Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (4): 1004-1014    DOI: 10.1016/S2095-3119(21)63698-5
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
The impact of tandem duplication on gene evolution in Solanaceae species
HUANG Yi-le1, 2, ZHANG Ling-kui2, ZHANG Kang2, CHEN Shu-min2, HU Jian-bin1, CHENG Feng2
1 College of Horticulture, Henan Agricultural University, Zhengzhou 450002, P.R.China
2 Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100097, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      

在植物基因组进化中普遍发生的全基因组加倍 (WGD) 和串联复制 (TD) 是基因扩增和功能创新的重要形式。我们分析了三个茄科物种 (番茄、辣椒和矮牵牛) 的基因组,这些茄科物种相对于与葡萄、可可和咖啡经历了一次额外的全基因组三倍化 (WGT) 事件。我们发现没有经历过这次WGT事件的葡萄比经历过WGT事件的茄科物种保留了相对更多和更长的串联复制基因簇 (TDG),并且发现较长TDG簇的形成往往来自于较古老的TD事件,这表明连续TD的基因(绝对剂量效应)在进化过程中长期积累。此外,茄科WGD和TD在基因保留的功能类别上表现出明显的偏向。WGD倾向于保留与生物过程有关的剂量敏感基因,包括DNA结合和转录因子活性等。TD倾向于保留参与逆境胁迫的绝对剂量基因。WGD和TD还通过基因融合和分裂为基因功能创新提供了更多途径。含有抗番茄镰刀菌枯萎病基因I3的TDG簇包含了15个串联重复基因,其中Solyc07g055560在串联重复事件后还经历了基因融合事件。这些结果为阐明TDG在适应环境变化中的新功能形成提供了依据。

Abstract  Whole genome duplication (WGD) and tandem duplication (TD) are important modes of gene amplification and functional innovation, and they are common in plant genome evolution.  We analyzed the genomes of three Solanaceae species (Solanum lycopersicum, Capsicum annuum, and Petunia inflata), which share a common distant ancestor with Vitis vinifera, Theobroma cacao, and Coffea canephora but have undergone an extra whole genome triplication (WGT) event.  The analysis was used to investigate the phenomenon of tandem gene evolution with (S. lycopersicum) or without WGT (V. vinifera).  Among the tandem gene arrays in these genomes, we found that V. vinifera, which has not experienced the WGT event, retained relatively more and larger tandem duplicated gene (TDG) clusters than the Solanaceae species that experienced the WGT event.  Larger TDG clusters tend to be derived from older TD events, so this indicates that continuous TDGs (absolute dosage) accumulated during long-term evolution.  In addition, WGD and TD show a significant bias in the functional categories of the genes retained.  WGD tends to retain dose-sensitive genes related to biological processes, including DNA-binding and transcription factor activity, while TD tends to retain genes involved in stress resistance.  WGD and TD also provide more possibilities for gene functional innovation through gene fusion and fission.  The TDG cluster containing the tomato fusarium wilt resistance gene I3 contains 15 genes, and one of these genes, Solyc07g055560, has undergone a fusion event after the duplication events.  These data provide evidence that helps explain the new functionalization of TDGs in adapting to environmental changes.  
Keywords:  tandem duplication       whole genome duplication        Solanaceae species        gene retention        gene fusion  
Received: 17 November 2020   Accepted: 07 April 2021
Fund: The work was supported by the National Natural Science Foundation of China (NSFC; 31972411 and 31722048), the Program for Scientific and Technological Innovative Talents in Universities of Henan Province, China (20HASTIT035), the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences, and the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, China.
About author:  Received 17 November, 2020 Accepted 7 April, 2021 Correspondence CHENG Feng, E-mail:; HU Jian-bin, E-mail:

Cite this article: 

HUANG Yi-le, ZHANG Ling-kui, ZHANG Kang, CHEN Shu-min, HU Jian-bin, CHENG Feng. 2022. The impact of tandem duplication on gene evolution in Solanaceae species. Journal of Integrative Agriculture, 21(4): 1004-1014.

