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Revealing the role of CCoAOMT1: fine-tuning bHLH transcription factors for optimal anther development

Science China(Life Sciences) 2024年第3期67卷 565-578页

作者： Zesen Lai Jianzheng Wang Ying Fu Menghan Wang Hong Ma Shiqing Peng Fang Chang State Key Laboratory of Genetic Engineering Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering and Institute of Biodiversity SciencesInstitute of Plant BiologySchool of Life SciencesFudan UniversityShanghai 200438China School of Tropical Agriculture and Forestry Agriculture-Rural Affairs and Rural RevitalizationHainan UniversityHaikou 570228China Key Laboratory of Biology and Genetic Resources of Tropical Crops Ministry of AgricultureInstitute of Tropical Bioscience and BiotechnologyChinese Academy of Tropical Agricultural SciencesHaikou 571101China Department of Biology Huck Institutes of the Life SciencesPennsylvania State UniversityUniversity ParkPA 16802USA

The tapetum,a crucial innermost layer encompassing male reproductive cells within the anther wall,plays a pivotal role in normal pollen development.The transcription factors (TFs) bHLH010/089/091 redundantly facilitate the rapid nuclear accumulation of DYSFUNCTIONAL TAPETUM 1,a gatekeeper TF in the tapetum.Nevertheless,the regulatory mechanisms governing the activity of bHLH010/089/091 remain unknown.In this study,we reveal that caffeoyl coenzyme A O-methyltransferase 1 (CCoAOMT1) is a negative regulator affecting the nuclear localization and function of bHLH010 and bHLH089,probably through their K259 site.Our findings underscore that CCoAOMT1 promotes the nuclear export and degradation of bHLH010 and bHLH089.Intriguingly,elevated CCoAOMT1 expression resulted in defective pollen development,mirroring the phenotype observed in bhlh010 bhlh089 mutants.Moreover,our investigation revealed that the K259A mutation in the bHLH089 protein disrupted its translocation from the nucleus to the cytosol and impeded its degradation induced by CCoAOMT1.Importantly,transgenic plants with the probHLH089::bHLH089^(K259A)construct failed to rescue proper pollen development or gene expression in bhlh010 bhlh089 mutants.Collectively,these findings emphasize the need to maintain balanced TF homeostasis for male fertility.They firmly establish CCoAOMT1 as a pivotal regulator that is instrumental in achieving equilibrium between the induction of the tapetum transcriptional network and ensuring appropriate anther development.

关键词： anther development nuclear localization bHLH O-methyltransferase transcription factor homeostasis

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GAMYB transcription factor LoMYB65 from lily plays a vital role in pollen development

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Horticultural Plant Journal 2024年第1期10卷 223-238页

作者： Xinyue Liu Ling He Ze Wu Nianjun Teng Key Laboratory of Landscaping Agriculture Ministry of Agriculture and Rural AffairsCollege of HorticultureNanjing Agricultural UniversityNanjingJiangsu 210095China Key Laboratory of Biology of Ornamental Plants in East China National Forestry and Grassland AdministrationCollege of HorticultureNanjing Agricultural UniversityNanjingJiangsu 210095China Jiangsu Graduate Workstation of Nanjing Agricultural University and Nanjing Oriole Island Modern Agricultural development Co. Ltd.NanjingJiangsu 210043China

