Gene Duplication and Functional Diversification of MADS-Box Genes in Malus × domestica following WGD: Implications for Fruit Type and Floral Organ Evolution
Abstract
:1. Introduction
2. Results
2.1. The Expansion in the Number of MADS-Box Genes across Different Fruit Types Is Correlated with WGD in Rosaceae
2.2. The Retention of Duplicated Genes in Maleae following WGD and Subsequent Chromosome Rearrangement
2.3. Four MADS-Gene Orthologous Groups Are Expressed in Plant Tissues
2.4. The MADS18 Genes Derived from WGD in M. × domestica Have Undergone Differential Evolution
2.5. The MADS6 Genes Derived from Both WGD and Tandem Duplication in M. × domestica Exhibit Differential Evolution
3. Discussion
3.1. Changes in Chromosomes and Genes Following the WGD Event in Rosaceae
3.2. The Expansion of the MADS-Box Gene Family Is Associated with Different Fruit Types in Rosaceae
3.3. MADS18 and MADS6 Are Expanded through WGD and Gene Duplication
3.4. MADS18 and MADS6 Have Different Expression Levels in Apple Fruits at Different Stages and Different Flower Organs
4. Materials and Methods
4.1. Collection of Publicly Available Genomic and Transcriptome Data
4.2. Phylogenetic Analysis and Time Inference
4.3. GO Term Enrichment
4.4. Gene Family Expansion and Contraction
4.5. Collinearity and Sequence Similarity Analysis
4.6. Ancestral Chromosome Karyotype Reconstruction and Evolution
4.7. Analysis of WGD and Gene Duplication
4.8. Transcriptome Analysis
4.9. Conserved Domain Search and Protein Structure Prediction
4.10. Plant Material and qRT-PCR
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Ren, R.; Wang, H.; Guo, C.; Zhang, N.; Zeng, L.; Chen, Y.; Ma, H.; Qi, J. Widespread Whole Genome Duplications Contribute to Genome Complexity and Species Diversity in Angiosperms. Mol. Plant 2018, 11, 414–428. [Google Scholar] [CrossRef]
- Soltis, P.S.; Soltis, D.E. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 2016, 30, 159–165. [Google Scholar] [CrossRef] [PubMed]
- Adams, K.L.; Wendel, J.F. Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 2005, 8, 135–141. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Wu, S.; Chang, X.; Wang, X.; Zhao, Y.; Xia, Y.; Trigiano, R.N.; Jiao, Y.; Chen, F. The ancient wave of polyploidization events in flowering plants and their facilitated adaptation to environmental stress. Plant Cell Environ. 2020, 43, 2847–2856. [Google Scholar] [CrossRef]
- Jiao, Y.N.; Leebens-Mack, J.; Ayyampalayam, S.; Bowers, J.E.; McKain, M.R.; McNeal, J.; Rolf, M.; Ruzicka, D.R.; Wafula, E.; Wickett, N.J.; et al. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 2012, 13, R3. [Google Scholar] [CrossRef] [PubMed]
- Jiao, Y.N.; Li, J.P.; Tang, H.B.; Paterson, A.H. Integrated Syntenic and Phylogenomic Analyses Reveal an Ancient Genome Duplication in Monocots. Plant. Cell 2014, 26, 2792–2802. [Google Scholar] [CrossRef]
- Chen, Y.C.; Li, Z.; Zhao, Y.X.; Gao, M.; Wang, J.Y.; Liu, K.W.; Wang, X.; Wu, L.W.; Jiao, Y.L.; Xu, Z.L.; et al. The Litsea genome and the evolution of the laurel family. Nat. Commun. 2020, 11, 1675. [Google Scholar] [CrossRef]
- Zhang, L.S.; Chen, F.; Zhang, X.T.; Li, Z.; Zhao, Y.Y.; Lohaus, R.; Chang, X.J.; Dong, W.; Ho, S.; Liu, X.; et al. The water lily genome and the early evolution of flowering plants. Nature 2020, 577, 79. [Google Scholar] [CrossRef] [PubMed]
