Special Issue:
园艺-分子生物合辑Horticulture — Genetics · Breeding
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Genome-wide analysis of the invertase genes in strawberry (Fragaria×ananassa) |
YUAN Hua-zhao, PANG Fu-hua, CAI Wei-jian, CHEN Xiao-dong, ZHAO Mi-zhen, YU Hong-mei |
Institute of Pomology, Jiangsu Academy of Agricultural Sciences/Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210014, P.R.China
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摘要
本文对八倍体栽培草莓INV家族基因进行了全面的分析,包括基因结构、染色体定位、保守结构域、基因进化和果实发育过程中的表达谱。我们的研究表明,多倍体事件导致INVs基因在栽培草莓基因组中大量扩增(几乎是三倍或四倍),这些扩增的INVs基因在草莓果实中表现为显性表达。超过一半的INVs转录产物由于可变剪切导致产生较短的编码框,同时具备较低的表达水平。前人的研究表明,CWINVs参与糖分的韧皮部卸载和库强度的调节。FaCWINV1在果实发育过程中表达量明显上调,在成熟果实中强烈表达。总糖含量与FaCWINV1的表达水平有显著的相关性。这些结果表明,FaCWINV1可能参与草莓果实中糖份的积累。综上所述,我们的研究结果将有助于进一步研究INVs在果实成熟调控中的作用。
Abstract Sugar is an important material basis in fruit development, and strawberry fruit flavour and sweetness largely depend on the sugar content and variety. Invertases (INVs) play an important role in the regulation of sugar accumulation because they irreversibly catalyse the hydrolysis of sucrose into the corresponding nucleoside diphosphate-glucose, glucose or fructose in fruit. In this work, we provided a comprehensive analysis of the INV gene family in octoploid strawberry (Fragaria×ananassa), including the gene structure, chromosomal locations, conserved domains, and gene evolution and expression profiles during strawberry fruit development. Our study revealed that polyploid events resulted in the abundant amplification (almost three- or four-fold) of the INV gene in the F.×ananassa genome, and these amplified INV genes showed dominant expression in strawberry fruit. More than half of the FaINVs transcripts with low expression had incomplete coding sequences by alternative splicing. Previous studies have shown that cell wall invertases (CWINV) are involved in the regulation of phloem unloading and sink strength establishment. The expression of FaCWINV1 was markedly upregulated during fruit development and strongly expressed in ripe fruit. Moreover, a significant correlation was observed between the total sugar content and the FaCWINV1 expression level. These findings suggest that FaCWINV1 may be involved in sugar accumulation in strawberry fruit. Taken together, the results of our study will be beneficial for further research into the functions of INVs in the regulation of fruit ripening.
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Received: 09 April 2020
Accepted:
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Fund: This work was funded by the Major Project for Breeding?New Varieties of Jiangsu Province, China (PZCZ201721), the National Horticulture Germplasm Resources Center, China (NHGRC2020-NH16), and the National Crop Germplasm Resources Protection of the Ministry of Agriculture and Rural Affairs of China (19200361). |
Corresponding Authors:
Correspondence YU Hong-mei, Tel: +86-25-84390219, Fax: +86-25-84391695, E-mail: yhmjsxh@163.com
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About author: YUAN Hua-zhao, Tel: +86-25-84390219, E-mail: 544250348@qq.com; |
Cite this article:
YUAN Hua-zhao, PANG Fu-hua, CAI Wei-jian, CHEN Xiao-dong, ZHAO Mi-zhen, YU Hong-mei.
2021.
Genome-wide analysis of the invertase genes in strawberry (Fragaria×ananassa). Journal of Integrative Agriculture, 20(10): 2652-2665.
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Altschul S F. 1990. Basic local alignment search tool (BLAST). Journal of Molecular Biology, 215, 403–410.
An Y, Furber K L, Ji S. 2017. Pseudogenes regulate parental gene expression via ceRNA network. Journal of Cellular and Molecular Medicine, 21, 185–192.
Bhaskar P B, Wu L, Busse J S, Whitty B R, Hamernik A J, Jansky S H, Buell C R, Bethke P C, Jiang J. 2010. Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiology, 154, 939–948.
Cannon S B, Mitra A, Baumgarten A, Young N D, May G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology, 4, 10.
Chen Z, Gao K, Su X, Rao P, An X. 2015. Genome-wide identification of the invertase gene family in Populus. PLoS ONE, 10, e0138540.
Deng W, Wang Y, Liu Z, Cheng H, Xue Y. 2014. HemI: A toolkit for illustrating heatmaps. PLoS ONE, 9, 111988.
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 L, Wai C M, Alger E I, Bird K A, Yocca A E, Pumplin N, Ou S, Ben-Zvi G, Brodt A, Baruch K, Swale T, Shiue L, et al. 2019. Origin and evolution of the octoploid strawberry genome. Nature Genetics, 51, 541–547.
Foyer C H. 1987. The basis of source–sink interaction in leaves. Plant Physiology and Biochemistry, 25, 649–659.
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins M R, Appel R D, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: Walker J M, ed., The Proteomics Protocols Handbook. Humana Press, Germany. pp. 571–607.
Goel N K, Kumar V, Bhardwaj Y K, Sabharwal S. 2006. Gibberellin-dependent induction of tomato extracellular invertase Lin7 is required for pollen development. Functional Plant Biology, 33, 547–554.