Ajilogba C F, Babalola O O. 2013. Integrated management strategies for tomato Fusarium wilt. Biocontrol Science, 18, 117–127.
Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society (Series B: Methodological), 57, 289–300.
Birchler J A, Veitia R A. 2007. The gene balance hypothesis: From classical genetics to modern genomics. Plant Cell, 19, 395–402.
Birchler J A, Veitia R A. 2012. Gene balance hypothesis: Connecting issues of dosage sensitivity across biological disciplines. Proceedings of the National Academy of Sciences of the United States of America, 109, 14746–14753.
Blanc G, Wolfe K H. 2004a. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell, 16, 1679–1691.
Blanc G, Wolfe K H. 2004b. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell, 16, 1667–1678.
Bodt S D, Maere S, Peer Y V D. 2005. Genome duplication and the origin of angiosperms. Trends in Ecology & Evolution, 20, 591–597.
Bowers J E, Chapman B A, Rong J, Paterson A H. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature, 422, 433–438.
Caicedo A L, Richards C, Ehrenreich I M, Purugganan M D. 2009. Complex rearrangements lead to novel chimeric gene fusion polymorphisms at the Arabidopsis thaliana MAF2–5 flowering time gene cluster. Molecular Biology and Evolution, 26, 699–711.
Catanzariti A, Lim G, Jones D A. 2015. The tomato I-3 gene: A novel gene for resistance to Fusarium wilt disease. New Phytologist, 207, 106–118.
Cheng F, Wu J, Fang L, Wang X. 2012. Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Frontiers in Plant Science, 3, 198.
Denoeud F, Carretero-Paulet L, Dereeper A, Droc G, Guyot R, Pietrella M, Zheng C, Alberti A, Anthony F, Aprea G. 2014. The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science, 345, 1181–1184.
Fernandez-Pozo N, Menda N, Edwards J D, Saha S, Tecle I Y, Strickler S R, Bombarely A, Fisher-York T, Pujar A, Foerster H. 2015. The Sol Genomics Network (SGN) - from genotype to phenotype to breeding. Nucleic Acids Research, 43, D1036–D1041.
Freeling M. 2009. Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annual Review of Plant Biology, 60, 433–453.
Geng D L, Lu L Y, Yan M J, Shen X X, Jiang L J, Li H Y, Wang L P, Yan Y, Xu J D, Li C Y, Yu J T, Ma F W, Guan Q M. 2019. Physiological and transcriptomic analyses of roots from Malus sieversii under drought stress. Journal of Integrative Agriculture, 18, 1280–1294.
Goodstein D, Shu S, Howson R, Neupane R, Hayes R D, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N H. 2012. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Research, 40, 1178–1186.
Hanada K, Zou C, Lehti-Shiu M D, Shinozaki K, Shiu S H. 2008. Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiology, 148, 993–1003.
Innan H, Kondrashov F. 2010. The evolution of gene duplications: Classifying and distinguishing between models. Nature Reviews Genetics, 11, 97–108.
Jander G, Barth C. 2007. Tandem gene arrays : A challenge for functional genomics. Trends in Plant Science, 12, 203–210.
Joshi R K, Nayak S. 2013. Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants. Physiology and Molecular Biology of Plants, 19, 1–9.
Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.
Kaul S, Koo H L, Jenkins J, Rizzo M, Rooney T, Tallon L J, Feldblyum T, Nierman W, Benito M I, Lin X. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796–815.
Kliebenstein D J, Kroymann J, Brown P D, Figuth A, Pedersen D, Gershenzon J, Mitchellolds T. 2001. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiology, 126, 811–825.
Liu D, Yang L, Zhang J Z, Zhu G T, Lü H J, Lü Y Q, Wang Y L, Cao X, Sun T S, Huang S W, Wu Y Y. 2020. Domestication and breeding changed tomato fruit transcriptome. Journal of Integrative Agriculture, 19, 120–132.
Long M, Betrán E, Thornton K, Wang W. 2003. The origin of new genes: Glimpses from the young and old. Nature Reviews Genetics, 4, 865–875.
Loughran N B, O’Connell M J, O’Connor B, Ó’Fágáin C. 2014. Stability properties of an ancient plant peroxidase. Biochimie, 104, 156–159.
Lynch M, Conery J S. 2000. The evolutionary fate and consequences of duplicate genes. Science, 290, 1151–1155.
Maere S, Bodt S D, Raes J, Casneuf T, Montagu M V, Kuiper M, Peer Y V D. 2005. Modeling gene and genome duplications in eukaryotes. Proceedings of the National Academy of Sciences of the United States of America, 102, 5454–5459.
Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R. 2013. Gene duplication as a major force in evolution. Journal of Genetics, 92, 155–161.
