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Quantitative trait loci identification reveals zinc finger protein CONSTANS-LIKE 4 as the key candidate gene of stigma color in watermelon(Citrullus lanatus)

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Journal of Integrative Agriculture 2024年第7期23卷 2292-2305页

作者： Shuang Pei Zexu Wu Ziqiao Ji Zheng Liu Zicheng Zhu Feishi Luan Shi Liu Key Laboratory of Biology and Genetic Improvement of Horticultural Crops(Northeast Region) Ministry of Agriculture and RuralAffairs/College of Horticulture and Landscape ArchitectureNortheast Agricultural UniversityHarbin 150030China Institute of Rural Revitalization Science and Technology Heilongjiang Academy of Agricultural SciencesHarbin 150028China

Stigma color is a critical agronomic trait in watermelon that plays an important role in pollination.However,there are few reports on the regulation of stigma color in watermelon.In this study,a genetic analysis of the F2 population derived from ZXG1553(P1,with orange stigma)and W1-17(P2,with yellow stigma)indicated that stigma color is a quantitative trait and the orange stigma is recessive compared with the yellow stigma.Bulk segregant analysis sequencing(BSA-seq)revealed a 3.75 Mb segment on chromosome 6 that is related to stigma color.Also,a major stable effective QTL Clqsc6.1(QTL stigma color)was detected in two years between cleaved amplified polymorphic sequencing(CAPS)markers Chr06_8338913 and Chr06_9344593 spanning a~1.01 Mb interval that harbors 51 annotated genes.Cla97C06G117020(annotated as zinc finger protein CONSTANS-LIKE 4)was identified as the best candidate gene for the stigma color trait through RNA-seq,quantitative real-time PCR(qRT-PCR),and gene structure alignment analysis among the natural watermelon panel.The expression level of Cla97C06G117020 in the orange stigma accession was lower than in the yellow stigma accessions with a significant difference.A nonsynonymous SNP site of the Cla97C06G117020 coding region that causes amino acid variation was related to the stigma color variation among nine watermelon accessions according to their re-sequencing data.Stigma color formation is often related to carotenoids,and we also found that the expression trend of ClCHYB(annotated asβ-carotene hydroxylase)in the carotenoid metabolic pathway was consistent with Cla97C06G117020,and it was expressed in low amounts in the orange stigma accession.These data indicated that Cla97C06G117020 and ClCHYB may interact to form the stigma color.This study provides a theoretical basis for gene fine mapping and mechanisms for the regulation of stigma color in watermelon.

关键词： watermelon stigma color gene mapping zinc finger protein CONSTANS-LIKE 4

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ClSnRK2.3 negatively regulates watermelon fruit ripening and sugar accumulation

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Journal of Integrative Plant Biology 2023年第10期65卷 2336-2348页

作者： Jinfang Wang Yanping Wang Yongtao Yu Jie Zhang Yi Ren Shouwei Tian Maoying Li Shengjin Liao Shaogui Guo Guoyi Gong Haiying Zhang Yong Xu State Key Laboratory of Vegetable Biobreeding National Engineering Research Center for VegetablesBeijing Key Laboratory of Vegetable Germplasms ImprovementBeijing Vegetable Research CenterBeijing Academy of Agriculture and Forestry ScienceBeijing 100097China

watermelon(Citrullus lanatus) as non-climacteric fruit is domesticated from the ancestors with inedible fruits. We previously revealed that the abscisic acid(ABA) signaling pathway gene ClSnRK2.3 might infuence watermelon fruit ripening. However,the molecular mechanisms are unclear. Here,we found that the selective variation of ClSnRK2.3 resulted in lower promoter activity and gene expression level in cultivated watermelons than ancestors, which indicated ClSnRK2.3 might be a negative regulator in fruit ripening. Overexpression (OE) of ClSnRK2.3 significantly delayed watermelon fruit ripening and suppressed the accumulation of sucrose, ABA and gibberellin GA4. Furthermore,we determined that the pyrophosphate-dependent phosphofructokinase(ClPFP1) in sugar metabolism pathway and GA biosynthesis enzyme GA20 oxidase(Cl GA20ox) could be phosphorylated by ClSnRK2.3 and thereby resulting in accelerated protein degradation in OE lines and finally led to low levels of sucrose and GA4. Besides that, ClSnRK2.3 phosphorylated homeodomain-leucine zipper protein(ClHAT1) and protected it from degradation to suppress the expression of the ABA biosynthesis gene 9’-cis-epoxycarotenoid dioxygenase 3(Cl NCED3). These results indicated that ClSnRK2.3 negatively regulated watermelon fruit ripening by manipulating the biosynthesis of sucrose, ABA and GA4. Altogether, these findings revealed a novel regulatory mechanism in non-climacteric fruit development and ripening.