- Bowers, J.E.; Chapman, B.A.; Rong, J.; Paterson, A.H. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003, 422, 433–438. [Google Scholar] [CrossRef] [PubMed]
- Tuskan, G.A.; Difazio, S.; Jansson, S.; Bohlmann, J.; Grigoriev, I.; Hellsten, U.; Putnam, N.; Ralph, S.; Rombauts, S.; Salamov, A.; et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313, 1596–1604. [Google Scholar] [CrossRef]
- Schmutz, J.; Cannon, S.B.; Schlueter, J.; Ma, J.; Mitros, T.; Nelson, W.; Hyten, D.L.; Song, Q.; Thelen, J.J.; Cheng, J.; et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463, 178–183. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Qiao, Q.; Du, X.; Zhang, X.; Hou, Y.; Wei, X.; Sun, C.; Zhang, R.; Yun, Q.; Crabbe, M.J.C.; et al. Cultivated hawthorn (Crataegus pinnatifida var. major) genome sheds light on the evolution of Maleae (apple tribe). J. Integr. Plant Biol. 2022, 64, 1487–1501. [Google Scholar] [CrossRef] [PubMed]
- Potter, D.; Eriksson, T.; Evans, R.C.; Oh, S.; Smedmark, J.E.E.; Morgan, D.R.; Kerr, M.; Robertson, K.R.; Arsenault, M.; Dickinson, T.A.; et al. Phylogeny and classification of Rosaceae. Plant Syst. Evol. 2007, 266, 5–43. [Google Scholar] [CrossRef]
- Zhang, S.D.; Jin, J.J.; Chen, S.Y.; Chase, M.W.; Soltis, D.E.; Li, H.T.; Yang, J.B.; Li, D.Z.; Yi, T.S. Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics. New Phytol. 2017, 214, 1355–1367. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.; Ma, H.; Jung, S.; Main, D.; Guo, L. Developmental Mechanisms of Fleshy Fruit Diversity in Rosaceae. Annu. Rev. Plant Biol. 2020, 71, 547–573. [Google Scholar] [CrossRef] [PubMed]
- Xiang, Y.; Huang, C.; Hu, Y.; Wen, J.; Li, S.; Yi, T.; Chen, H.; Xiang, J.; Ma, H. Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication. Mol. Biol. Evol. 2017, 34, 262–281. [Google Scholar] [CrossRef] [PubMed]
- Xiang, Y.; Zhang, T.; Zhao, Y.; Dong, H.; Chen, H.; Hu, Y.; Huang, C.H.; Xiang, J.; Ma, H. Angiosperm-wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits. J. Integr. Plant Biol. 2024, 66, 228–251. [Google Scholar] [CrossRef]
- Su, W.B.; Zhu, Y.M.; Zhang, L.; Yang, X.H.; Gao, Y.S.; Lin, S.Q. The cellular physiology of loquat (Eriobotrya japonica Lindl.) fruit with a focus on how cell division and cell expansion processes contribute to pome morphogenesis. Sci. Hortic. 2017, 224, 142–149. [Google Scholar] [CrossRef]
- Daccord, N.; Celton, J.M.; Linsmith, G.; Becker, C.; Choisne, N.; Schijlen, E.; van de Geest, H.; Bianco, L.; Micheletti, D.; Velasco, R.; et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat. Genet. 2017, 49, 1099–1106. [Google Scholar] [CrossRef] [PubMed]
- Kang, C.Y.; Darwish, O.; Geretz, A.; Shahan, R.; Alkharouf, N.; Liu, Z.C. Genome-Scale Transcriptomic Insights into Early-Stage Fruit Development in Woodland Strawberry Fragaria vesca. Plant. Cell 2013, 25, 1960–1978. [Google Scholar] [CrossRef]
- Mezzetti, B.; Landi, L.; Pandolfini, T.; Spena, A. The defH9-iaaM auxin-synthesizing gene increases plant fecundity and fruit production in strawberry and raspberry. BMC Biotechnol. 2004, 4, 4. [Google Scholar] [CrossRef]
- Becker, A.; Theissen, G. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 2003, 29, 464–489. [Google Scholar] [CrossRef]
- Theißen, G.; Melzer, R.; Rümpler, F. MADS-domain transcription factors and the floral quartet model of flower development: Linking plant development and evolution. Development 2016, 143, 3259–3271. [Google Scholar] [CrossRef]
