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Journal of Integrative Agriculture  2021, Vol. 20 Issue (6): 1540-1553    DOI: 10.1016/S2095-3119(20)63376-7
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
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The transcriptional landscape of cultivated strawberry (Fragaria×ananassa) and its diploid ancestor (Fragaria vesca) during fruit development
LI Yong-ping1, 2*, LIU Tian-jia3*, LUO Hui-feng4, LIU Sheng-cai1
1 Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China
2 School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong 999077, P.R.China
3 Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 999077, P.R.China
4 Institute of Horticulture, Hangzhou Academy of Agricultural Sciences, Hangzhou 310024, P.R.China
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摘要  

栽培草莓(Fragaria×ananassa)来自四个二倍体祖先:F. vescaF. viridisF .iinumaeF. nipponica。其中,F. vesca是栽培草莓最主要的亚基因组。目前,基因表达如何促进二倍体和八倍体草莓之间的果实发育过程中的差异的机制沿不清楚。在这里,我们对F. vescaF.×ananassa的转录组进行全面分析,以研究水果发育不同阶段的基因表达。通过二倍体和八倍体之间的成对比较,我们总共获得了3,741个(转色期)和3,960个(成熟期)差异表达的基因。类黄酮生物合成中涉及的基因在八倍体的转色阶段被显著上调,并且我们还通过加权共表达网络(WGCNA)分析发现了与几种类黄酮生物合成基因(包括FveMYB10FveMYB9/11FveRAP)相关的成熟果实特异性模块。此外,我们确定了八倍体和二倍体果实中的物种特异调控网络。值得注意的是,我们发现WAK和F-box基因分别在八倍体和二倍体果实中富集。总体而言,这项研究有助于阐明草莓的类黄酮生物合成和果实大小,这对栽培草莓的未来分子育种具有重要意义。




Abstract  
Cultivated strawberry (Fragaria×ananassa) originated from four diploid ancestors: F. vesca, F. viridis, F. iinumae and F. nipponica.  Among them, F. vesca is the dominant subgenome for cultivated strawberry.  It is not well understood how differences in gene expression between diploid and octoploid strawberry contribute to differences during fruit development.  In this study, we used comprehensive transcriptomic analyses of F. vesca and Fananassa to investigate gene expression at the different stages of fruit development.  In total, we obtained 3 508 (turning stage) and 3 958 (red stage) differentially expressed genes with pairwise comparisons between diploid and octoploid.  The genes involved in flavonoid biosynthesis were almost upregulated in the turning stages of octoploid, and we also discovered a ripe fruit-specific module associated with several flavonoid biosynthetic genes, including FveMYB10, FveMYB9/11, and FveRAP, using weighted gene coexpression network analysis (WGCNA).  Furthermore, we identified the species-specific regulated networks in the octoploid and diploid fruit.  Notably, we found that the WAK and F-box genes were enriched in the octoploid and diploid fruits, respectively.  This study elucidates new findings on flavonoid biosynthesis and fruit size of strawberry with important implications for future molecular breeding in cultivated strawberry. 
Keywords:  strawberry        Fragaria vesca        Fragaria×ananassa        RNA-Seq        fruit        development        anthocyanin  
Received: 04 March 2020   Accepted:
Fund: This work was supported by the Program for High-level University Construction of the Fujian Agriculture and Forestry University, China (612014028), the Natural Science Foundation of Fujian Province, China (2018J01700) and Rural Revitalization Service Team of Fujian Agriculture and Forestry University, China (11899170125).
Corresponding Authors:  Correspondence LIU Sheng-cai, E-mail: 1215698900@qq.com    
About author:  LI Yong-ping, E-mail: yplee614@163.com; * These authors contributed equally to this study.

Cite this article: 

LI Yong-ping, LIU Tian-jia, LUO Hui-feng, LIU Sheng-cai . 2021. The transcriptional landscape of cultivated strawberry (Fragaria×ananassa) and its diploid ancestor (Fragaria vesca) during fruit development. Journal of Integrative Agriculture, 20(6): 1540-1553.

