The red flower wintersweet genome provides insights into the evolution of magnoliids and the molecular mechanism for tepal color development.
Anthocyanins
/ genetics
Calycanthaceae
/ genetics
Flowers
/ genetics
Frameshift Mutation
Gene Expression Regulation, Plant
Genome, Plant
Laurales
/ genetics
Molecular Sequence Annotation
Phylogeny
Pigmentation
/ genetics
Plant Proteins
/ genetics
Transcription Factors
/ genetics
Whole Genome Sequencing
Chimonanthus praecox
MYB transcription factor
flower color development
genome
magnoliid evolution
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
09
04
2021
accepted:
01
10
2021
pubmed:
9
10
2021
medline:
4
2
2022
entrez:
8
10
2021
Statut:
ppublish
Résumé
Wintersweet (Chimonanthus praecox) is one of the most important ornamental plants. Its color is mainly determined by the middle tepals. However, the molecular mechanisms underlying the intriguing flower color development among different wintersweet groups are still largely unknown. In addition, wintersweet belongs to magnoliids, and the phylogenetic position of magnoliids remains to be determined conclusively. Here, the whole genome of red flower wintersweet, a new wintersweet type, was sequenced and assembled with high quality. The genome comprised 11 super-scaffolds (chromosomes) with a total size of 737.03 Mb. Based on the analyses of the long branch attraction, incomplete lineage sorting, sparse taxon sampling, and other factors, we suggest that a bifurcating tree may not fully represent the complex early diversification of the angiosperms and that magnoliids are most likely sister to the eudicots. The wintersweet genome appears to have undergone two whole-genome duplication (WGD) events: a recent WGD event representing an independent event specific to the Calycanthaceae and an ancient WGD event shared by Laurales. By integrating genomic, transcriptomic, and metabolomic data, CpANS1 and the transcription factor CpMYB1 were found to play key roles in regulating tepal color development, whereas CpMYB1 needs to form a complex with bHLH and WD40 to fully perform its regulatory function. The present study not only provides novel insights into the evolution of magnoliids and the molecular mechanism for flower color development, but also lays the foundation for subsequent functional genomics study and molecular breeding of wintersweet.
Substances chimiques
Anthocyanins
0
Plant Proteins
0
Transcription Factors
0
cyanidin
7732ZHU564
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1662-1678Informations de copyright
© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Albert, N.W., Lewis, D.H., Zhang, H., Schwinn, K.E., Jameson, P.E. & Davies, K.M. (2011) Members of an r2r3-myb transcription factor family in petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning. The Plant Journal, 65, 771-784.
Allan, A.C. & Espley, R.V. (2018) MYBs drive novel consumer traits in fruits and vegetables. Trends in Plant Science, 23, 693-705.
Baas, P., Wheeler, E. & Chase, M. (2000) Dicotyledonous wood anatomy and the APG system of angiosperm classification. Botanical Journal of the Linnean Society, 134, 3-17.
Bergsten, J. (2005) A review of long-branch attraction. Cladistics, 21, 163-193.
Boeckmann, B., Bairoch, A., Apweiler, R., Blatter, M.-C., Estreicher, A., Gasteiger, E. et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Research, 31, 365-370.
Cantino, P.D., Doyle, J.A., Graham, S.W., Judd, W.S., Olmstead, R.G., Soltis, D.E. et al. (2007) Towards a phylogenetic nomenclature of Tracheophyta. Taxon, 56, E1-E44.
Cao, Y., Li, K., Li, Y., Zhao, X. & Wang, L. (2020) MYB transcription factors as regulators of secondary metabolism in plants. Biology, 9, 61.
Cao, Y., Liu, M., Long, H., Zhao, Q., Jiang, L. & Zhang, L. (2020) Hidden in plain sight: systematic investigation of Leucine-rich repeat containing genes unveil the their regulatory network in response to Fusarium wilt in tung tree. International Journal of Biological Macromolecules, 163, 1759-1767.
Chan, P.P. & Lowe, T.M. (2019) tRNAscan-SE: searching for tRNA genes in genomic sequences. In: Gene Prediction: Humana, NY: Springer, pp. 1-14.
