency.

关键词： Brassinosteroids Sugar Nitrogen Phosphorus Iron