Almeida J R, D’amico E, Preuss A, Carbone F, De Vos C R, Deiml B, Mourgues F, Perrotta G, Fischer T C, Bovy A G. 2007. Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria×ananassa). Archives of Biochemistry and Biophysics, 465, 61–71.
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. 2010. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proceedings of the National Academy of Sciences of the United States of America, 107, 9452–9457.
Buggs R J, Zhang L J, Miles N, Tate J A, Gao L, Wei W, Schnable P S, Barbazuk W B, Soltis P S, Soltis D E. 2011.Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Current Biology, 21, 551–556.
Campbell M A, Haas B J, Hamilton J P, Mount S M, Buell C R. 2006. Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics, 7, 1–17.
Carbone F, Preuss A, De Vos R C, D’amico E, Perrotta G, Bovy A G, Martens S, Rosati C. 2009. Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant, Cell & Environment, 32, 1117–1131.
Chen Z J, Ni Z F. 2006. Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays, 28, 240–262.
Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics, 6, 836–846.
Conesa A, Götz S J I. 2008. Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics, 2008, 619832.
Cosgrove D J. 1997. Relaxation in a high-stress environment: The molecular bases of extensible cell walls and cell enlargement. The Plant Cell, 9, 1031–1041.
Dobin A, Davis C A, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras T R. 2013. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15–21.
Edger P P, Poorten T J, Vanburen R, Hardigan M A, Colle M, Mckain M R, Smith R D, Teresi S J, Nelson A D, Wai C M. 2019. Origin and evolution of the octoploid strawberry genome. Nature Genetics, 51, 541–547.
Edger P P, Vanburen R, Colle M, Poorten T J, Wai C M, Niederhuth C E, Alger E I, Ou S, Acharya C B, Wang J, Callow P, Mckain M R, Shi J, Collier C, Xiong Z, Mower J P, Slovin J P, Hytonen T, Jiang N, Childs K L, et al. 2018. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. GigaScience, 7, 1–7.
Griesser M, Hoffmann T, Bellido M L, Rosati C, Fink B, Kurtzer R, Aharoni A, Munoz-Blanco J, Schwab W. 2008. Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit. Plant Physiology, 146, 1528–1539.
Gu T T, Jia S F, Huang X R, Wang L, Fu W M, Huo G T, Gan L J, Ding J, Li Y. 2019. Transcriptome and hormone analyses provide insights into hormonal regulation in strawberry ripening. Planta, 250, 145–162.
Halbwirth H, Puhl I, Haas U, Jezik K, Treutter D, Stich K. 2006. Two-phase flavonoid formation in developing strawberry (Fragaria×ananassa) fruit. Journal of Agricultural and Food Chemistry, 54, 1479–1485.
Hammond-Kosack K E, Jones J G D. 1996. Resistance gene-dependent plant defense responses. The Plant Cell, 8, 1773–1791.
Hancock Jr J, Bringhurst R. 1981. Evolution in California populations of diploid and octoploid Fragaria (Rosaceae): A comparison. American Journal of Botany, 68, 1.
Hawkins C, Caruana J, Li J, Zawora C, Darwish O, Wu J, Alkharouf N, Liu Z C. 2017. An eFP browser for visualizing strawberry fruit and flower transcriptomes. Horticulture Research, 4, 1–8.
Hegarty M J, Barker G L, Wilson I D, Abbott R J, Edwards K J, Hiscock S J. 2006. Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. Current Biology, 16, 1652–1659.
Jiao Y, Wickett N J, Ayyampalayam S, Chanderbali A S, Landherr L, Ralph P E, Tomsho L P, Hu Y, Liang H, Soltis P S. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature, 473, 97–100.
Kang C Y, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z C. 2013. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. The Plant Cell, 25, 1960–1978.
Kohorn B D. 2000. Plasma membrane-cell wall contacts. Plant Physiology, 124, 31–38.