Chase, M.W., Christenhusz, M.J.M., Fay, M.F., Byng, J.W., Judd, W.S., Soltis, D.E. et al. (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181, 1-20.
Chaw, S.-M., Liu, Y.-C., Wu, Y.-W., Wang, H.-Y., Lin, C.-Y., Wu, C.-S. et al. (2019) Stout camphor tree genome fills gaps in understanding of flowering plant genome evolution. Nature Plants, 5, 63-73.
Chen, J., Hao, Z., Guang, X., Zhao, C., Wang, P., Xue, L. et al. (2019) Liriodendron genome sheds light on angiosperm phylogeny and species-pair differentiation. Nature Plants, 5, 18-25.
Chen, S.-P., Sun, W.-H., Xiong, Y.-F., Jiang, Y.-T., Liu, X.-D., Liao, X.-Y. et al. (2020) The Phoebe genome sheds light on the evolution of magnoliids. Horticulture Research, 7, 1-13.
Chen, S., Zhou, Y., Chen, Y. & Gu, J. (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34, i884-i890.
Chen, Y.-C., Li, Z., Zhao, Y.-X., Gao, M., Wang, J.-Y., Liu, K.-W. et al. (2020) The Litsea genome and the evolution of the laurel family. Nature Communications, 11, 1-14.
Chin, C.-S., Alexander, D.H., Marks, P., Klammer, A.A., Drake, J., Heiner, C. et al. (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods, 10, 563-569.
Debes, M.A., Arias, M.E., Grellet-Bournonville, C.F., Wulff, A.F., Martínez-Zamora, M.G., Castagnaro, A.P. et al. (2011) White-fruited Duchesnea indica (Rosaceae) is impaired in ANS gene expression. American Journal of Botany, 98, 2077-2083.
Dong, S., Liu, M., Liu, Y., Chen, F., Yang, T., Chen, L.U. et al. (2021) The genome of Magnolia biondii Pamp. provides insights into the evolution of Magnoliales and biosynthesis of terpenoids. Horticulture Research, 8, 38.
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.
Espley, R.V., Brendolise, C., Chagné, D., Kutty-Amma, S., Green, S., Volz, R. et al. (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. The Plant Cell, 21, 168-183.
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.
Gene Ontology Consortium (2019) The gene ontology resource: 20 years and still GOing strong. Nucleic Acids Research, 47, D330-D338.
Gong, Z., Yamazaki, M., Sugiyama, M., Tanaka, Y. & Saito, K. (1997) Cloning and molecular analysis of structural genes involved in anthocyanin biosynthesis and expressed in a forma-specific manner in Perilla frutescens. Plant Molecular Biology, 35, 915-927.
Gu, Z., Zhu, J., Hao, Q., Yuan, Y.-W., Duan, Y.-W., Men, S. et al. (2019) A novel R2R3-MYB transcription factor contributes to petal blotch formation by regulating organ-specific expression of PsCHS in tree peony (Paeonia suffruticosa). Plant and Cell Physiology, 60, 599-611.
Haston, E., Richardson, J.E., Stevens, P.F., Chase, M.W. & Harris, D.J. (2007) A linear sequence of Angiosperm Phylogeny Group II families. Taxon, 56, 7-E6.
Haston, E., Richardson, J.E., Stevens, P.F., Chase, M.W. & Harris, D.J. (2009) The Linear Angiosperm Phylogeny Group (LAPG) III: a linear sequence of the families in APG III. Botanical Journal of the Linnean Society, 161, 128-131.
Hawkins, C., Caruana, J., Schiksnis, E. & Liu, Z. (2016) Genome-scale DNA variant analysis and functional validation of a SNP underlying yellow fruit color in wild strawberry. Scientific Reports, 6, 29017.
Heywood, V.H., Brummitt, R.K., Culham, A. & Seberg, O. (2007) Flowering plant families of the world. Richmond Hill, Canada: Firefly Books Ontario.
Horsch, R.B., Fry, J.E., Hovmann, N.L., Eichholtz, D., Rogers, S.G. & Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science, 227, 1229-1231.
