Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (12): 2753-2770    DOI: 10.1016/S2095-3119(19)62818-2
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Evolution of the R2R3-MYB gene family in six Rosaceae species and expression in woodland strawberry
LIU Hui1, XIONG Jin-song1, JIANG Yue-ting1, WANG Li1, CHENG Zong-ming (Max)1, 2 
1 College of Horticulture, Nanjing Agricultural University, Nanjing 210095, P.R.China
2 Department of Plant Sciences, University of Tennessee, Knoxville 37996, USA
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
R2R3-MYB gene family play important roles in plants development, metabolism, and responses to various biotic and abiotic stresses.  In this study, 838 R2R3-MYB genes were identified from six Rosaceae species, including 105 in woodland strawberry (Fragaria vesca), 173 in European pear (Pyrus communis), 219 in apple (Malus domestica), 121 in peach (Prunus persica), 121 in Chinese rose (Rosa chinensis), and 99 in black raspberry (Rubus occidentalis).  All R2R3-MYB genes in the six Rosaceae species were clustered into 51 species-specific duplicated clades with 109 genes and 50 lineage-specific duplicated clades with 242 genes according to phylogenetic analysis.  R2R3-MYB genes were distributed on all chromosomes in each of the six species, with a small amount of tandem duplication events.  The proportion of tandem repeat genes ranged from 0 to 25.1%.  The R2R3-MYB protein was conserved in a clade and likely to share similar functions.  The distribution of Ks showed the duplication times of R2R3-MYB genes in six Rosaceae species.  Furthermore, most of the R2R3-MYB genes had Ka/Ks values less than 1, which indicated they were driven by purifying selection during the evolutionary processes.  The GO term enrichment analysis revealed that R2R3-MYB genes in strawberry and black raspberry were more divergent than in other Rosaceae species.  Analysis of transcriptomes of 42 different tissues and development stages of woodland strawberry showed that high expression levels of R2R3-MYB suggested that the R2R3-MYB genes in strawberry played a key role in growth and development of both vegetative tissues and fruits.  The strawberry R2R3-MYB genes in sub-group of S1, S2, S11, S20, and S22 had high expression levels both in young leaves (YL) and old leaves (OL) strawberry tissues under drought treatments.
Keywords:  R2R3-MYB gene        Rosaceae species        duplication events  
Received: 06 June 2019   Accepted:
Fund: This study was supported by the Fundamental Research Funds for the Central Universities, China (SYSB201804) and partly supported by the open funds of the State Key Laboratory of Crop Genetics and Germplasm Enhancement, China (ZW201813).
Corresponding Authors:  Correspondence CHENG Zong-ming (Max), E-mail: zmc@njau.edu.cn   
About author:  LIU Hui, E-mail: 2017204003@njau.edu.cn;

Cite this article: 

LIU Hui, XIONG Jin-song, JIANG Yue-ting, WANG Li, CHENG Zong-ming (Max). 2019. Evolution of the R2R3-MYB gene family in six Rosaceae species and expression in woodland strawberry. Journal of Integrative Agriculture, 18(12): 2753-2770.

Ambawat S, Sharma P, Yadav N R, Yadav R C. 2013. MYB transcription factor genes as regulators for plant responses: An overview. Physiology and Molecular Biology of Plants, 19, 307–321.
Amoutzias G D, Veron AS, Weiner J, Robinson-Rechavi M, Bornberg-Bauer E, Oliver S G, Robertson D L. 2007. One billion years of bZIP transcription factor evolution: Conservation and change in dimerization and DNA-binding site specificity. Molecular Biology and Evolution, 24, 827–835.
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.
Cao Y P, Han Y H, Li D H, Lin Y, Cai Y P. 2016. MYB transcription factors in Chinese pear (Pyrus bretschneideri Rehd.): Genome-wide identification, classification, and expression profiling during fruit development. Frontiers in Plant Science, 7, 577.
Cao Z H, Zhang S Z, Wang R K, Zhang R F, Hao Y J. 2013. Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS ONE, 8, e69955.
Crooks G E, Hon G, Chandonia J M, Brenner S E. 2004. WebLogo: A sequence logo generator. Genome Research, 14, 1188–1190.
Darwish O, Shahan R, Liu Z, Slovin J P, Alkharouf N W. 2015. Re-annotation of the woodland strawberry (Fragaria vesca) genome. BMC Genomics, 16, 29.
Du H, Feng B R, Yang S S, Huang Y B, Tang Y X. 2012a. The R2R3-MYB transcription factor gene family in maize. PLoS ONE, 7, e37463.
Du H, Yang S S, Liang Z, Feng B R, Liu L, Huang Y B, Tang Y X. 2012b. Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biology, 12, 106.
Du H, Zhang L, Liu L, Tang X F, Yang W J, Wu Y M, Huang Y B, Tang Y X. 2009. Biochemical and molecular characterization of plant MYB transcription factor family. Biochemistry (Moscow), 74, 1–11.