- Becker, A.; Kaufmann, K.; Freialdenhoven, A.; Vincent, C.; Li, M.A.; Saedler, H.; Theissen, G. A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol. Genet. Genom. 2002, 266, 942–950. [Google Scholar] [CrossRef] [PubMed]
- Bowman, J.L.; Smyth, D.R.; Meyerowitz, E.M. The ABC model of flower development: Then and now. Development 2012, 139, 4095–4098. [Google Scholar] [CrossRef] [PubMed]
- Causier, B.; Schwarz-Sommer, Z.; Davies, B. Floral organ identity: 20 years of ABCs. Semin. Cell Dev. Biol. 2010, 21, 73–79. [Google Scholar] [CrossRef] [PubMed]
- Theissen, G.; Melzer, R. Combinatorial Control of Floral Organ Identity by MADS-Domain Transcription Factors; Wiley: Hoboken, NJ, USA, 2006; pp. 253–265. [Google Scholar]
- Favaro, R.; Pinyopich, A.; Battaglia, R.; Kooiker, M.; Borghi, L.; Ditta, G.; Yanofsky, M.F.; Kater, M.M.; Colombo, L. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant. Cell 2003, 15, 2603–2611. [Google Scholar] [CrossRef]
- Pinyopich, A.; Ditta, G.S.; Savidge, B.; Liljegren, S.J.; Baumann, E.; Wisman, E.; Yanofsky, M.F. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 2003, 424, 85–88. [Google Scholar] [CrossRef]
- Battaglia, R.; Brambilla, V.; Colombo, L.; Stuitje, A.R.; Kater, M.M. Functional analysis of MADS-box genes controlling ovule development in Arabidopsis using the ethanol-inducible alc gene-expression system. Mech. Dev. 2006, 123, 267–276. [Google Scholar] [CrossRef]
- Laitinen, R.; Broholm, S.; Albert, V.A.; Teeri, T.H.; Elomaa, P. Patterns of MADS-box gene expression mark flower-type development in Gerbera hybrida (Asteraceae). BMC Plant Biol. 2006, 6, 11. [Google Scholar] [CrossRef]
- Eckardt, N.A. MADS monsters: Controlling floral organ identity. Plant. Cell 2003, 15, 803–805. [Google Scholar] [CrossRef]
- Gramzow, L.; Theissen, G. A hitchhiker’s guide to the MADS world of plants. Genome Biol. 2010, 11, 214. [Google Scholar] [CrossRef]
- Vekemans, D.; Proost, S.; Vanneste, K.; Coenen, H.; Viaene, T.; Ruelens, P.; Maere, S.; Van de Peer, Y.; Geuten, K. Gamma paleohexaploidy in the stem lineage of core eudicots: Significance for MADS-box gene and species diversification. Mol. Biol. Evol. 2012, 29, 3793–3806. [Google Scholar] [CrossRef] [PubMed]
- Tian, Y.; Dong, Q.; Ji, Z.; Chi, F.; Cong, P.; Zhou, Z. Genome-wide identification and analysis of the MADS-box gene family in apple. Gene 2015, 555, 277–290. [Google Scholar] [CrossRef]
- Meng, D.; Cao, Y.; Chen, T.; Abdullah, M.; Jin, Q.; Fan, H.; Lin, Y.; Cai, Y. Evolution and functional divergence of MADS-box genes in Pyrus. Sci. Rep. 2019, 9, 1266. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.; Zhu, G.; Zhao, H.; Liu, H.; Luo, Y.; Xu, W.; Huang, M.; Wu, Y.; Wang, L. Genome-wide Identification of MADS-box Gene Family and Expression Analysis in Prunus sibirica. Mol. Plant Breed. 2020, 18, 6575–6585. [Google Scholar]
- Wells, C.E.; Vendramin, E.; Tarodo, S.J.; Verde, I.; Bielenberg, D.G. A genome-wide analysis of MADS-box genes in peach [Prunus persica (L.) Batsch]. BMC Plant Biol. 2015, 15, 41. [Google Scholar] [CrossRef]
- Nie, C.R.; Xu, X.G.; Zhang, X.Q.; Xia, W.S.; Sun, H.B.; Li, N.; Ding, Z.Q.; Lv, Y.M. Genome-Wide Identified MADS-Box Genes in Prunus campanulata ‘Plena’ and Theirs Roles in Double-Flower Development. Plants 2023, 12, 3171. [Google Scholar] [CrossRef] [PubMed]
