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Rapid evolution of T2/S-RNase genes in fragaria linked to multiple transitions from self-incompatibility to self-compatibility

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Plant Diversity 2023年第2期45卷 219-228页

作者： Wu Chen Hong Wan Fang Liu Haiyuan Du Chengjun Zhang Weishu Fan Andan Zhu Germplasm Bank of Wild Species Kunming Institute of BotanyChinese Academy of SciencesKunmingYunnan 650201China University of Chinese Academy of Sciences Beijing 100049China Horticultural Research Institute Yunnan Academy of Agricultural SciencesKunmingYunnan 650205China

The T2/RNase gene family is widespread in eukaryotes,and particular members of this family play critical roles in the gametophytic self-incompatibility(GSI) system in plants.Wild diploid strawberry(fragaria)species have diversified their sexual systems via self-incompatible and self-compatible traits,yet how these traits evolved in fragaria remains elusive.By integrating the published and de novo assembled genomes and the newly generated RNA-seq data,members of the RNase T2 gene family were systematically identified in six fragaria species,including three self-incompatible species(fragaria nipponica,fragaria nubicola,and fragaria viridis) and three self-compatible species(fragaria nilgerrensis,fragaria vesca,and fragaria iinumae).In total,115 RNase T2 genes were identified in the six fragaria genomes and can be classified into three classes(Ⅰ-Ⅲ) according to phylogenetic analysis.The identified RNase T2 genes could be divided into 22 homologous gene sets according to amino acid sequence similarity and phylogenetic and syntenic relationships.We found that extensive gene loss and pseudogenization coupled with small-scale duplications mainly accounted for variations in the RNase T2 gene numbers in fragaria.Multiple copies of homologous genes were mainly generated from tandem and segmental duplication events.Furthermore,we newly identified five S-RNase genes in three self-incompatible fragaria genomes,including two in F.nipponica,two in F.viridis,and one in F.nubicola,which fit for typical features of a pistil determinant,including highly pistil-specific expression,highly polymorphic proteins and alkaline isoelectric point(pI),while no S-RNase genes were found in all three selfcompatible fragaria species.Surprisingly,these T2/S-RNase genes contain at least one large intron(>10 kb).This study revealed that the rapid evolution of T2/S-RNase genes within the fragaria genus could be associated with its sexual mode,and repeated evolution of the self-compatible traits in fragaria was convergent via losses of S-RNase.

关键词： fragaria RNase T2 Self-(in)compatibility S-RNase

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The telomere-to-telomere genome of fragaria vesca reveals the genomic evolution of fragaria and the origin of cultivated octoploid strawberry

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Horticulture Research 2023年第4期10卷 101-109页

作者： Yuhan Zhou Jinsong Xiong Ziqiang Shu Chao Dong Tingting Gu Pengchuan Sun Shuang He Mian Jiang Zhiqiang Xia Jiayu Xue Wasi Ullah Khan Fei Chen Zong-Ming Cheng College of Horticulture Nanjing Agricultural UniversityNanjing 210095China Hainan Yazhou Bay Seed Laboratory Sanya 572024China Wuhan Benagen Tech Solutions Company Limited WuhanHubei 430021China Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education&State Key Laboratory of Hydraulics&Mountain River Engineering College of Life SciencesSichuan UniversityChengdu 610065China College of Tropical Crops Hainan UniversityHaikou 570228China Sanya Nanfan Research Institute from Hainan University Sanya 572025China