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends in Plant Science, 15, 573–581.
Feller A, Machemer K, Braun E L, Grotewold E. 2011. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. The Plant Journal, 66, 94–116.
Galis I, Simek P, Narisawa T, Sasaki M, Horiguchi T, Fukuda H, Matsuoka K. 2006. A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. The Plant Journal, 46, 573–592.
Gao J J, Zhang Z, Peng R H, Xiong A S, Xu J, Zhu B, Yao Q H. 2011. Forced expression of Mdmyb10, a myb transcription factor gene from apple, enhances tolerance to osmotic stress in transgenic Arabidopsis. Molecular Biology Reports, 38, 205–211.
Gonzalez A, Zhao M, Leavitt J M, Lloyd A M. 2008. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal, 53, 814–827.
Hajiebrahimi A, Owji H, Hemmati S. 2017. Genome-wide identification, functional prediction, and evolutionary analysis of the R2R3-MYB superfamily in Brassica napus. Genome, 60, 797–814.
Himmelreich R, Hilbert H, Plagens H, Pirkl E, Li B C, Herrmann R. 1996. Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Research, 24, 4420–4449.
Hurst L D. 2002. The Ka/Ks ratio: Diagnosing the form of sequence evolution. Trends in Genetics, 18, 486.
Ignazio V, Abbott A G, Simone S, Sook J, Sheng Q S, Fabio M, Tatyana Z, Maria T D, Jane G, Federica C, Andrea Z, Laura R, Jerry J, Elisa V, Lee A M, Veronique D, Bryon S, Simon P, Therese M, Alberto P, et al. 2013. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics, 45, 487–494.
Jin H L, Martin C. 1999. Multifunctionality and diversity within the plant MYB-gene family. Plant Molecular Biology, 41, 577–585.
Kanei-Ishii C, Sarai A, Sawazaki T, Nakagoshi H, He D N, Ogata K, Nishimura Y, Ishii S. 1990. The tryptophan cluster: A hypothetical structure of the DNA-binding domain of the myb protooncogene product. Journal of Biological Chemistry, 265, 19990–19995.
Kang C Y, Omar D, Aviva G, Rachel S, Nadim A, Liu Z C. 2013. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. The Plant Cell, 25, 1960–1978.
Katiyar A, Smita S, Lenka S K, Rajwanshi R, Chinnusamy V, Bansal K C. 2012. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics, 13, 544.
Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
Kaul S, Koo H L, Jenkins J, Rizzo M, Rooney T, Tallon L J, Feldblyum T, Nierman W, Benito M I, Lin X Y, Town C D, Venter J C, Fraser C M, Tabata S, Nakamura Y, Kaneko T, Sato S, Asamizu E, Kato T, Kotani H, Sasamoto S, et al. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796–815.
Klenk H P, Clayton R A, Tomb J F, White O, Nelson K E, Ketchum K A, Dodson R J, Gwinn M, Hickey E K, Peterson J D, Richardson D L, Kerlavage A R, Graham D E, Kyrpides N C, Fleischmann R D, Quackenbush J, Lee N H, Sutton G G, Gill S, Kirkness E F, et al. 1997. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature, 390, 364–370.
Kousuke H, Cheng Z, Lehti-Shiu M D, Kazuo S, 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.
Kranz H D, Denekamp M, Greco R, Jin H, Leyva A, Meissner R C, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B. 1998. Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. The Plant Journal, 16, 263–276.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Larkin M A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.
Li C N, Ng C K Y, Fan L M. 2015. MYB transcription factors, active players in abiotic stress signaling. Environmental and Experimental Botany, 114, 80–91.
Li W H, Gu Z L, Wang H D, Nekrutenko A. 2001. Evolutionary analyses of the human genome. Nature, 409, 847–849.
Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T K, Espley R V, Hellens R P, Allan A C. 2010. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology, 10, doi: 10.1186/1471-2229-10-50
Liu C, Wang X, Xu Y, Deng X, Xu Q. 2014. Genome-wide analysis of the R2R3-MYB transcription factor gene family in sweet orange (Citrus sinensis). Molecular Biology Reports, 41, 6769–6785.
Liu C, Xie T, Chen C, Luan A, Long J, Li C, Ding Y, He Y. 2017. Genome-wide organization and expression profiling of the R2R3-MYB transcription factor family in pineapple (Ananas comosus). BMC Genomics, 18, 503.
Liu H, Zhong Y, Guo C, Wang X L, Xiong J, Cheng Q, Cheng Z M. 2017. Genome-wide analysis and evolution of the bZIP transcription factor gene family in six Fragaria species. Plant Systematics and Evolution, 303, 1225–1237.
Liu J Y, Osbourn A, Ma P D. 2015. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Molecular Plant, 8, 689–708.
Longhi S, Giongo L, Buti M, Surbanovski N, Viola R, Velasco R, Ward J A, Sargent D J. 2014. Molecular genetics and genomics of the Rosoideae: State of the art and future perspectives. Horticulture Research, 1, 1.