- Jung, S.; Cestaro, A.; Troggio, M.; Main, D.; Zheng, P.; Cho, I.; Folta, K.M.; Sosinski, B.; Abbott, A.; Celton, J.M.; et al. Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies. BMC Genom. 2012, 13, 129. [Google Scholar] [CrossRef] [PubMed]
- Wu, F.; Shi, X.; Lin, X.; Liu, Y.; Chong, K.; Theißen, G.; Meng, Z. The ABCs of flower development: Mutational analysis of AP1/FUL-like genes in rice provides evidence for a homeotic (A)-function in grasses. Plant J. 2017, 89, 310–324. [Google Scholar] [CrossRef]
- Chang, Y.Y.; Chiu, Y.F.; Wu, J.W.; Yang, C.H. Four orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS box genes show novel expression patterns and cause different effects on floral transition and formation in Arabidopsis thaliana. Plant Cell Physiol. 2009, 50, 1425–1438. [Google Scholar] [CrossRef]
- Velasco, R.; Zharkikh, A.; Affourtit, J.; Dhingra, A.; Cestaro, A.; Kalyanaraman, A.; Fontana, P.; Bhatnagar, S.K.; Troggio, M.; Pruss, D.; et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat. Genet. 2010, 42, 833–839. [Google Scholar] [CrossRef] [PubMed]
- Ibanez, A.M.; Dandekar, A.M. Apple. In Transgenic Crops V. Biotechnology in Agriculture and Forestry; Springer: Berlin/Heidelberg, Germany, 2007; pp. 241–282. [Google Scholar] [CrossRef]
- Shulaev, V.; Korban, S.S.; Sosinski, B.; Abbott, A.G.; Aldwinckle, H.S.; Folta, K.M.; Iezzoni, A.; Main, D.; Arus, P.; Dandekar, A.M.; et al. Multiple models for Rosaceae genomics. Plant Physiol. 2008, 147, 985–1003. [Google Scholar] [CrossRef] [PubMed]
- Lv, W.; Miao, D.; Miao, R.; Fan, D.; Meng, J.; Liu, X.; Cheng, T.; Zhang, Q.; Sun, L. Advances in the omics research of Rosaceae. Ornam. Plant Res. 2024, 4, e013. [Google Scholar] [CrossRef]
- Jung, S.; Lee, T.; Cheng, C.H.; Buble, K.; Zheng, P.; Yu, J.; Humann, J.; Ficklin, S.P.; Gasic, K.; Scott, K.; et al. 15 years of GDR: New data and functionality in the Genome Database for Rosaceae. Nucleic Acids. Res. 2019, 47, D1137–D1145. [Google Scholar] [CrossRef]
- Jacob, P.; Hirt, H.; Bendahmane, A. The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol. J. 2017, 15, 405–414. [Google Scholar] [CrossRef] [PubMed]
- Heimhofer, U.; Hochuli, P.A.; Burla, S.; Dinis, J.; Weissert, H. Timing of Early Cretaceous angiosperm diversification and possible links to major paleoenvironmental change. Geology 2005, 33, 141–144. [Google Scholar] [CrossRef]
- Nie, Y.; Guo, L.; Cui, F.; Shen, Y.; Ye, X.; Deng, D.; Wang, S.; Zhu, J.; Wu, W. Innovations and stepwise evolution of CBFs/DREB1s and their regulatory networks in angiosperms. J. Integr. Plant Biol. 2022, 64, 2111–2125. [Google Scholar] [CrossRef]
- Thomashow, M.F. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Biol. 1999, 50, 571–599. [Google Scholar] [CrossRef]
- Park, S.; Lee, C.M.; Doherty, C.J.; Gilmour, S.J.; Kim, Y.; Thomashow, M.F. Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. Plant J. 2015, 82, 193–207. [Google Scholar] [CrossRef]
- Chaudhury, A.M.; Craig, S.; Dennis, E.S.; Peacock, W.J. Ovule and embryo development, apomixis and fertilization. Curr. Opin. Plant Biol. 1998, 1, 26–31. [Google Scholar] [CrossRef] [PubMed]
- Tang, N.; Cao, Z.Y.; Wu, P.Y.; Zhang, X.; Lou, J.; Liu, Y.N.; Wang, Q.Y.; Hu, Y.; Si, S.; Sun, X.F.; et al. Genome-wide identification, interaction of the MADS-box proteins in Zanthoxylum armatum and functional characterization of ZaMADS80 in floral development. Front. Plant Sci. 2022, 13, 1038828. [Google Scholar] [CrossRef] [PubMed]