fragaria vesca,commonly known as wild or woodland strawberry,is the most widely distributed diploid fragaria species and is native to Europe and Asia.Because of its small plant size,low heterozygosity,and relative ease of genetic transformation,F.vesca has been a model plant for fruit research since the publication of its Illumina-based genome in 2011.However,its genomic contribution to octoploid cultivated strawberry remains a long-standing question.Here,we de novo assembled and annotated a telomere-to-telomere,gap-free genome of F.vesca‘Hawaii 4’,with all seven chromosomes assembled into single contigs,providing the highest completeness and assembly quality to date.The gap-free genome is 220785082 bp in length and encodes 36173 protein-coding gene models,including 1153 newly annotated genes.All 14 telomeres and seven centromeres were annotated within the seven chromosomes.Among the three previously recognized wild diploid strawberry ancestors,F.vesca,F.iinumae,and F.viridis,phylogenomic analysis showed that F.vesca and F.viridis are the ancestors of the cultivated octoploid strawberry F.×ananassa,and F.vesca is its closest relative.Three subgenomes of F.×ananassa belong to the F.vesca group,and one is sister to F.viridis.We anticipate that this high-quality,telomere-to-telomere,gap-free F.vesca genome,combined with our phylogenomic inference of the origin of cultivated strawberry,will provide insight into the genomic evolution of fragaria and facilitate strawberry genetics and molecular breeding.

关键词： straw fragaria origin

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Molecular characteristics of S-RNase alleles as the determ inant of self-i ncompatibility in the style of fragaria viridi

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Horticulture Research 2021年第1期8卷 2456-2473页

作者： Jianke Du Chunfeng Ge Tingting Li Sanhong Wang Zhihong Gao Hidenori Sassa Yushan Qiao Laboratory of Fruit Crop Biotechnology College of HorticultureNanjing Agricultural UniversityNanjing 210095 JiangsuChina Laboratory of Genetics and Plant Breeding Graduate School of HorticultureChiba UniversityMatsudo 271-8510 ChibaJapan Present address:Institute of Botany Jiangsu Province and Chinese Academy of SciencesNanjing 210014 JiangsuChina

Strawberry(fragaria spp.)is a member of the Rosoideae subfamily in the family Rosaceae.The self-incompatibility(SI)of some diploid species is a key agronomic trait that acts as a basic pollination barrier;however,the genetic mechanism underlying SI control in strawberry remains unclear.Two candidate S-RNases(S a-and S^-RNase)identi fi ed in the transcriptome of the styles of the self-incompatible fragaria viridis 42 were con fi rmed to be SI determinants at the S locus following genotype identi fi cation and intraspeci fi c hybridization using sel fi ng progenies.Whole-genome collinearity and RNase T2 family analysis revealed that only an S locus exists in fragaria;however,none of the compatible species contained S-RNase.Although the results of interspeci fi c hybridization experiments showed that F.viridis(SI)styles could accept pollen from F.mandshurica(self-compatible),the reciprocal cross was incompatible.S a and S b-RNase contain large introns,and their noncoding sequences(promotors and introns)can be transcribed into long noncoding RNAs(lncRNAs).Overall,the genus fragaria exhibits S-RNase-based gametophytic SI,and S-RNase loss occurs at the S locus of compatible germplasms.In addition,a type of SI-independent unilateral incompatibility exists between compatible and incompatible fragaria species.Furthermore,the large introns and neighboring lncRNAs in S-RNase in fragaria could offer clues about S-RNase expression strategies.

关键词： fragaria spp alleles

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A pentaploid-based linkage map of the ancestral octoploid strawberry fragaria virginiana reveals instances of sporadic hyper-recombination

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Horticulture Research 2020年第1期7卷 1796-1810页

作者： Thomas M.Davis Yilong Yang Lise L.Mahoney Daniel C.Frailey Department of Agriculture Nutritionand Food SystemsUniversity of New HampshireDurhamNH 03824USA