Marchler-Bauer A, Bryant S H. 2004. CD-Search: Protein domain annotations on the fly. Nucleic Acids Research, 32, W327–W331.
Matsumoto T, Wu J, Kanamori H, Katayose Y, Fujisawa M, Namiki N, Mizuno H, Yamamoto K, Antonio B A, Baba T. 2005. The map-based sequence of the rice genome. Nature, 436, 793–800.
McDowell J M, Simon S A. 2006. Recent insights into R gene evolution. Molecular Plant Pathology, 7, 437–448.
Meng X, Zhang S. 2013. MAPK cascades in plant disease resistance signaling. Annual Review of Phytopathology, 51, 245–266.
Messing J, Bharti A K, Karlowski W M, Gundlach H, Kim H R, Yu Y, Wei F, Fuks G, Soderlund C, Mayer K F X. 2004. Sequence composition and genome organization of maize. Proceedings of the National Academy of Sciences of the United States of America, 101, 14349–14354.
Meyers B C, Shen K A, Rohani P, Gaut B S, Michelmore R W. 1998. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell, 10, 1833–1846.
Michelmore R W, Meyers B C. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Research, 8, 1113–1130.
Mindrebo J T, Nartey C M, Seto Y, Burkart M D, Noel J P. 2016. Unveiling the functional diversity of the alpha/beta hydrolase superfamily in the plant kingdom. Current Opinion in Structural Biology, 41, 233–246.
Ori N, Eshed Y, Paran I, Presting G, Aviv D, Tanksley S, Zamir D, Fluhr R. 1997. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell, 9, 521–532.
Panchy N, Lehti-Shiu M, Shiu S H. 2016. Evolution of gene duplication in plants. Plant Physiology, 171, 2294–2316.
Paterson A H, Freeling M, Tang H, Wang X. 2010. Insights from the comparison of plant genome sequences. Annual Review of Plant Biology, 61, 349–372.
Peer Y V D, Maere S, Meyer A. 2009. The evolutionary significance of ancient genome duplications. Nature Reviews Genetics, 10, 725–732.
Rizzon C, Ponger L, Gaut B S. 2006. Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Computational Biology, 2, e115.
Rojas-Gracia P, Roque E, Medina M, López-Martín M J, Cañas L A, Beltrán J P, Gómez-Mena C. 2019. The DOF transcription factor SlDOF10 regulates vascular tissue formation during ovary development in tomato. Frontiers in Plant Science, 10, 216.
Röth S, Mirus O, Bublak D, Scharf K D, Schleiff E. 2017. DNA-binding and repressor function are prerequisites for the turnover of the tomato heat stress transcription factor HsfB1. The Plant Journal, 89, 31–44.
Saha B, Borovskii G, Panda S K. 2016. Alternative oxidase and plant stress tolerance. Plant Signaling & Behavior, 11, e1256530.
Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S, Kaneko T, Nakamura Y, Shibata D, Aoki K. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635–641.
Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
Tuskan G A, Difazio S P, Jansson S, Bohlmann J, Grigoriev I V, Hellsten U, Putnam N H, Ralph S G, Rombauts S, Salamov A. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 313, 1596–1604.
Wang D, Zhang Y, Zhang Z, Zhu J, Yu J. 2010. KaKs_Calculator 2.0: A toolkit incorporating gamma-series methods and sliding window strategies. Genomics, Proteomics & Bioinformatics, 8, 77–80.
Wang Y F, Liao Y Q, Wang Y P, Yang J W, Zhang N, Si H J. 2020. Genome-wide identification and expression analysis of StPP2C gene family in response to multiple stresses in potato (Solanum tuberosum L.). Journal of Integrative Agriculture, 19, 1609–1624.
Wen J, Jiang F, Weng Y, Sun M, Shi X, Zhou Y, Yu L, Wu Z. 2019. Identification of heat-tolerance QTLs and high-temperature stress-responsive genes through conventional QTL mapping, QTL-seq and RNA-seq in tomato. BMC Plant Biology, 19, 398.
Yu G, Wang L G, Han Y, He Q Y. 2012. ClusterProfiler: An R package for comparing biological themes among gene clusters. OMICS: A Journal of Integrative Biology, 16, 284–287. 
Yu J, Tehrim S, Wang L, Dossa K, Zhang X, Ke T, Liao B. 2017. Evolutionary history and functional divergence of the cytochrome P450 gene superfamily between Arabidopsis thaliana and Brassica species uncover effects of whole genome and tandem duplications. BMC Genomics, 18, 733.
Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, Dai L. 2012. ParaAT: A parallel tool for constructing multiple protein-coding DNA alignments. Biochemical and Biophysical Research Communications, 419, 779–781.
Zhu H L, Zhu B Z, Li Y C, Shao Y, Wang X G, Xie Y H, Chen A J, Luo J J, Jia X Y, Luo Y B. 2008. Expression and DNA binding activity of the tomato transcription factor RIN (ripening inhibitor). Bioscience, Biotechnology, and Biochemistry, 72, 250–252.
No related articles found!
No Suggested Reading articles found!