- Guimaraes, L.A.; Dusi, D.; Masiero, S.; Resentini, F.; Gomes, A.; Silveira, E.D.; Florentino, L.H.; Rodrigues, J.; Colombo, L.; Carneiro, V. BbrizAGL6 Is Differentially Expressed During Embryo Sac Formation of Apomictic and Sexual Brachiaria brizantha Plants. Plant Mol. Biol. Rep. 2013, 31, 1397–1406. [Google Scholar] [CrossRef]
- Emms, D.M.; Kelly, S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 2019, 20, 238. [Google Scholar] [CrossRef]
- Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef]
- Talavera, G.; Castresana, J. Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments. Syst. Biol. 2007, 56, 564–577. [Google Scholar] [CrossRef]
- Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef]
- Yang, Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol. Biol. Evol. 2007, 24, 1586–1591. [Google Scholar] [CrossRef]
- Wang, S.; Wei, S.; Deng, Y.; Wu, S.; Peng, H.; Qing, Y.; Zhai, X.; Zhou, S.; Li, J.; Li, H.; et al. HortGenome Search Engine, a universal genomic search engine for horticultural crops. Hortic. Res. 2024, 11, uhae100. [Google Scholar] [CrossRef]
- Mendes, F.K.; Vanderpool, D.; Fulton, B.; Hahn, M.W. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 2020, 36, 5516–5518. [Google Scholar] [CrossRef]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
- Sun, P.C.; Jiao, B.B.; Yang, Y.Z.; Shan, L.X.; Li, T.; Li, X.N.; Xi, Z.X.; Wang, X.Y.; Liu, J.Q. WGDI: A user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Mol. Plant 2022, 15, 1841–1851. [Google Scholar] [CrossRef]
- Wang, Y.P.; Tang, H.B.; DeBarry, J.D.; Tan, X.; Li, J.P.; Wang, X.Y.; Lee, T.H.; Jin, H.Z.; Marler, B.; Guo, H.; et al. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012, 40, e49. [Google Scholar] [CrossRef] [PubMed]
- Pertea, M.; Kim, D.; Pertea, G.M.; Leek, J.T.; Salzberg, S.L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 2016, 11, 1650–1667. [Google Scholar] [CrossRef] [PubMed]
- Abramson, J.; Adler, J.; Dunger, J.; Evans, R.; Green, T.; Pritzel, A.; Ronneberger, O.; Willmore, L.; Ballard, A.J.; Bambrick, J.; et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature 2024, 630, 493–500. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Gao, Y.; Yang, Q.; Yan, X.; Wu, X.; Yang, F.; Li, J.; Wei, J.; Ni, J.; Ahmad, M.; Bai, S.; et al. High-quality genome assembly of ‘Cuiguan’ pear (Pyrus pyrifolia) as a reference genome for identifying regulatory genes and epigenetic modifications responsible for bud dormancy. Hortic. Res. 2021, 8, 197. [Google Scholar] [CrossRef] [PubMed]
- Su, W.; Jing, Y.; Lin, S.; Yue, Z.; Yang, X.; Xu, J.; Wu, J.; Zhang, Z.; Xia, R.; Zhu, J.; et al. Polyploidy underlies co-option and diversification of biosynthetic triterpene pathways in the apple tribe. Proc. Natl. Acad. Sci. USA 2021, 118, e2101767118. [Google Scholar] [CrossRef]
- The International Peach Genome Initiative; Verde, I.; Abbott, A.G.; Scalabrin, S.; Jung, S.; Shu, S.; Marroni, F.; Zhebentyayeva, T.; Dettori, M.T.; Grimwood, J.; et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat. Genet. 2013, 45, 487–494. [Google Scholar] [CrossRef] [PubMed]
- Le Dantec, L.; Girollet, N.; Gouzy, J.; Sallet, E.; Fouche, M.; Quero-Garcia, J.; Dirlewanger, E. An improved assembly of the diploid ‘Regina’ Sweet cherry genome. In Proceedings of the International Plant & Animal Genome XXVII, San Diego, CA, USA, 12–16 January 2019. [Google Scholar]