Martin C, Paz-Ares J. 1997. MYB transcription factors in plants. Trends in Genetics, 13, 67–73.
Matus J T, Aquea F, Arce-Johnson P. 2008. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biology, 8, doi: 10.1186/1471-2229-8-83
Medina-Puche L, Molina-Hidalgo FJ, Boersma M, Schuurink R C, Lopez-Vidriero I, Solano R, Franco-Zorrilla J M, Caballero J L, Blanco-Portales R, Munoz-Blanco J. 2015. An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruit receptacles. Plant Physiology, 168, 598–614.
Millar A A, Gubler F. 2005. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. The Plant Cell, 17, 705–721.
Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, Nishimura Y. 1992. Solution structure of a DNA-binding unit of Myb: A helix–turn–helix-related motif with conserved tryptophans forming a hydrophobic core. Proceedings of the National Academy of Sciences of the United States of America, 89, 6428–6432.
Ogata K, Morikawa S, Nakamura H, Hojo H, Yoshimura S, Zhang R H, Aimoto S, Ametani Y, Hirata Z, Sarai A, Ishii S, Nishimura Y. 1995. Comparison of the free and DNA-complexed forms of the DNA-binding domain from c-Myb. Nature Structural Biology, 2, 309–320.
Peterson G I, Masel J. 2009. Quantitative prediction of molecular clock and Ka/Ks at short timescales. Molecular Biology and Evolution, 26, 2595–2603.
Price M N, Dehal P S, Arkin A P. 2010. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, e9490.
Qin Y X, Wang M C, Tian Y C, He W X, Han L, Xia G M. 2012. Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Molecular Biology Reports, 39, 7183–7192.
Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J. 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Molecular Plant, 11, 414–428.
Riechmann J L, Heard J, Martin G, Reuber L, Jiang C Z, Keddie J, Adam L, Pineda O, Ratcliffe O J, Samaha R R, Creelman R, Pilgrim M, Broun P, Zhang J Z, Ghandehari D, Sherman B K, Yu C L. 2000. Arabidopsis transcription factors: Genome-wide comparative analysis among eukaryotes. Science, 290, 2105–2110.
Song S K, Ryu K H, Kang Y H, Song J H, Cho Y H, Yoo S D, Schiefelbein J, Lee M M. 2011. Cell fate in the arabidopsis root epidermis is determined by competition between WEREWOLF and CAPRICE. Plant Physiology, 157, 1196–1208.
Stracke R, Ishihara H, Barsch G H A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. The Plant Journal, 50, 660–677.
Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology, 4, 447–456.
Tombuloglu H, Kekec G, Sakcali M S, Unver T. 2013. Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Molecular Genetics and Genomics, 288, 141–155.
VanBuren R, Bryant D, Bushakra J M, Vining K J, Edger P P, Rowley E R, Priest H D, Michael T P, Lyons E, Filichkin S A. 2016. The genome of black raspberry (Rubus occidentalis). The Plant Journal, 87, 535–547.
Wang L Q, Guo K, Li Y, Tu Y Y, Hu H Z, Wang B R, Cui X C, Peng L C. 2010. Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biology, 10, doi: 10.1186/1471-2229-10-282
Wang X C, Niu Q W, Teng C, Li C, Mu J Y, Chua N H, Zuo J R. 2009. Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Research, 19, 224–235.
Wei Y L, Li J N, Lu J, Tang Z L, Pu D C, Chai Y R. 2007. Molecular cloning of Brassica napus TRANSPARENT TESTA 2 gene family encoding potential MYB regulatory proteins of proanthocyanidin biosynthesis. Molecular Biology Reports, 34, 105–120.
Wilkins O, Nahal H, Foong J, Provart N J, Campbell M M. 2009. Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiology, 149, 981–993.
Yang A, Dai X Y, Zhang W H. 2012. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. Journal of Experimental Botany, 63, 2541–2556.
Zhang C H, Ma R J, Xu J L, Yan J, Guo L, Song J, Feng R C, Yu M L. 2018. Genome-wide identification and classification of MYB superfamily genes in peach. PLoS ONE, 13, doi: 10.1371/journal.pone.0199192
Zhang L C, Zhao G Y, Jia J Z, Liu X, Kong X Y. 2012. Molecular characterization of 60 isolated wheat MYB genes and analysis of their expression during abiotic stress. Journal of Experimental Botany, 63, 203–214.
Zhu K, Wang X, Liu J, Tang J, Cheng Q, Chen J G, Cheng Z M M. 2018. The grapevine kinome: Annotation, classification and expression patterns in developmental processes and stress responses. Horticulture Research, 5, 19.
Zhu K K, Chen F, Liu J Y, Chen X L, Hewezi T, Cheng Z M. 2016. Evolution of an intron-poor cluster of the CIPK gene family and expression in response to drought stress in soybean. Scientific Reports, 6, doi: 10.1038/srep28225
No related articles found!
No Suggested Reading articles found!