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Two gene clusters and their positive regulator SlMYB13 that have undergone domestication-associated negative selection control phenolamide accumulation and drought tolerance in tomato

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Molecular Plant 2024年第4期17卷 579-597页

作者： Peng Cao Jun Yang Linghao Xia Zhonghui Zhang Zeyong Wu Yingchen Hao Penghui Liu Chao wang Chun Li Jie Yang Jun Lai Xianggui Li Meng Deng shouchuang wang School of Breeding and Multiplication(Sanya Institute of Breeding and Multiplication) Hainan UniversitySanya 572025China College of Tropical Agriculture and Forestry Hainan UniversityHaikou 572208China Collaborative Innovation Center of Nanfan and High-Efficiency Tropical Agriculture Hainan UniversityHaikou 572208China

Among plant metabolites,phenolamides,which are conjugates of hydroxycinnamic acid derivatives and polyamines,play important roles in plant adaptation to abiotic and biotic stresses.However,the molecular mechanisms underlying phenolamide metabolism and regulation as well as the effects of domestication and breeding on phenolamide diversity in tomato remain largely unclear.In this study,we performed a metabolite-based genome-wide association study and identified two biosynthetic gene clusters(BGC7 and BGC11)containing 12 genes involved in phenolamide metabolism,including four biosynthesis genes(two 4CL genes,one C3H gene,and one CPA gene),seven decoration genes(five AT genes and two UGT genes),and one transport protein gene(DTX29).Using gene co-expression network analysis we further discovered that SlMYB13 positively regulates the expression of two gene clusters,thereby promoting phenolamide accumulation.Genetic and physiological analyses showed that BGC7,BGC11 and SlMYB13 enhance drought tolerance by enhancing scavenging of reactive oxygen species and increasing abscisic acid content in tomato.Natural variation analysis suggested that BGC7,BGC11 and SlMYB13 were negatively selected during tomato domestication and improvement,leading to reduced phenolamide content and drought tolerance of cultivated tomato.Collectively,our study discovers a key mechanism of phenolamide biosynthesis and regulation in tomato and reveals that crop domestication and improvement shapes metabolic diversity to affect plant environmental adaptation.

关键词： tomato phenolamides gene cluster drought tolerance natural variation evolution

Population analysis reveals the roles of DNA methylation in tomato domestication and metabolic diversity

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Science China(Life Sciences) 2023年第8期66卷 1888-1902页

作者： Hao Guo Peng Cao Chao wang Jun Lai Yuan Deng Chun Li Yingchen Hao Zeyong Wu Ridong Chen Qi Qiang Alisdair RFernie Jun Yang shouchuang wang Sanya Nanfan Research Institute of Hainan University Hainan Yazhou Bay Seed LaboratorySanya 572025China College of Tropical Crops Hainan UniversityHaikou 572208China Max-Planck-Institute of Molecular Plant Physiology Potsdam-Golm 144776Germany

DNA methylation is an important epigenetic marker,yet its diversity and consequences in tomato breeding at the population level are largely unknown.We performed whole-genome bisulfite sequencing(WGBS),RNA sequencing,and metabolic profiling on a population comprising wild tomatoes,landraces,and cultivars.A total of 8,375 differentially methylated regions(DMRs)were identified,with methylation levels progressively decreasing from domestication to improvement.We found that over 20%of DMRs overlapped with selective sweeps.Moreover,more than 80%of DMRs in tomato were not significantly associated with single-nucleotide polymorphisms(SNPs),and DMRs had strong linkages with adjacent SNPs.We additionally profiled 339 metabolites from 364 diverse accessions and further performed a metabolic association study based on SNPs and DMRs.We detected 971 and 711 large-effect loci via SNP and DMR markers,respectively.Combined with multi-omics,we identified 13 candidate genes and updated the polyphenol biosynthetic pathway.Our results showed that DNA methylation variants could complement SNP profiling of metabolite diversity.Our study thus provides a DNA methylome map across diverse accessions and suggests that DNA methylation variation can be the genetic basis of metabolic diversity in plants.