关键词： fruit ripening SnRK2.3 sucrose watermelon

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A telomere-to-telomere gap-free reference genome of watermelon and its mutation library provide important resources for gene discovery and breeding

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Molecular Plant 2022年第8期15卷 1268-1284页

作者： Yun Deng Shoucheng Liu Yilin Zhang Jingsheng Tan Xiaopeng Li Xiao Chu Binghua Xu Yao Tian Yudong Sun Bosheng Li YunbiXu Xing Wang Deng Hang He Xingping Zhang Peking University Institute of Advanced Agricultural Sciences Shandong Laboratory of Advanced Agricultural Sciences at WeifangWeifangShandong 261000China School of Advanced Agricultural Sciences and School of Life Sciences State Key Laboratory of Protein and Plant Gene ResearchPeking UniversityBeijing 100871China Jiangsu Xuhuai Area Huaiyin Institute of Agricultural Science HuaianJiangsu 223300China

watermelon,Citrullus lanatus,is the world's third largest fruit crop.Reference genomes with gaps and a narrow genetic base hinder functional genomics and genetic improvement of watermelon.Here,we report the assembly of a telomere-to-telomere gap-free genome of the elite watermelon inbred line G42 by incorporating high-coverage and accurate long-read sequencing data with multiple assembly strategies.All 11 chromosomes have been assembled into single-contig pseudomolecules without gaps,representing the highest completeness and assembly quality to date.The G42 reference genome is 369321829 bp in length and contains 24205 predicted protein-coding genes,with all 22 telomeres and 11 centromeres characterized.Furthermore,we established a pollen-EMS mutagenesis protocol and obtained over 200000M1 seeds from G42.In a sampling pool,48 monogenic phenotypic mutations,selected from 223M1and 78 M2 mutants with morphological changes,were confirmed.The average mutation density was 1 SNP/1.69Mband1 indel/4.55 Mb per M1 plant and 1SNP/1.08Mb and 1 indel/6.25 Mb per M2 plant.Taking advantage of the gap-free G42 genome,8039 mutations from 32 plants sampled from M1 and M2 families were identified with 100%accuracy,whereas only 25% of the randomly selected mutations identified using the 97103v2 reference genome could be confirmed.Using this library and the gap-free genome,two genes responsible for elongated fruit shape and male sterility(CiMs1)were identified,both caused by a single basechange from G to A.The validated gap-free genome and its EMS mutation library provide invaluable resources for functional genomics and genetic improvement of watermelon.

关键词： watermelon gap-free genome EMS,mutation library gene discovery genome-wide sequencing genic male sterility

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Genetic relationship and pedigree of Chinese watermelon varieties based on diversity of perfect SNPs

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Horticultural Plant Journal 2022年第4期8卷 489-498页

作者： Jingjing Yang Jian Zhang Hushan Du Hong Zhao Aijun Mao Xiaofei Zhang Luo Jiang Haiying Zhang Changlong Wen Yong Xu Beijing Vegetable Research Center(BVRC) Beijing Academy of Agricultural and Forestry SciencesNational Engineering Research Center for VegetablesBeijing 100097China Key Laboratory of Biology and Genetics Improvement of Horticultural Crops(North China) MOARBeijing 100097China Beijing Key Laboratory of Vegetable Germplasms Improvement Beijing 100097China State Key Laboratory of Vegetable Germplasm Innovation Tianjin 300380China