Lily(Lilium spp.)is an important horticultural crop,but its use is limited due to serious pollen contamination problems.There are many studies on pollen development in model plants,but few on flower crops such as lilies.Gibberellin(GA)is a large class of hormones and plays an important role in plant vegetative growth and reproductive development.GAMYB is a group of the R2R3-MYB family upregulated by gibberellin,and plays an important role in anther development.Here,we isolated a novel GAMYB,named LoMYB65,from lily,which was closely related to the AtMYB65 and AtMYB33 in Arabidopsis.Fluorescence quantitative PCR results showed that LoMYB65 was mainly expressed in lily anthers.LoMYB65 could be activated by 288μmol·L^(-1)GA3treatment and the LoMYB65 protein was located in the nucleus and cytoplasm,and had transactivation in yeast and tobacco leaf cells.The conserved motif within 226 amino acids of the C-terminal of LoMYB65 contributed to its transactivation.Overexpression of LoMYB65 caused dwarf phenotype,unnormal tapetum development,less seeds of siliques in transgenic Arabidopsis plants,the transgenic plants showed partly male sterile.Simultaneously,silencing of LoMYB65 with VIGS(Virus Induced Gene Silencing)in lily anthers caused unnormal pollen development and reduced the pollen amount.Overexpression of LoMYB65 in Arabidopsis and silencing of LoMYB65 in lily resulted in decreased pollen counts,so we speculate that LoMYB65 may be dose-dependent.Overall,these findings suggest that LoMYB65 may play an important role in anther development and pollen formation in lily.LoMYB65 may provide a useful candidate gene for pollenless breeding of lily.

关键词： Lily anther development Pollen pollution GAMYB VIGS

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Exploring key developmental phases and phase-specific genes across the entirety of anther development in maize

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Journal of Integrative Plant Biology 2022年第7期64卷 1394-1410页

作者： Yingjia Han Mingjian Hu Xuxu Ma Ge Yan Chunyu Wang Siqi Jiang Jinsheng Lai Mei Zhang Key Laboratory of Plant Molecular Physiology Institute of BotanyThe Chinese Academy of SciencesBeijing 100093China State Key Laboratory of Plant Physiology and Biochemistry&National Maize Improvement Center of China Department of Plant Genetics and Breeding China Agricultural UniversityBeijing 100193China University of Chinese Academy of Sciences Beijing 100049China

anther development from stamen primordium to pollen dispersal is complex and essential to sexual reproduction.How this highly dynamic and complex developmental process is controlled genetically is not well understood,especially for genes involved in specific key developmental phases.Here we generated RNA sequencing libraries spanning 10 key stages across the entirety of anther development in maize(Zea mays).Global transcriptome analyses revealed distinct phases of cell division and expansion,meiosis,pollen maturation,and mature pollen,for which we detected 50,245,42,and 414 phase-specific marker genes,respectively.Phase-specific transcription factor genes were significantly enriched in the phase of meiosis.The phase-specific expression of these marker genes was highly conserved among the maize lines Chang7-2 and W23,indicating they might have important roles in anther development.We explored a desiccationrelated protein gene,ZmDRP1,which was exclusively expressed in the tapetum from the tetrad to the uninucleate microspore stage,by generating knockout mutants.Notably,mutants in ZmDRP1 were completely male-sterile,with abnormal Ubisch bodies and defective pollen exine.Our work provides a glimpse into the gene expression dynamics and a valuable resource for exploring the roles of key phase-specific genes that regulate anther development.

关键词： anther development maize male-sterile phase-specific genes transcriptome ZmDRP1

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ABCB1 and ABCB19 auxin transporters have synergistic effects on early and late Arabidopsis anther development

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Journal of Integrative Plant Biology 2015年第12期57卷 1089-1098页

作者： Valentina Cecchetti Patrizia Brunetti Nadia Napoli Laura Fattorini Maria Maddalena Altamura Paolo Costantino Maura Cardarelli IBPM-CNR Institute of Molecular Biology and Pathology National Research Council Sapienza University of Rome Department of Biology and Biotechnology Sapienza University of Rome Department of Environmental Biology Sapienza University of Rome