关键词： DNA methylation domestication multi-omics mGWAS mEWAS metabolic diversity tomato

OsRLCK160 contributes to flavonoid accumulation and UV-B tolerance by regulating OsbZIP48 in rice

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Science China(Life Sciences) 2022年第7期65卷 1380-1394页

作者： Feng Zhang Jiacheng Huang Hao Guo Chenkun Yang Yufei Li Shuangqian Shen Chuansong Zhan Lianghuan Qu Xianqing Liu shouchuang wang Wei Chen Jie Luo National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research(Wuhan) Huazhong Agricultural UniversityWuhan 430070China College of Plant Science and Technology Huazhong Agricultural UniversityWuhan 430070China College of Tropical Crops Hainan UniversityHaikouHainan 570288China

Plants produce specialized metabolites to adapt to the ever-changing environments.Flavonoids are antioxidants essential for growth,development,and breeding with increased stress resistance in crops.However,the mechanism of the involvement of flavonoids in ultraviolet-B(UV-B)stress in rice(Oryza sativa)is largely unknown.In this study,we cloned and functionally identified a receptor-like kinase(OsRLCK160)and a bZIP transcription factor(OsbZIP48)positively regulating flavonoid accumulation through metabolite-based genome-wide association study of the flavonoid content in rice.Meanwhile,OsRLCK160 interacted with and phosphorylated OsbZIP48 to regulate the flavonoid accumulation and participate in UV-B tolerance in rice.Our study indicates the importance of applying OsRLCK160 and OsbZIP48 to advance the fundamental understanding of stable rice production and breed UV-B-tolerant rice varieties,which may contribute to breeding high-yield rice varieties.

关键词： flavonoids natural variation Oryza sativa receptor-like kinase transcription factor UV-B tolerance

Elucidation of the melitidin biosynthesis pathway in pummelo

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Journal of Integrative Plant Biology 2023年第11期65卷 2505-2518页

作者： Shuangqian Shen shouchuang wang Chenkun Yang Chao wang Qianqian Zhou Shen Zhou Ran Zhang Yufei Li Zixuan wang Liupan Dai Wenjv Peng Yingchen Hao Hao Guo Guangping Cao Xianqing Liu Fan Yao Qiang Xu Alisdair RFernie Jie Luo Sanya Nanfan Research Institute of Hainan University Hainan UniversitySanya 572025China National Key Laboratory of Crop Genetic Improvement National Center of Plant Gene Research(Wuhan)Huazhong Agricultural UniversityWuhan 430070China Hubei Hongshan Laboratory College of Life Science and TechnologyCollege of Biomedicine and HealthHuazhong Agricultural UniversityWuhan 430070China Key Laboratory of Horticultural Plant Biology of Ministry of Education Huazhong Agricultural UniversityWuhan 430070China Max Planck Institute of Molecular Plant Physiology Potsdam-Golm 14476Germany Centre of Plant Systems Biology and Biotechnology Plovdiv 4000Bulgaria Yazhouwan National Laboratory Sanya 572025China

Specialized plant metabolism is a rich resource of compounds for drug discovery.The acylated flavonoid glycoside melitidin is being developed as an anti-cholesterol statin drug candidate,but its biosynthetic route in plants has not yet been fully characterized.Here,we describe the gene discovery and functional characterization of a new flavonoid gene cluster(UDP-glucuronosyltransferases(Cg UGTs),1,2rhamnosyltransferase(Cg1,2Rha T),acyltransferases(Cg ATs))that is responsible for melitidin biosynthesis in pummelo(Citrus grandis(L.)Osbeck).Population variation analysis indicated that the tailoring of acyltransferases,specific for bitter substrates,mainly determine the natural abundance of melitidin.Moreover,3-hydroxy-3-methylglutaryl-Co A reductase enzyme inhibition assays showed that the product from this metabolic gene cluster,melitidin,may be an effective anti-cholesterol statin drug candidate.Co-expression of these clustered genes in Nicotiana benthamiana resulted in the formation of melitidin,demonstrating the potential for metabolic engineering of melitidin in a heterologous plant system.This study establishes a biosynthetic pathway for melitidin,which provides genetic resources for the breeding and genetic improvement of pummelo aimed at fortifying the content of biologically active metabolites.