Kohorn B D, Johansen S, Shishido A, Todorova T, Martinez R, Defeo E, Obregon P. 2009. Pectin activation of MAP kinase and gene expression is WAK2 dependent. The Plant Journal, 60, 974–982.
Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559–568.
Li Y P, Dai C, Hu C G, Liu Z C, Kang C Y. 2017. Global identification of alternative splicing via comparative analysis of SMRT- and Illumina-based RNA-seq in strawberry. The Plant Journal, 90, 164–176.
Li Y P, Pi M T, Gao Q, Liu Z C, Kang C Y. 2019. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Horticulture Research, 6, 1–9.
Liao Y, Smyth G K, Shi W. 2013. FeatureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923–930.
Lin Y X, Jiang L Y, Chen Q, Li Y L, Zhang Y T, Luo Y, Zhang Y, Sun B, Wang X R, Tang H R. 2018. Comparative transcriptome profiling analysis of red- and white-fleshed strawberry (Fragaria×ananassa) provides new insight into the regulation of the anthocyanin pathway. Plant and Cell Physiology, 59, 1844–1859.
Liston A, Cronn R, Ashman T L. 2014. Fragaria: A genus with deep historical roots and ripe for evolutionary and ecological insights. American Journal of Botany, 101, 1686–1699.
Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 1–21.
Luo H F, Dai C, Li Y P, Feng J, Liu Z C, Kang C Y. 2018. Reduced Anthocyanins in Petioles codes for a GST anthocyanin transporter that is essential for the foliage and fruit coloration in strawberry. Journal of Experimental Botany, 69, 2595–2608.
Matus J T, Aquea F, Espinoza C, Vega A, Cavallini E, Dal Santo S, Cañón P, De La Guardia A R H, Serrano J, Tornielli G B, Arce-Johnson P. 2014. Inspection of the grapevine BURP superfamily highlights an expansion of RD22 genes with distinctive expression features in berry development and ABA-mediated stress responses. PLoS ONE, 9, e110327.
Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco A, Caballero J L, Schwab W, Muñoz-Blanco J, Blanco-Portales R. 2013. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria×ananassa fruits. Journal of Experimental Botany, 65, 401–417.
Niknafs Y S, Pandian B, Iyer H K, Chinnaiyan A M, Iyer M K. 2017. TACO produces robust multisample transcriptome assemblies from RNA-seq. Nature Methods, 14, 68–79.
Pertea M, Pertea G M, Antonescu C M, Chang T C, Mendell J T, Salzberg S L. 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature biotechnology, 33, 290–295.
Pessina S, Pavan S, Catalano D, Gallotta A, Visser R G, Bai Y, Malnoy M, Schouten H J. 2014. Characterization of the MLO gene family in Rosaceae and gene expression analysis in Malus domestica. BMC Genomics, 15, 1–12.
Pillet J, Yu H W, Chambers A H, Whitaker V M, Folta K M. 2015. Identification of candidate flavonoid pathway genes using transcriptome correlation network analysis in ripe strawberry (Fragaria×ananassa) fruits. Journal of Experimental Botany, 66, 4455–4467.
Rousseau-Gueutin M, Gaston A, Aïnouche A, Aïnouche M L, Olbricht K, Staudt G, Richard L, Denoyes-Rothan B. 2009. Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): New insights from phylogenetic analyses of low-copy nuclear genes. Molecular Phylogenetics and Evolution, 51, 515–530.
Rousseau-Gueutin M, Lerceteau-Köhler E, Barrot L, Sargent D J, Monfort A, Simpson D, Arus P, Guérin G, Denoyes-Rothan B. 2008. Comparative genetic mapping between octoploid and diploid Fragaria species reveals a high level of colinearity between their genomes and the essentially disomic behavior of the cultivated octoploid strawberry. Genetics, 179, 2045–2060.