Arabidopsis abcbl abcb19 double mutants defective in the auxin transporters ABCB1/PGP1 and ABCB19/PGP19 are altered in stamen elongation, anther dehiscence and pollen maturation. To assess the contribution of these transporters to stamen development we performed phenotypic, histological analyses, and in situ hybridizations on abcbl and abcbl9 single mutant flowers. We found that pollen maturation and anther dehiscence are precocious in the abcbl but not in the abcb19 mutant. Accordingly, endothecium ligniflcation is altered only in abcbl anthers. Both abcbl and abcb1 abcb19 stamens also show altered early development, with asynchronous anther Iocules and a multilayer tapetum. DAPI staining showed that the timing of meiosis is asynchronous in abcbl abcb19 anther Iocules, while only a small percentage of pollen grains are non- viable according to Alexander＇s staining. In agreement, TAM （TARDY ASYNCHRONOUS MEIOSIS）, as well as BAM2 （BARELY ANY MERISTEM）involved in tapetal cell development--areoverexpressed in abcbl abcb19 young flower buds. Corre- spondingly, ABCB1 and ABCB19 mRNA localization supports the observed phenotypes of abcbl and abcbl abcb19 mutant anthers. In conclusion, we provide evidence that auxin transport plays a significant role both in early and late stamen development： ABCB1 plays a major role during anther development, while ABCB19 has a synergistic role.

关键词： anther development Arabidopsis auxin transport endothecium lignification tapetum differentiation

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Normal Structure and Function of Endothecium Chloroplasts Maintained by ZmMs33-Mediated Lipid Biosynthesis in Tapetal Cells Are Critical for anther development in Maize

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Molecular Plant 2020年第11期13卷 1624-1643页

作者： Taotao Zhu Ziwen Li Xueli An Yan Long Xiaofeng Xue Ke Xie Biao Ma Danfeng Zhang Yijian Guan Canfang Niu Zhenying Dong Quancan Hou Lina Zhao Suowei Wu Jinping Li Weiwei Jin Xiangyuan Wan Zhongzhi International Institute of Agricultural Biosciences Biology and Agriculture Research Center of USTBUniversity of Science and Technology Beijing(USTB)Beijing 100024China Beijing Engineering Laboratory of Main Crop Bio-Tech Breeding Beijing International Science and Technology Cooperation Base of Bio-Tech BreedingBeijing Solidwill Sci-Tech Co.Ltd.Beijing 100192China Risk Assessment Laboratory for Bee Products Quality and Safety of Ministry of Agriculture Institute of Apicultural ResearchChinese Academy of Agricultural SciencesBeijing 100093China State Key Laboratory of Plant Physiology and Biochemistry National Maize Improvement CenterKey Laboratory of Biology and Genetic Improvement of Maize(MOA)Beijing Key Laboratory of Crop Genetic ImprovementChina Agricultural UniversityBeijing 100193China

Genic male sterility(GMS)is critical for heterosis utilization and hybrid seed production.Although GMS mutants and genes have been studied extensively in plants,it has remained unclear whether chloroplast-associated photosynthetic and metabolic activities are involved in the regulation of anther development.In this study,we characterized the function of ZmMs33/ZmGPAT6,which encodes a member of the glycerol-3-phosphate acyltransferase(GPAT)family that catalyzes the first step of the glycerolipid synthetic pathway.We found that normal structure and function of endothecium(En)chloroplasts maintained by ZmMs33-mediated lipid biosynthesis in tapetal cells are crucial for maize anther development.ZmMs33 is expressed mainly in the tapetum at early anther developmental stages and critical for cell proliferation and expansion at late stages.Chloroplasts in En cells of wild-type anthers function as starch storage sites before stage 10 but as photosynthetic factories since stage 10 to enable starch metabolism and carbohydrate supply.Loss of ZmMs33 function inhibits the biosynthesis of glycolipids and phospholipids,which are major components of En chloroplast membranes,and disrupts the development and function of En chloroplasts,resulting in the formation of abnormal En chloroplasts containing numerous starch granules.Further analyses reveal that starch synthesis during the day and starch degradation at night are greatly suppressed in the mutant anthers,leading to carbon starvation and low energy status,as evidenced by low trehalose-6-phosphate content and a reduced ATP/AMP ratio.The energy sensor and inducer of autophagy,SnRK1,was activated to induce early and excessive autophagy,premature PCD,and metabolic reprogramming in tapetal cells,finally arresting the elongation and development of mutant anthers.Taken together,our results not only show that ZmMs33 is required for normal structure and function of En chloroplasts but also reveal that starch metabolism and photosynthetic activities of En chloroplasts at different devel