关键词： bioactive metabolites biosynthetic pathway flavonoids melitidin natural variation

Targeted approaches to improve tomato fruit taste

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Horticulture Research 2023年第1期10卷 57-68页

作者： shouchuang wang Qi Qiang Lijun Xiang Alisdair R.Fernie Jun Yang Sanya Nanfan Research Institute of Hainan University Hainan Yazhou Bay Seed LaboratorySanya572025China College of Tropical Crops Hainan UniversityHaikou570228China Max Planck Institute of Molecular Plant Physiology Potsdam-Golm 14476Germany

Tomato(Solanum lycopersicum)is the most valuable fruit and horticultural crop species worldwide.Compared with the fruits of their progenitors,those of modern tomato cultivars are,however,often described as having unsatisfactory taste or lacking f lavor.The f lavor of a tomato fruit arises from a complex mix of tastes and volatile metabolites,including sugars,acids,amino acids,and various volatiles.However,considerable differences in fruit f lavor occur among tomato varieties,resulting in mixed consumer experiences.While tomato breeding has traditionally been driven by the desire for continual increases in yield and the introduction of traits that provide a long shelf-life,consumers are prepared to pay a reasonable premium for taste.Therefore,it is necessary to characterize preferences of tomato f lavor and to define its underlying genetic basis.Here,we review recent conceptual and technological advances that have rendered this more feasible,including multi-omics-based QTL and association analyses,along with the use of trained testing panels,and machine learning approaches.This review proposes how the comprehensive datasets compiled to date could allow a precise rational design of tomato germplasm resources with improved organoleptic quality for the future.

关键词： breeding cultivar render

The Structure and Function of Major Plant Metabolite Modifications

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Molecular Plant 2019年第7期12卷 899-919页

作者： shouchuang wang Saleh Alseekh Alisdair R.Fernie Jie Luo Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresource College of Tropical Crops Hainan University Haikou 572208 China Max Planck Institute of Molecular Plant Physiology Potsdam-Golm 14476 Germany Centre of Plant Systems Biology and Biotechnology Plovdiv 4000 Bulgaria National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan) Huazhong Agricultural University Wuhan 430070 China

Plants produce a myriad of structurally and functionally diverse metabolites that play many different roles in plant growth and development and in plant response to continually changing environmental conditions as well as abiotic and biotic stresses. This metabolic diversity is, to a large extent, due to chemical modification of the basic skeletons of metabolites. Here, we review the major known plant metabolite modifications and summarize the progress that has been achieved and the challenges we are facing in the field. We focus on discussing both technical and functional aspects in studying the influences that various modifications have on biosynthesis, degradation, transport, and storage of metabolites, as well as their bioactivity and toxicity. Finally, we discuss some emerging insights into the evolution of metabolic pathways and metabolite functionality.

关键词： metabolic diversity metabolite modification genetic basis evolution of metabolism

Rice metabolic regulatory network spanning the entire life cycle

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Molecular Plant 2022年第2期15卷 258-275页

作者： Chenkun Yang Shuangqian Shen Shen Zhou Yufei Li Yuyuan Mao Junjie Zhou Yuheng Shi Longxu An Qianqian Zhou Wenju Peng Yuanyuan Lyu Xuemei Liu Wei Chen shouchuang wang Lianghuan Qu Xianqing Liu Alisdair R.Fernie Jie Luo National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research(Wuhan) Huazhong Agricultural UniversityWuhan 430070China College of Tropical Crops Hainan UniversityHaikou 570228China Sanya Nanfan Research Institute of Hainan University Hainan Yazhou Bay Seed LaboratorySanya 572025China College of Plant Science and Technology Huazhong Agricultural UniversityWuhan 430070China Max Planck Institute of Molecular Plant Physiology Potsdam-Golm 14476Germany Centre of Plant Systems Biology and Biotechnology Plovdiv 4000Bulgaria

As one of the most important crops in the world,rice(Oryza sativa)is a model plant for metabolome research.Although many studies have focused on the analysis of specific tissues,the changes in metab-olite abundance across the entire life cycle have not yet been determined.In this study,combining both tar-geted and nontargeted metabolite profiling methods,a total of 825 annotated metabolites were quantified in rice samples from different tissues covering the entire life cycle.The contents of metabolites in different tissues of rice were significantly different,with various metabolites accumulating in the plumule and radicle during seed germination.Combining these data with transcriptome data obtained from the same time period,we constructed the Rice Metabolic Regulation Network.The metabolites and co-expressed genes were further divided into 12 clusters according to their accumulation patterns,with members within each cluster displaying a uniform and clear pattern of abundance across development.Using this dataset,we established a comprehensive metabolic profile of the rice life cycle and used two independent strategies to identify novel transcription factors-namely the use of known regulatory genes as bait to screen for new networks underlying lignin metabolism and the unbiased identification of new glycerophospholipid metabolism regulators on the basis of tissue specificity.This study thus demonstrates how guilt-by-association analysis of metabolome and transcriptome data spanning the entire life cycle in cereal crops provides novel resources and tools to aid in understanding the mechanisms underlying important agro-nomic traits.