The first high-resolution genetic linkage map of the ancestral octoploid(2n=8x=56)strawberry species,fragaria virginiana,was constructed using segregation data obtained from a pentaploid progeny population.This novel mapping population of size 178 was generated by crossing highly heterozygous F.virginiana hybrid“LB48”as a paternal parent with diploid(2n=2x=14)fragaria vesca“Hawaii 4”.The LB48 linkage map comprises 6055 markers genotyped on the Axiom®IStraw90 strawberry SNP array.The map consists of 28 linkage groups(LGs)organized into seven homoeology groups of four LGs each,and excludes a small 29th LG of undefined homoeology.One member of each homoeology group was assignable to an“A”subgenome associated with ancestral diploid fragaria vesca,while no other subgenomes were defined.Despite an intriguing discrepancy within homoeology group VI,synteny comparisons with the previously published fragaria×ananassa DA×MO linkage map revealed substantial agreement.Following initial map construction,examination of crossover distributions revealed that six of the total 5162(=29 chromosomes/individual×178 individuals)chromosomes making up the data set exhibited abnormally high crossover counts,ranging from 15 to 48 crossovers per chromosome,as compared with the overall mean of 0.66 crossovers per chromosome.Each of these six hyper-recombinant(HypR)chromosomes occurred in a different LG and in a different individual.When calculated upon exclusion of the six HypR chromosomes,the canonical(i.e.,broadly representative)LB48 map had 1851 loci distributed over a total map length of 1873 cM,while their inclusion increased the number of loci by 130,and the overall map length by 91 cM.Discovery of these hyper-recombinant chromosomes points to the existence of a sporadically acting mechanism that,if identified and manipulable,could be usefully harnessed for multiple purposes by geneticists and breeders.

关键词： fragaria straw linkage

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Genome-wide identification and expression analysis of auxin response factor(ARF) gene family in strawberry(fragaria vesca)

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Journal of Integrative Agriculture 2019年第7期18卷 1587-1603页

作者： WANG Shao-xi SHI Feng-yan DONG Xiang-xiang LI Yu-xiang ZHANG Zhi-hong LI He College of Horticulture Shenyang Agricultural University/Liaoning Key Laboratory of Strawberry Breeding and Cultivation

Auxin signaling plays a significant role in the whole process of plant growth and development from embryogenesis to senescence.Auxin response factors(ARFs) are reported to regulate the expression of auxin response genes by binding to auxin response elements.ARF is the most critical transcription factor family which has been released in most species,but few reports in strawberry.In this study,the structure characterization of 12 FvARF genes in strawberry,their expression patterns at different development stages,different organizations,and different indole-3-acetic acid(IAA) treatments were analyzed.The expression of 12 FvARFs was found in all experiment tissues and showed almost the same trend during fruit development.All FvARFs respond to the treatment of IAA.Our study provides comprehensive information on ARF family in strawberry,including gene structures,chromosome locations,phylogenetic relationships and expression patterns.The information on FvARF genes paves the way for future research on strawberry ARF genes.

关键词： auxin auxin response factor fragaria vesca gene structure gene expression

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The sugar transporter system of strawberry:genome-wide identification and expression correlation with fruit soluble sugar-related traits in a fragaria×ananassa germplasm collection

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Horticulture Research 2020年第1期7卷 1303-1321页

作者： Hai-Ting Liu Ying Ji Ya Liu Shu-Hua Tian Qing-Hua Gao Xiao-Hua Zou Jing Yang Chao Dong Jia-Hui Tan Di-An Ni Ke Duan Shanghai Key Laboratory of Protected Horticultural Technology Forestry and Fruit Tree Research InstituteShanghai Academy of Agricultural Sciences(SAAS)Shanghai 201403China Ecological Technique and Engineering College Shanghai Institute of TechnologyShanghai 201418China Environmental Engineering College Suzhou Polytechnic Institute of AgricultureSuzhou 215008China

Sugar from plant photosynthesis is a basic requirement for life activities.Sugar transporters are the proteins that mediate sugar allocation among or within source/sink organs.The transporters of the major facilitator superfamily(MFS)targeting carbohydrates represent the largest family of sugar transporters in many plants.Strawberry(fragaria×ananassa Duchesne)is an important crop appreciated worldwide for its unique fruit flavor.The involvement of MFS sugar transporters(STs)in cultivated strawberry fruit sugar accumulation is largely unknown.In this work,we characterized the genetic variation associated with fruit soluble sugars in a collection including 154 varieties.Then,a total of 67 ST genes were identified in the v4.0 genome integrated with the v4.0.a2 protein database of F.vesca,the dominant subgenome provider for modern cultivated strawberry.Phylogenetic analysis updated the nomenclature of strawberry ST homoeologs.Both the chromosomal distribution and structural characteristics of the ST family were improved.Semi-RT-PCR analysis in nine tissues from cv.Benihoppe screened 34 highly expressed ST genes in fruits.In three varieties with dramatically differing fruit sugar levels,qPCR integrated with correlation analysis between ST transcript abundance and sugar content identified 13 sugar-correlated genes.The correlations were re-evaluated across 19 varieties,including major commercial cultivars grown in China.Finally,a model of the contribution of the sugar transporter system to subcellular sugar allocation in strawberry fruits was proposed.Our work highlights the involvement of STs in controlling strawberry fruit soluble sugars and provides candidates for the future functional study of STs in strawberry development and responses and a new approach for strawberry genetic engineering and molecular breeding.