关键词： ZmMs33/ZmGPAT6 chloroplast SnRK1 autophagy anther development maize

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Maize MS2 encodes an ATP-binding cassette transporter that is essential for anther development

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The Crop Journal 2021年第6期9卷 1301-1308页

作者： Qilong Xu Li Yang Dan Kang Zhenjing Ren Yunjun Liu Institute of Crop Sciences Chinese Academy of Agricultural SciencesBeijing 100081China

The anther cuticle and pollen exine play a critical role in male gametophyte development. The sporopollenin precursors and cuticular lipid monomers are transported to the surface of the microspores and the epidermis by lipid transport proteins(LTPs) and ATP-binding cassette G(ABCG) transporters for the formation of the pollen wall and anther cuticle, respectively. However, the function of ABCG transporters in maize anther development is unclear. Here, we cloned the MS2 gene from the maize male sterile2 mutant using map-based cloning and determined that it encodes an ABCG transporter. MS2 protein was experimentally confirmed to be located on the cell membrane. The quantitative real-time PCR(qRT-PCR)results showed that MS2 was ubiquitously expressed in all vegetative and reproductive tissues, whereas a high transcriptional level of MS2 was observed in anthers, especially at the young microspore stage. Gas chromatography-mass spectrometry(GC–MS) analysis showed decreased accumulation of cutin and wax components in ms2 anthers, indicating that MS2 plays a role in the transport of lipid molecules to anther cuticle and pollen exine. To our knowledge, MS2 is the first reported ABCG transporter gene that participates in anther development in maize.

关键词： Zea mays ABCG transporter Male sterility anther development

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Regulation of Arabidopsis Early anther development by Putative Cell-Cell Signaling Molecules and Transcriptional Regulators

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Journal of Integrative Plant Biology 2007年第1期49卷 60-68页

作者： Yu-Jin Sun Carey LH Hord Chang-Bin Chen Hong Ma Department of Biology and the Huck Institutes of the Life Sciences Pennsylvania State University University Park PA 16802 USA The Integrative Bioscience Graduate Program Pennsylvania State University University Park PA 16802 USA

anther development in flowering plants involves the formation of several cell types, including the tapetal and pollen mother cells. The use of genetic and molecular tools has led to the identification and characterization of genes that are critical for normal cell division and differentiation in Arabidopsis early anther development. We review here several recent studies on these genes, including the demonstration that the putative receptor protein kinases BAM1 and BAM2 together play essential roles in the control of early cell division and differentiation. In addition, we discuss the hypothesis that BAM1/2 may form a positive-negative feedback regulatory loop with a previously identified key regulator, SPOROCYTELESS （also called NOZZLE）, to control the balance between sporogenous and somatic cell types in the anther. Furthermore, we summarize the isolation and functional analysis of the DYSFUNCTIONAL TAPETUM1 （DYT1） gene in promoting proper tapetal cell differentiation. Our finding that DYT1 encodes a putative transcription factor of the bHLH family, as well as relevant expression analyses, strongly supports a model that DYT1 serves as a critical link between upstream factors and downstream target genes that are critical for normal tapetum development and function. These studies, together with other recently published works, indicate that cell-cell communication and transcriptional control are key processes essential for cell fate specification in anther development.

关键词： anther development Arabidopsis signaling tapetum transcription factor

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Molecular Control of Male Reproductive development and Pollen Fertility in Rice

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Journal of Integrative Plant Biology 2012年第12期54卷 967-978页

作者： Jing-Xin Guo Yao-Guang Liu State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources College of Life SciencesSouth China Agricultural University

anther development and male fertility are essential biological pro- cesses for flowering plants and are important for crop seed produc- tion. Genetic manipulation of male fertility/sterility is critical for crop hybrid breeding. Rice （Oryza sativa L.） male sterility phenotypes, including genic male sterility, hybrid male sterility, and cytoplasmic male sterility, are generally caused by mutations of fertility-related genes, by incompatible interactions between divergent allelic or non-allelic genes, or by genetic incompatibilities between cytoplas-mic and nuclear genomes. Here, we review the recent advances in the molecular basis of anther development and male fertility-sterility conversion in specific genetic backgrounds, and the interactions with certain environmental factors. The highlighted findings in this review have significant implications in both basic studies and rice genetic improvement.