- Groppi, A.; Liu, S.; Cornille, A.; Decroocq, S.; Bui, Q.T.; Tricon, D.; Cruaud, C.; Arribat, S.; Belser, C.; Marande, W.; et al. Population genomics of apricots unravels domestication history and adaptive events. Nat. Commun. 2021, 12, 3956. [Google Scholar] [CrossRef]
- Huang, Z.; Shen, F.; Chen, Y.; Cao, K.; Wang, L. Chromosome-scale genome assembly and population genomics provide insights into the adaptation, domestication, and flavonoid metabolism of Chinese plum. Plant J. 2021, 108, 1174–1192. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Li, M.; Li, Y.; Xiao, Y.; Luo, X.; Gao, S.; Ma, Z.; Sadowski, N.; Timp, W.; Dardick, C.; et al. Comparison of red raspberry and wild strawberry fruits reveals mechanisms of fruit type specification. Plant Physiol. 2023, 193, 1016–1035. [Google Scholar] [CrossRef] [PubMed]
- VanBuren, R.; Wai, C.M.; Colle, M.; Wang, J.; Sullivan, S.; Bushakra, J.M.; Liachko, I.; Vining, K.J.; Dossett, M.; Finn, C.E.; et al. A near complete, chromosome-scale assembly of the black raspberry (Rubus occidentalis) genome. Gigascience 2018, 7, giy094. [Google Scholar] [CrossRef] [PubMed]
- Brůna, T.; Aryal, R.; Dudchenko, O.; Sargent, D.J.; Mead, D.; Buti, M.; Cavallini, A.; Hytönen, T.; Andres, J.; Pham, M.; et al. A chromosome-length genome assembly and annotation of blackberry (Rubus argutus, cv.“Hillquist”). G3 Genes|Genomes|Genetics 2023, 13, jkac289. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Peng, Y.; Liu, L.; Li, G.; Zhao, X.; Wang, X.; Cao, S.; Muyle, A.; Zhou, Y.; Zhou, H. Phased gap-free genome assembly of octoploid cultivated strawberry illustrates the genetic and epigenetic divergence among subgenomes. Hortic. Res. 2023, 11, uhad252. [Google Scholar] [CrossRef] [PubMed]
- Massonnet, M.; Cochetel, N.; Minio, A.; Vondras, A.M.; Lin, J.; Muyle, A.; Garcia, J.F.; Zhou, Y.; Delledonne, M.; Riaz, S.; et al. The genetic basis of sex determination in grapes. Nat. Commun. 2020, 11, 2902. [Google Scholar] [CrossRef]
- Zhang, L.; Hu, J.; Han, X.; Li, J.; Gao, Y.; Richards, C.M.; Zhang, C.; Tian, Y.; Liu, G.; Gul, H.; et al. A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat. Commun. 2019, 10, 1494. [Google Scholar] [CrossRef]
- Duan, Y.; Ma, S.; Chen, X.; Shen, X.; Yin, C.; Mao, Z. Transcriptome changes associated with apple (Malus domestica) root defense response after Fusarium proliferatum f. sp. malus domestica infection. BMC Genom. 2022, 23, 484. [Google Scholar] [CrossRef]
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Wang, B.; Xiao, Y.; Yan, M.; Fan, W.; Zhu, Y.; Li, W.; Li, T. Gene Duplication and Functional Diversification of MADS-Box Genes in Malus × domestica following WGD: Implications for Fruit Type and Floral Organ Evolution. Int. J. Mol. Sci. 2024, 25, 8962. https://doi.org/10.3390/ijms25168962
Wang B, Xiao Y, Yan M, Fan W, Zhu Y, Li W, Li T. Gene Duplication and Functional Diversification of MADS-Box Genes in Malus × domestica following WGD: Implications for Fruit Type and Floral Organ Evolution. International Journal of Molecular Sciences. 2024; 25(16):8962. https://doi.org/10.3390/ijms25168962
Chicago/Turabian StyleWang, Baoan, Yao Xiao, Mengbo Yan, Wenqi Fan, Yuandi Zhu, Wei Li, and Tianzhong Li. 2024. "Gene Duplication and Functional Diversification of MADS-Box Genes in Malus × domestica following WGD: Implications for Fruit Type and Floral Organ Evolution" International Journal of Molecular Sciences 25, no. 16: 8962. https://doi.org/10.3390/ijms25168962