watermelon(Citrullus lanatus)is one of the world’s most important fruit crops,and China produces the most watermelons in the world.Recently,a watermelon variome consisting of 414 key resequenced accessions was reported.However,the genetic relationships and pedigree of Chinese watermelon varieties in the seed market remain unclear.In this study,241 evenly distributed perfect single nucleotide polymorphisms(SNPs)derived from the watermelon variome were selected for variety identification.The diversity of 247 Chinese watermelon varieties was identified based on their SNP genotypes.The 247 watermelon varieties were clustered into five subpopulations:the East Asian ecotype,intermediate ecotype,small fruit with red flesh ecotype,small fruit with yellow flesh ecotype,and American ecotype.We further established the pedigree of four subpopulations,of which JingXinNo.1,ZaoChunHongYu,HuangXiaoYu and XiaoLan,and Sugarlee were the main doner of the East Asian ecotype,small fruit with red flesh ecotype,small fruit with yellow flesh ecotype,and American ecotype,respectively.Thirty-two core SNPs were selected and applied in watermelon variety identification.They were also validated by the Kompetitive allele-specific PCR(KASPar)platform.The present study furthered our understanding of the genetic relationships and pedigree of watermelon varieties in China,and will help to manage the plant variety protection in watermelon.

关键词： watermelon Perfect SNP Genetic relationship Pedigree Variety identification

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Development of branchless watermelon near isogenic lines by marker assisted selection

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Horticultural Plant Journal 2022年第5期8卷 627-636页

作者： Junling Dou Yinping Wang Huihui Yang Huanhuan Niu Dongming Liu Sen Yang Huayu Zhu Shouru Sun Luming Yang Henan Key Laboratory of Fruit and Cucurbit Biology College of HorticultureHenan Agricultural UniversityZhengzhou450002China

Pruning is time-consuming and laborious in watermelon cultivation,which can not meet the needs for simplified cultivation in the future.The development of branchless lines will provide important germplasms for breeding watermelon varieties and is an important method for genetic improvement.In this study,the watermelon accession,Wu Cha Zao(WCZ)is a branchless inbred line that carries the branchless gene Clbl,which was used as the donor parent to develop branchless near isogenic lines(NILs).To construct the NILs of Clbl,WCZ crossed with the normal branching watermelon inbred line WT20 which was used as the recurrent parent.The co-segregating markers dCAPS10 and Indel1 with Clbl were used for foreground selection,and a total of 108 SSR markers was selected with good polymorphism between two parental lines for background selection which had relatively uniform distribution across 11 chromosomes.Using these markers to select individuals from the BC_(1)F_(1),BC_(2)F_(1),and BC_(2)F_(2) generations,three NILs with a proportion of recurrent parent genome(PRPG)>99%were finally obtained.The lateral branch and plant height phenotypes did not significantly differ between the NILs and WCZ,indicating that the NILs of Clbl under the genetic background of WT20 has been successfully developed.These results provide ideal materials for further in-depth analysis of the genetic mechanisms of lateral branch development and ideal plant architecture breeding in watermelon.

关键词： watermelon Branchless Clbl Near isogenic lines Marker assisted selection

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Genome-wide analysis of nuclear factor Y genes and functional investigation of watermelon ClNF-YB9 during seed development

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作物学报:英文版 2023年第5期11卷 1469-1479页

作者： Qin Feng Ling Xiao Jiafa Wang Jie Wang Chenyang Chen Jianyang Sun Xixi Wu Man Liu Xian Zhang Shujuan Tian Li Yuan State Key Laboratory of Crop Stress Biology for Arid Areas College of HorticultureNorthwest A&F UniversityYangling 712100ShaanxiChina Shenzhen Research Institute Northwest A&F UniversityShenzhen 518000GuangdongChina

The nuclear factor Y(NF-Y) gene family is a class of transcription factors that are widely distributed in eukaryotes and are involved in various biological processes. However, the NF-Y gene family members in watermelon, a valued and nutritious fruit, remain largely unknown and their functions have not been characterized. In the present study, 22 ClNF-Y genes in watermelon, 29 CsNF-Y genes in cucumber, and 24CmNF-Y genes in melon were identified based on the whole-genome investigation and their protein properties, gene location, gene structure, motif composition, conserved domain, and evolutionary relationship were investigated. ClNF-YB9 from watermelon and its homologs in cucumber and melon were expressed specifically in seeds. Its expression remained low in the early stages of watermelon seed development,increased at 20 days after pollination(DAP), and peaked at 45–50 DAP. Moreover, the knockout mutant Clnf-yb9 exhibited abnormal leafy cotyledon phenotype, implying its critical role during seed formation.Finally, protein interaction assays showed that ClNF-YB9 interacts with all ClNF-YCs and the ClNF-YB9-YC4 heterodimer was able to recruit a ClNF-YA7 subunit to assemble a complete NF-Y complex, which may function in seed development. This study revealed the structure and evolutionary relationships of the NF-Y gene family in Cucurbitaceae and the novel function of ClNF-YB9 in regulating seed development in watermelon.