Goetz M, Godt D E, Guivarc’h A, Kahmann U, Chriqui D, Roitsch T. 2001. Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proceedings of the National Academy of Sciences of the United States of America, 98, 6522–6527.
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.
Hu B, Jin J, Guo A Y, Zhang H, Luo J, Gao G. 2015. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31, 1296–1297.
Hummer K E, Hancock J F 2009. Strawberry genomics: botanical history, cultivation, traditional breeding, and new technologies. In: Folta K M, Gardiner S E, eds., Genetics and Genomics of Rosacease. Springer, New York, USA, pp. 413–435.
Iraqi D, Tremblay F M. 2001. Analysis of carbohydrate metabolism enzymes and cellular contents of sugars and proteins during spruce somatic embryogenesis suggests a regulatory role of exogenous sucrose in embryo development. Journal of Experimental Botany, 52, 2301–2311.
Ji X, Van den Ende W, Van Laere A, Cheng S, Bennett J. 2005. Structure, evolution, and expression of the two invertase gene families of rice. Journal of Molecular Evolution, 60, 615–634.
Jia H, Jiu S, Zhang C, Wang C, Tariq P, Liu Z, Wang B, Cui L, Fang J. 2016. Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress ripening transcription factor. Plant Biotechnology Journal, 14, 2045–2065.
Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y, Li X, Ding N, Li C, Ji W, Jia W. 2013. Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytologist, 198, 453–456.
Jia H F, Chai Y M, Li C L, Lu D, Luo J J, Qin L, Shen Y Y. 2011. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiology, 157, 188–199.
Klann E M, Hall B, Bennett A B. 1996. Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiology, 112, 1321–1330.
Koch K. 2004. Sucrose metabolism: Regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology, 7, 235–246.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549.
Langmead B, Salzberg S. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357–359.
Lemoine R, LaCamera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J L, Laloi M, Coutos-Thévenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M. 2013. Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in Plant Science, 4, 272.
Li K B. 2003. ClustalW-MPI: ClustalW analysis using distributed and parallel computing. Bioinformatics, 19, 1585–1586.
Li W H, Gojobori T, Nei M. 1981. Pseudogenes as a paradigm of neutral evolution. Nature, 292, 237–239.
Pelleschi S, Rocher J P, Prioul J L. 1997. Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell and Environment, 20, 493–503.
Proteggente A R, Pannala A S, Paganga G, Van Buren L, Wagner E, Wiseman S, Van De Put F, Dacombe C, Rice-Evans C A. 2009. The antioxidant activity of regularly consumed fruits and vegetables reflects their phenolic and vitamin C composition. Free Radical Research, 36, 217–233.
Roitsch T, Gonzalez M C. 2004. Function and regulation of plant invertases: Sweet sensations. Trends in Plant Science, 9, 606–613.
Rossouw D, Kossmann J, Botha F. 2010. Reduced neutral invertase activity in the culm tissues of transgenic sugarcane plants results in a decrease in respiration and sucrose cycling and an increase in the sucrose to hexose ratio. Functional Plant Biology, 37, 22–31.
Ruan Y L. 2014. Sucrose metabolism: Gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology, 65, 33–67.
Shen L B, Qin Y L, Qi Z Q, Niu Y, Liu Z J, Liu H H, Cao Z M, Yang Y. 2018. Genome-wide analysis, expression profile, and characterization of the acid invertase gene family in pepper. International Journal of Molecular Sciences, 20, 15–29.
Shen L B, Yao Y, He H, Qin Y L, Liu Z J, Liu W X, Qi Z Q, Yang L J, Cao Z M, Yang Y. 2018. Genome-wide identification, expression, and functional analysis of the alkaline/neutral invertase gene family in pepper. International Journal of Molecular Sciences, 19, 224.
Sherson S M, Alford H L, Forbes S M, Wallace G, Smith S M. 2003. Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. Journal of Experimental Botany, 54, 525–531.
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, Jiang J. 2007. Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics, 176, 2055–2067.
Sturm A. 1999. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiology, 121, 1–7.
Vargas W A, Salerno G L. 2010. The Cinderella story of sucrose hydrolysis: alkaline/neutral invertases from cyanobacteria to unforeseen roles in plant cytosol and organelles. Plant Science, 178, 1–8.
Wang L, Zheng Y, Ding S, Zhang Q, Chen Y, Zhang J. 2017. Molecular cloning, structure, phylogeny and expression analysis of the invertase gene family in sugarcane. BMC Plant Biology, 17, 109.
Yao Y, Geng M T, Wu X H, Liu J, Li R M, Hu X W, Guo J C. 2014. Genome-wide identification, 3D modeling, expression and enzymatic activity analysis of cell wall invertase gene family from cassava (Manihot esculenta crantz). International Journal of Molecular Sciences, 15, 7313–7331.
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 Z, Yu H M, Huang T, Shen X J, Xia J, Pang F H, Wang J, Zhao M Z. 2019. The complexity of the Fragaria×ananassa (octoploid) transcriptome by single-molecule long-read sequencing. Horticulture Research, 6, 63.
Zanor M I, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, Sulpice R, Zhou Y H, Fernie A R. 2009. RNA interference of LIN5 in tomato confirms its role in controlling brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology, 150, 1204–1218.
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