关键词： straw fragaria Sugar

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Assembly and annotation of fragaria vesca‘Yellow Wonder'genome,a model diploid strawberry for molecular genetic research

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Fruit Research 2022年第1期2卷 124-128页

作者： Dirk Joldersma Norah Sadowski Winston Timp Zhongchi Liu Department of Cell Biology and Molecular Genetics University of MarylandCollege ParkMD 20742USA Department of Biomedical Engineering Johns Hopkins UniversityBaltimoreMD 21218USA

fragaria vesca,a wild diploid strawberry,serves as a fundamental research model for cultivated strawberry.The current reference genomes available are limited to two closely-related accessions,Hawaii 4 and CFRA2339.The widely-used model accession‘Yellow Wonder'does not yet have its reference genome.In this study,the genome of a 7^(th) generation inbred'Yellow Wonder'was assembled using a combination of Oxford Nanopore long reads and Illumina short reads.The de novo chromosome-scale assembly of this 220 megabase genome possesses 34,007 genes which were annotated through lift over from the Hawaii 4 genome annotation.Genome comparisons show that the‘Yellow Wonder'genome is relatively distinct from the two previously published F.vesca accessions,Hawaii 4 and CFRA2339.The availability of a‘Yellow Wonder'reference genome adds another important genomic resource to fragaria vesca and enables rapid research progress in strawberry.

关键词： straw fragaria cultivated

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The complexity of the fragaria x ananassa(octoploid)transcriptome by singlemolecule long-read sequencing

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Horticulture Research 2019年第1期6卷 1206-1219页

作者： Huazhao Yuan Hongmei Yu Tao Huang Xinjie Shen Jin Xia Fuhua Pang Jing Wang Mizhen Zhao Institute of Pomology Jiangsu Academy of Agricultural Sciences/Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement210014 NanjingChina Biomarker Technologies Corporation 101300 BeijingChina Key Laboratory of Biology and Genetic Improvement of Oil Crops Ministry of Agriculture of People’s Republic of ChinaOil Crops Research InstituteChinese Academy of Agricultural Sciences430062 WuhanPeople’s Republic of China

Strawberry(fragaria x ananassa)is an allopolyploid species with diverse and complex transcripts.The regulatory mechanisms of fruit development and maturation have been extensively studied;however,little is known about the signaling mechanisms that direct this process in octoploid strawberry(fragaria x ananassa).Here,we used long-read sequencing(LRS)technology and RNA-seq analysis to investigate the diversity and complexity of the polyploid transcriptome and differentially expressed transcripts along four successive fruit developmental stages of cultivated strawberry.We obtained a reference transcriptome with 119,897 unique full-length isoforms,including 2017 new isoforms and 2510 long noncoding RNAs.Based on the genome of the plausible progenitor(fragaria vesca),20,229 alternative splicing(AS)events were identified.Using this transcriptome,we found 17,485 differentially expressed transcripts during strawberry fruit development,including 527 transcription factors(TFs)belonging to 41 families.The expression profiles of all members of the auxin,ABA pathway,and anthocyanin biosynthesis gene families were also examined,and many of them were highly expressed at the ripe fruit stage,strongly indicating that the role of those genes is in the regulation of fruit ripening.We produce a high-quality reference transcriptome for octoploid strawberry,including much of the full-length transcript diversity,to help understand the regulatory mechanisms of fruit development and maturation of polyploid species,particularly via elucidation of the biochemical pathways involved in auxin,ABA,and anthocyanin biosynthesis.