Hu, L., Xu, Z., Wang, M., Fan, R., Yuan, D., Wu, B. et al. (2019) The chromosome-scale reference genome of black pepper provides insight into piperine biosynthesis. Nature Communications, 10, 1-11.
Iwashina, T. (2015) Contribution to flower colors of flavonoids including anthocyanins: a review. Natural Product Communications, 10, https://doi.org/10.1177/1934578X1501000335
Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C. et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics, 30, 1236-1240.
Katoh, K., Kuma, K.-I., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511-518.
Kim, D., Paggi, J.M., Park, C., Bennett, C. & Salzberg, S.L. (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37, 907-915.
Kohl, M., Wiese, S. & Warscheid, B. (2011) Cytoscape: software for visualization and analysis of biological networks. In: Michael, H., Martin, E. & Christian, S. (Eds.) Data mining in proteomics. Humana, NY: Springer, pp. 291-303.
Kumar, S., Stecher, G., Suleski, M. & Hedges, S.B. (2017) TimeTree: a resource for timelines, timetrees, and divergence times. Molecular Biology and Evolution, 34, 1812-1819.
Lagesen, K., Hallin, P., Rødland, E.A., Staerfeldt, H.-H., Rognes, T. & Ussery, D.W. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Research, 35, 3100-3108.
Langfelder, P. & Horvath, S. (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.
Lavigne, R., Seto, D., Mahadevan, P., Ackermann, H.-W. & Kropinski, A.M. (2008) Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Research in Microbiology, 159, 406-414.
Li, L., Stoeckert, C.J. & Roos, D.S. (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Research, 13, 2178-2189.
Liao, Y., Smyth, G.K. & Shi, W. (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923-930.
Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A. et al. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326, 289-293.
Lowe, T.M. & Eddy, S.R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research, 25, 955-964.
Lv, Q., Qiu, J., Liu, J., Li, Z., Zhang, W., Wang, Q. et al. (2020) The Chimonanthus salicifolius genome provides insight into magnoliids evolution and flavonoids biosynthesis. The Plant Journal, 103, 1910-1923.
Massoni, J., Couvreur, T.L.P. & Sauquet, H. (2015) Five major shifts of diversification through the long evolutionary history of Magnoliidae (angiosperms). BMC Evolutionary Biology, 15, 1-14.
Massoni, J., Forest, F. & Sauquet, H. (2014) Increased sampling of both genes and taxa improves resolution of phylogenetic relationships within Magnoliidae, a large and early-diverging clade of angiosperms. Molecular Phylogenetics and Evolution, 70, 84-93.
Mirarab, S., Reaz, R., Bayzid, M.S., Zimmermann, T., Swenson, M.S. & Warnow, T. (2014) ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics, 30, i541-i548.
Mistry, J., Chuguransky, S., Williams, L., Qureshi, M., Salazar, G., Sonnhammer, E.L.L. et al. (2020) Pfam: the protein families database in 2021. Nucleic Acids Research, 49(D1), D412-D419.
Misyura, M., Colasanti, J. & Rothstein, S.J. (2013) Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. Journal of Experimental Botany, 64, 229-240.
Nakatsuka, T., Saito, M., Sato-Ushiku, Y., Yamada, E., Nakasato, T., Hoshi, N. et al. (2012) Development of DNA markers that discriminate between white-and blue-flowers in Japanese gentian plants. Euphytica, 184, 335-344.
Parra, G., Bradnam, K. & Korf, I. (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics, 23, 1061-1067.
Polturak, G., Heinig, U., Grossman, N., Battat, M., Leshkowitz, D., Malitsky, S. et al. (2018) Transcriptome and metabolic profiling provides insights into betalain biosynthesis and evolution in Mirabilis jalapa. Molecular Plant, 11, 189-204.
Qu, X.-J., Jin, J.-J., Chaw, S.-M., Li, D.-Z. & Yi, T.-S. (2017) Multiple measures could alleviate long-branch attraction in phylogenomic reconstruction of Cupressoideae (Cupressaceae). Scientific Reports, 7, 1-11.
Ramsay, N.A. & Glover, B.J. (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in Plant Science, 10, 63-70.