Saminathan T, Nimmakayala P, Manohar S, Malkaram S, Almeida A, Cantrell R, Tomason Y, Abburi L, Rahman M A, Vajja V G, Khachane A, Kumar B, Rajasimha H K, Levi A, Wehner T, Reddy U K. 2015. Differential gene expression and alternative splicing between diploid and tetraploid watermelon. Journal of Experimental Botany, 66, 1369–1385.
Sánchez-Sevilla J F, Vallarino J G, Osorio S, Bombarely A, Posé D, Merchante C, Botella M A, Amaya I, Valpuesta V J 2017. Gene expression atlas of fruit ripening and transcriptome assembly from RNA-seq data in octoploid strawberry (Fragaria×ananassa). Scientific Reports, 7, 13737.
Schaart J G, Dubos C, De La Fuente I R, Van Houwelingen A M, De Vos R C, Jonker H H, Xu W, Routaboul J M, Lepiniec L, Bovy A G. 2013. Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria×ananassa) fruits. New Phytologist, 197, 454–467.
Shen S, Park J W, Huang J, Dittmar K A, Lu Z X, Zhou Q, Carstens R P, Xing Y. 2012. MATS: A Bayesian framework for flexible detection of differential alternative splicing from RNA-Seq data. Nucleic Acids Research, 40, 8.
Slovin J P, Schmitt K, Folta K M. 2009. An inbred line of the diploid strawberry Fragaria vesca f. semperflorens for genomic and molecular genetic studies in the Rosaceae. Plant Methods, 5, e61.
Smoot M E, Ono K, Ruscheinski J, Wang P L, Ideker T J B. 2010. Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics, 27, 431–432.
Stupar R M, Bhaskar P B, Yandell B S, Rensink W A, Hart A L, Ouyang S, Veilleux R E, Busse J S, Erhardt R J, Buell C R. 2007. Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics, 176, 2055–2067.
Sun Y, Xiao H. 2015. Identification of alternative splicing events by RNA sequencing in early growth tomato fruits. BMC Genomics, 16, 948.
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller L A, Rhee S Y, Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal, 37, 914–939.
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D R, Pimentel H, Salzberg S L, Rinn J L, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7, 562–578.
Wang B, Tseng E, Regulski M, Clark T A, Hon T, Jiao Y P, Lu Z Y, Olson A, Stein J C, Ware D. 2016. Unveiling the complexity of the maize transcriptome by single-molecule long-read sequencing. Nature Communications, 7, 11708.
Xia R, Ye S, Liu Z R, Meyers B, Liu Z C. 2015. Novel and recently evolved miRNA clusters regulate expansive F-box gene networks through phasiRNAs in wild diploid strawberry. Plant Physiology, 15, 00253.
Yang C W, Zhao L, Zhang H K, Yang Z Z, Wang H, Wen S S, Zhang C Y, Rustgi S, Von Wettstein D, Liu B. 2014. Evolution of physiological responses to salt stress in hexaploid wheat. Proceedings of the National Academy of Sciences of the United States of America, 111, 11882–11887.
Yoo M J, Liu X, Pires J C, Soltis P S, Soltis D E. 2014. Nonadditive gene expression in polyploids. Annual Review of Genetics, 48, 485–517.
Yuan H, Yu H, Huang T, Shen X, Xia J, Pang F, Wang J, Zhao M. 2019. The complexity of the Fragaria×ananassa (octoploid) transcriptome by single-molecule long-read sequencing. Horticulture Research, 6, 46.
Zhang T Z, Hu Y, Jiang W K, Fang L, Guan X Y, Chen J D, Zhang J B, Saski C A, Scheffler B E, Stelly D M. 2015. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM–1) provides a resource for fiber improvement. Nature Biotechnology, 33, 531–542.
Zhou R C, Moshgabadi N, Adams K L J. 2011. Extensive changes to alternative splicing patterns following allopolyploidy in natural, resynthesized polyploids. Proceedings of the National Academy of Sciences of the United States of America, 108, 16122–16127.
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