关键词： rice metabolome transcriptome transcription factor co-expression glycerophospholipid

Control of Leaf Senescence by an MeOH- Jasmonates Cascade that Is Epigenetically Regulated by OsSRT1 in Rice

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Molecular Plant 2016年第10期9卷 1366-1378页

作者： ChuanYing Fang Hua Zhang Jian Wan YangYang Wu Kang Li Cheng Jin Wei Chen shouchuang wang WenSheng wang HaiWei Zhang Pan Zhang Fei Zhang LiangHuan Qu Xianqing Liu Dao-Xiu Zhou Jie Luo National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan) Huazhong Agricultural University Wuhan 430070China Institute for Nutritional Sciences Shanghai Institutes for Biological Sciences Chinese Academy of Sciences University of Chinese Academy of Sciences Shanghai200031 China College of Life Science and Technology Huazhong Agricultural University Wuhan 430070 China Institute of Plant Sciences Paris-Saclay Universite Paris-sud 11 Orsay 91405 France

Although considerable progress has been made in identifying the genes regulating accumulation of hormones that are involved in leaf senescence, only a few studies have focused on natural variations in jasmonates content and much less on the underlying genetic basis. Moreover, the epigenetic regulation of jasmonate-mediated leaf senescence remains largely unknown, in this study, we carried out metabolic profiling of a worldwide collection of rice accessions and demonstrated that there are substantial variations in jasmonate levels among these accessions. A subsequent metabolite-based genornewide association study identified candidates for two major quantitative genes （QTGs）, OsPME1 and OsTSD2, affecting the content of jasmonates. Further investigations using a series of relevant mutants and transgenic lines revealed the MeOH-jasmonata cascade plays an important role in regulating leaf senescence. Moreover, we showed that OsSRT1, one of the two Sir2 （silent information regugator 2） homologs in rice, negatively regulates leaf senescence by repressing expression of the biosynthetic genes of this metabolic cascade and at least particiaUy through histone H3K9 deacetylation of OsPME1. Taken together, our results indicate that the MeOH-jasmonates cascade and its epigenetic regulation are crucial for controlling leaf senescence process in rice.

关键词： MeOH-jasmonate cascade leaf senescence natural variation epigenetic regulation

Manipulation of SlMXl for enhanced carotenoids accumulation and drought resistance in tomato

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Science Bulletin 2016年第18期61卷 1413-1418页

作者： Mohamed Ewas Yanqiang Gao shouchuang wang Xianqing Liu Hongyan Zhang Elsayed M. E. Nishawy Farhan Aii Raheel Shahzad Khurram Ziaf Hizar Subthain Cathie Martin Jie Luo National Key Laboratory of Crop Genetic Improvement andNational Center of Plant Gene Research (Wuhan) Huazhong Agricultural University Wuhan 430070 China College of Life Science and Technology Huazhong Agricultural University Wuhan 430070 China Key Laboratory of Horticultural Plant Biology Ministry of Education Huazhong Agricultural University Wuhan 430070China John Innes Centre Norwich Research Park Colney Norwich NR4 7UH UK

Plants are the ultimate source of nutrients in the human diet. To ensure adequate availability of high quality food for an increasing world population, traits including improved tolerance of stresses and nutrient levels need to be selected in crops, both individually and in combination. Here we report the identification of Sl MX1 encoding a MIXTA-like MYB transcription factor in tomato that simultaneously modulates drought resistance and metabolic processes through regulating key structural and regulatory genes of the corresponding pathways. Over-expression of Sl MX1 results in substantially increased drought tolerance and improved fruit quality, while knocking down Sl MX1 resulted in the opposite phenotypes. Our study indicates an effective way with multiple beneficial traits by genetic engineering of a single regulatory gene and can be a novel approach to breeding crops.

关键词：抗旱性类胡萝卜素番茄 MYB转录因子操纵积累果实品质世界人口