关键词： anther development cytoplasmic male sterility hybrid sterility male fertility meiosis rice.

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A Genetic Pathway for Tapetum development and Function in Arabidopsis

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Journal of Integrative Plant Biology 2011年第11期53卷 892-900页

作者： Jun Zhu Yue Lou Xiaofeng Xu Zhong-Nan Yang College of Life and Environmental Sciences Shanghai Normal University Shanghai 200234 China

In anther development, tapetal cells take part in complex processes, including endomitosis and apoptosis （programmed cell death）. The tapetum provides many of the proteins, lipids, polysaccharides and other molecules necessary for pollen development. Several transcription factors, including DYT1, TDF1, AMS, MS188 and MS1, have been reported to be essential for tapetum development and function in Arabidopsis thaliana. Here, we present a detailed cytological analysis of knockout mutants for these genes, along with an in situ RNA hybridization experiment and double mutant analysis showing that these transcription factors form a genetic pathway in tapetum development. DYT1, TDF1 and AMS function in early tapetum development, while MS188 and MS1 are important for late tapetum development. The genetic pathway revealed in this work facilitates further investigation of the function and molecular mechanisms of tapetum development in Arabidopsis.

关键词： anther development genetic pathway pollen development tapetum transcription factor DYT1 TDF1 AMS MS188 MS1.

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Transcription Factor Genes and Their miRNA and ceRNA Regulators Associated with Maize anther development

Transcription Factor Genes and Their miRNA and ceRNA Regulat...

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第十九届中国作物学会学术年会

作者： Ziwen Li Taotao Zhu Yuwen Zhang Xiangyuan Wan Zhongzhi International Institute of Agricultural Biosciences Biology and Agriculture Research Center University of Science and Technology Beijing

【Background】anther development is a multistage and programmed biological process that is crucial for plant male reproduction. Genome-wide analysis on the functions of transcriptional factor(TF) genes and their microRNA(miRNA) regulators in maize anther development has not been comprehensively studied and our understanding on the molecular mechanisms of anther development and its underlying regulatory network is far from complete. 【Method】 Here, by using the previously published RNA-seq and small RNA-seq data from maize anthers sampled of five or ten different anther lengths covering the major anther development stages in three genic male sterility(GMS) lines(ocl4, mac1, and ms23) and a male-fertility inbred line(W23) respectively, we computationally analyzed TF genes and miRNAs associated with anther development in maize.【Results】We found that expression patterns of the predicted 2154 TF genes were grouped into six clusters(premeiotic, meiotic, postmeiotic, premeiotic-meiotic, premeiotic-postmeiotic, and meiotic-postmeiotic types). Furthermore, the function enrichment results of genes co-expressed with each of the six expression patterns were consistent with the major characteristics of maize anther development at cytological level. In addition, 118 miRNAs harbored detectable expression levels in the ten sampled lengths of maize anthers, among which zma-miR529, zma-miR218, zma-miR166, zma-miR319, zma-miR2275, zma-miR159, zma-miR408, zma-miR168, zma-miR167, and zma-miR396 were highly expressed. Differentially expressed genes(DEGs) and miRNAs between W23 and each of the three GMS lines were identified and the following combination analysis predicted more than 50 miRNA-TF gene regulatory modules, which were highly associated with maize anther development, such as miR169-NF-YA, miR156-SBP, miR166-HD-ZIP, miR396-GRF, and miR156/miR319-MYB. Finally, several ce RNA regulators of miRNAs associated with maize anther development were identified. 【Conclusion】 These findings may expand the regulatory network between RNAs and

关键词： transcription factor gene microRNA genic male sterility gene anther development maize

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