关键词： watermelon NF-Y gene family Evolution relationship ClNF-YB9 gene function Seed development

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Transcriptomic profiling of watermelon(Citrullus lanatus) provides insights into male flowers development

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Journal of Integrative Agriculture 2022年第2期21卷 407-421页

作者： ZHU Ying-chun YUAN Gao-peng JIA Sheng-feng AN Guo-lin LI Wei-hua SUN De-xi LIU Jun-pu Zhengzhou Fruit Research Institute Chinese Academy of Agricultural SciencesZhengzhou 450000P.R.China

watermelon(Citrullus lanatus(Thunb.) Matsum. & Nakai) is an important cucurbit crop grown worldwide. watermelon fruit quality, fertility, and seed-setting rate are closely related to male flower development. In this study, the different developmental stages of flower buds of the watermelon cultivar ’Xinteda Zhengkang 9’ were distinguished by cytological observation, and transcriptome sequencing analysis was performed subsequently. Acetocarmine staining of anthers was performed and the longitudinal and transverse diameters of the unopened male flower buds were measured. Cytological observations of anthers at different developmental stages showed that the anther grew from the tetrad to the mature stage, and the longitudinal and transverse diameters of the flower buds increased. The length of the male flower buds also changed significantly during development. Transcriptome sequencing analysis at four periods, the tetrad(A group), mononuclear(B group), dikaryophase(C group), and mature stages(D group). A total of 16 288 differentially expressed genes(DEGs) were detected in the four stages, with the prolongation of developmental stages, the number of DEGs increased gradually in the comparison groups, there was 2 014, 3 259, 4 628, 1 490, 3 495 and 1 132 DEGs revealed in six comparison groups(A-vs.-B, A-vs.-C, A-vs.-D, B-vs.-C, B-vs.-D, and C-vs.-D), respectively. Gene Ontology(GO) and KEGG enrichment analysis showed that the DEGs were mainly enriched in cellular component and starch and sucrose metabolism, phenylpropanoid biosynthesis and pentose sugar, etc. Finally, we completely screened 59 DEGs in the six comparison groups, interestingly, we found one pollen-specific protein(Cla001608) that was significantly down-regulated(the value of log2 Fold Change up to 17.32), which indicated that it may play an important role in the development of male flowers. This work provides insight into the molecular basis of the developmental stages of male flowers in watermelon and may aid in dominant cross breeding.

关键词： watermelon male flowers development cytological observation transcriptome sequencing

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Gold-based lateral-flow strip for the detection of penconazole in watermelon and cucumber samples

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Food Quality and Safety 2022年第2期6卷 257-264页

作者： Yang Liu Xinxin Xu Liqiang Liu Liguang Xu Hua Kuang Chuanlai Xu State Key Laboratory of Food Science and Technology Jiangnan UniversityWuxiChina International Joint Research Laboratory for Biointerface and Biodetection School of Food Science and TechnologyJiangnan UniversityWuxiChina

As a typical triazole fungicide,penconazole(PEN)is widely used in agriculture but has been proven to be toxic.In this study,we designed a new hapten to prepare a highly sensitive and specific anti-PEN monoclonal antibody(mAb)and established a gold nanoparticle-based lateral-flow immunoassay(LFIA)for the detection of PEN residues in watermelon and cucumber.The 50%inhibitory concentration(IC_(50))of the mAb was 0.42 ng/mL and the LFIA strip had a visual limit of detection(vLOD)of 2.5 ng/g and a cut-off value of 10 ng/g in watermelon and cucumbers.The calculated limit of detection(LOD)of the LFIA strip was 0.36 ng/g for watermelon and 0.29 ng/g for cucumber.The LFIA strip also gave a re-covery rate of 92.5%-109.0%for watermelon samples and 92.5%-106.7%for cucumber samples.These results using the LFIA strip are highly consistent with those seen using liquid chromatography-tandem mass spectrometry.Thus our developed LFIA strip represents a potentially reliable tool for the rapid on-site screening for PEN in watermelons and cucumbers.