关键词： fragaria straw cultivated

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An effector-reporter system to study cellular signal transduction in strawberry fruit (fragaria ananassa)

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Horticulture Research 2021年第1期8卷 842-854页

作者： Baozhen Zeng Tianyu Li Wei Wang Zhengrong Dai Jie Li Zhiyuan Xi Kenan Jia Yu Xing Bingbing Li Jiaqi Yan Wensuo Jia College of Horticulture China Agricultural UniversityBeijing 100193China College of International Education Beijing University of Chemical TechnologyBeijing 100029China College of Plant Science and Technology Beijing University of AgricultureBeijing 102206China

An effector-reporter system is a powerful tool used to study cellular signal transduction,but this technique has been traditionally used in protoplasts.A similar system to study cellular signal transduction in fruits has not yet been established.In this study,we aimed to establish an effector–reporter system for strawberry fruit,a model nonclimacteric fruit.We first investigated the characteristics of transient gene expression in strawberry fruits and found marked variation in gene expression levels among individual fruits,and this variation has complicated the establishment of a technical system.To overcome this difficulty,we investigated a sampling strategy based on a statistical analysis of the activity pattern of four different reporters(GUS,GFP,FLuc,and RLuc)among individual fruits and combinations of pairs of reporters(GUS/GFP and RLuc/FLuc).Based on an optimized sampling strategy,we finally established a step-by step protocol for the effector/reporter assay.Using FaMYB10 and FaWRKY71 as the effectors and GUS driven by the FaCHS promoter as the reporter,we demonstrated that this effector/reporter system was practical and reliable.This effector/reporter technique will contribute to an in-depth exploration of the signaling mechanism for the regulation of strawberry fruit ripening.

关键词： straw fragaria system

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Updated annotation of the wild strawberry fragaria vesca V4 genome

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Horticulture Research 2019年第1期6卷 1056-1064页

作者： Yongping Li Mengting Pi Qi Gao Zhongchi Liu Chunying Kang Key Laboratory of Horticultural Plant Biology(Ministry of Education) College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhanHubei 430070China Department of Cell Biology and Molecular Genetics University of MarylandCollege ParkMD 20742USA

The diploid strawberry fragaria vesca serves as an ideal model plant for cultivated strawberry(fragaria×ananassa,8x)and the Rosaceae family.The F.vesca genome was initially published in 2011 using older technologies.Recently,a new and greatly improved F.vesca genome,designated V4,was published.However,the number of annotated genes is remarkably reduced in V4(28,588 genes)compared to the prior annotations(32,831 to 33,673 genes).Additionally,the annotation of V4(v4.0.a1)implements a new nomenclature for gene IDs(FvH4_XgXXXXX),rather than the previous nomenclature(geneXXXXX).Hence,further improvement of the V4 genome annotation and assigning gene expression levels under the new gene IDs with existing transcriptome data are necessary to facilitate the utility of this high-quality F.vesca genome V4.Here,we built a new and improved annotation,v4.0.a2,for F.vesca genome V4.The new annotation has a total of 34,007 gene models with 98.1%complete Benchmarking Universal Single-Copy Orthologs(BUSCOs).In this v4.0.a2 annotation,gene models of 8,342 existing genes are modified,9,029 new genes are added,and 10,176 genes possess alternatively spliced isoforms with an average of 1.90 transcripts per locus.Transcription factors/regulators and protein kinases are globally identified.Interestingly,the transcription factor family FAr-red-impaired Response 1(FAR1)contains 82 genes in v4.0.a2 but only two members in v4.0.a1.Additionally,the expression levels of all genes in the new annotation across a total of 46 different tissues and stages are provided.Finally,miRNAs and their targets are reanalyzed and presented.Altogether,this work provides an updated genome annotation of the F.vesca V4 genome as well as a comprehensive gene expression atlas with the new gene ID nomenclature,which will greatly facilitate gene functional studies in strawberry and other evolutionarily related plant species.

关键词： straw fragaria cultivated

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