Ren, Q., Wang, Q.S., Firth, A.E., Chan, M., Gouw, J.W., Guarna, M.M. et al. (2012) Alternative reading frame selection mediated by a trna-like domain of an internal ribosome entry site. Proceedings of the National Academy of Sciences of the United States of America, 109(11), 4033-4034.
Rendón-Anaya, M., Ibarra-Laclette, E., Méndez-Bravo, A., Lan, T., Zheng, C., Carretero-Paulet, L. et al. (2019) The avocado genome informs deep angiosperm phylogeny, highlights introgressive hybridization, and reveals pathogen-influenced gene space adaptation. Proceedings of the National Academy of Sciences, 116, 17081-17089.
Sanderson, M.J., Wojciechowski, M.F., Hu, J.M., Khan, T.S. & Brady, S.G. (2000) Error, bias, and long-branch attraction in data for two chloroplast photosystem genes in seed plants. Molecular Biology and Evolution, 17, 782-797.
Shang, J., Tian, J., Cheng, H., Yan, Q., Li, L., Jamal, A. et al. (2020) The chromosome-level wintersweet (Chimonanthus praecox) genome provides insights into floral scent biosynthesis and flowering in winter. Genome Biology, 21, 1-28.
Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V. & Zdobnov, E.M. (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313.
Tanaka, Y. & Ohmiya, A. (2008) Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. Current Opinion in Biotechnology, 19, 190-197.
Tang, H., Bowers, J.E., Wang, X., Ming, R., Alam, M. & Paterson, A.H. (2008) Synteny and collinearity in plant genomes. Science, 320, 486-488.
Tian, J., Peng, Z., Zhang, J., Song, T., Wan, H., Zhang, M. et al. (2015) Mc MYB 10 regulates coloration via activating McF3′ H and later structural genes in ever-red leaf crabapple. Plant Biotechnology Journal, 13, 948-961.
Veitch, N.C. & Grayer, R.J. (2011) Flavonoids and their glycosides, including anthocyanins. Natural Product Reports, 28, 1626-1695.
Walker, A.R., Lee, E., Bogs, J., McDavid, D.A.J., Thomas, M.R. & Robinson, S.P. (2007) White grapes arose through the mutation of two similar and adjacent regulatory genes. The Plant Journal, 49, 772-785.
Wang, Y., Tang, H., DeBarry, J.D., Tan, X., Li, J., Wang, X. et al. (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40, e49.
Wiens, J.J. (2005) Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Systematic Biology, 54, 731-742.
Yang, L., Su, D., Chang, X., Foster, C.S.P., Sun, L., Huang, C.-H. et al. (2020) Phylogenomic insights into deep phylogeny of Angiosperms based on broad nuclear gene sampling. Plant Communications, 1, 100027.
Yang, N., Zhao, K., Li, X., Zhao, R., Aslam, M.Z., Yu, L.I. et al. (2018) Comprehensive analysis of wintersweet flower reveals key structural genes involved in flavonoid biosynthetic pathway. Gene, 676, 279-289.
Yang, Z. (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586-1591.
Zeng, L., Zhang, Q., Sun, R., Kong, H., Zhang, N. & Ma, H. (2014) Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nature Communications, 5, 1-12.
Zhang, J., Han, Z.-Y., Tian, J., Zhang, X., Song, T.-T. & Yao, Y.-C. (2015) The expression level of anthocyanidin synthase determines the anthocyanin content of crabapple (Malus sp.) petals. Acta Physiologiae Plantarum, 37, 109.
Zhang, L., Chen, F., Zhang, X., Li, Z., Zhao, Y., Lohaus, R. et al. (2020) The water lily genome and the early evolution of flowering plants. Nature, 577, 79-84.
Zhang, L., Liu, M., Long, H., Dong, W., Pasha, A., Esteban, E. et al. (2019) Tung tree (Vernicia fordii) genome provides a resource for understanding genome evolution and improved oil production. Genomics, Proteomics & Bioinformatics, 17, 558-575.
Zhang, N., Zeng, L., Shan, H. & Ma, H. (2012) Highly conserved low-copy nuclear genes as effective markers for phylogenetic analyses in angiosperms. New Phytologist, 195, 923-937.