关键词： Penconazole monoclonal antibody lateral flow immunoassay watermelon cucumber

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Genome-wide identification and expression analysis of NIN-like Protein(NLP)genes reveals their potential roles in the response to nitrate signaling in watermelon

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Horticultural Plant Journal 2022年第5期8卷 602-614页

作者： Gaopeng Yuan Dexi Sun Yifan Wang Guolin An Weihua Li Wenjing Si Junpu Liu Yingchun Zhu Zhengzhou Fruit Research Institute of the Chinese Academy of Agricultural Sciences Zhengzhou 450000China

To balance the relationship between high yield and low nitrogen supply,the nitrogen utilization efficiency of watermelon needs to be improved urgently.Nodule inception-like Protein(NLP)transcription factors play a key node role in nitrate response and growth and development of plant,however,comprehensive analysis of the NLP gene family in watermelon is unclear.This study explored the functional classification,evolutionary characteristics,and expression profile of the ClNLP gene family.Three ClNLPs were categorized into three groups according to their gene structure and phylogeny.All of them contained the conserved RWP-RK and PB1 domains.Evolutionary analysis of ClNLPs revealed that ClNLP1 and ClNLP3 underwent strong purified selection.In addition,cis-acting elements related to plant hormones and abiotic stresses were present in the ClNLP promoter.According to tissue-specific analysis ClNLP was widely expressed in roots,stems,leaves,flowers and fruits,and ClNLP1 was significantly induced in the roots of different nitrogen utilization varieties under different nitrate nitrogen supply.The SRTING functional protein association network suggested that ClNLP1 is associated with most genes,such as NRT1.1,NRT2.1,NIA1,and NIR1,and the dual-luciferase reporter assay found that ClNLP1 positively regulates the expression of ClNRT2.1.We speculated that ClNLP1 might play a central role in regulating the response of watermelon to nitrate nitrogen.

关键词： Genome-wide identification NLP Nitrate signaling Nitrate nitrogen watermelon

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Drought-induced proline is mainly synthesized in leaves and transported to roots in watermelon under water deficit

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Horticultural Plant Journal 2022年第5期8卷 615-626页

作者： Zhongyuan Wang Yongchao Yang Vivek Yadav Wei Zhao Yaping He Xian Zhang Chunhua Wei College of Horticulture State Key Laboratory of Crop Stress Biology in Arid AreasNorthwest A&F UniversityYangling 712100ShaanxiChina College of Biological and Agricultural Sciences Honghe UniversityMengzi 661100YunnanChina State Key Laboratory of Vegetable Germplasm Innovation Tianjin Kernel Agricultural Corporation LtdTianjin 300384China

Proline accumulation has been shown to occur in plants in response to various environmental stresses.Although proline metabolismrelated genes have been functionally characterized,the inter-organ transport of proline in stressed plants remains unclear.In this study,free proline was detected with significant accumulations in the roots,stems,and leaves of watermelon drought-tolerant germplasm M08 and drought-susceptible line Y34 under drought stress.Expression profiling and enzyme activity measurements revealed that ClP5CS1 gene,rather than its paralog ClP5CS2,mainly contributes to the proline synthesis in leaves via the Glu pathway.Additionally,over-expression of the ClP5CS genes significantly enhanced the drought tolerance of transgenic Arabidopsis lines.Furthermore,we confirmed that proline is mainly synthesized in leaves and transported to roots in watermelon under drought stress.Transcriptome and expression analyses revealed that the genes involved in proline metabolism exhibited different expression levels.Specifically,ClP5CS1 was upregulated in leaves and roots,while ClP5CS2 was downregulated under drought stress.Also,415 and 362 differently expressed TFs were identified in roots and leaves,respectively,with the majority upregulated in the former.Ultimately,a model for proline metabolism was proposed.The findings of this study provided new insights into the biosynthesis,transport,and regulatory mechanism of drought-induced proline in plants.

关键词： watermelon Drought stress Proline Inter-organ transport

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