Chromosome-scale genomes of Quercus sichourensis and Quercus rex provide insights into the evolution and adaptation of Fagaceae

Xue Liu; Weixiong Zhang; Yongting Zhang; Jing Yang; Peng Zeng; Zunzhe Tian; Weibang Sun; Jing Cai

doi:10.1016/j.jgg.2024.03.012

Volume 51 Issue 5

May 2024

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2024 > 51(5): 554-565

PDF( 2187 KB)

Chromosome-scale genomes of Quercus sichourensis and Quercus rex provide insights into the evolution and adaptation of Fagaceae

doi: 10.1016/j.jgg.2024.03.012

a. Shaanxi Key Laboratory of Qinling Ecological Intelligent Monitoring and Protection, School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, Shaanxi 710072, China;
b. Yunnan Key Laboratory for Integrative Conservation of Plant Species with Extremely Small Populations, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China

Funds:

We thank many people who provided feedback, samples and encouragement, especially Kunming Botanical Garden. This work was supported by “the Thousand Talents Plan” (5113190037 to J.C.), Fundamental Research Funds for the Central Universities (3102019JC007), Science and Technology Basic Resources Investigation Program of China (2017FY100100) and NSFC (National Natural Science Foundation of China)-Yunnan Joint Fund (U1302262).

Received Date: 2023-12-26
Accepted Date: 2024-03-28
Rev Recd Date: 2024-03-25

Available Online: 2025-06-06

Publish Date: 2024-04-02

Abstract

Abstract

The Fagaceae, a plant family with a wide distribution and diverse adaptability, has garnered significant interest as a subject of study in plant speciation and adaptation. Meanwhile, certain Fagaceae species are regarded as highly valuable wood resources due to the exceptional quality of their wood. In this study, we present two high-quality, chromosome-scale genome sequences for Quercus sichourensis (848.75 Mb) and Quercus rex (883.46 Mb). Comparative genomics analysis reveals that the difference in the number of plant disease resistance genes and the nonsynonymous and synonymous substitution ratio (Ka/Ks) of protein-coding genes among Fagaceae species are related to different environmental adaptations. Interestingly, most genes related to starch synthesis in the investigated Quercoideae species are located on a single chromosome, as compared to the outgroup species, Fagus sylvatica. Furthermore, resequencing and population analysis of Q. sichourensis and Q. rex reveal that Q. sichourensis has lower genetic diversity and higher deleterious mutations compared to Q. rex. The high-quality, chromosome-level genomes and the population genomic analysis of the critically endangered Q. sichourensis and Q. rex will provide an invaluable resource as well as insights for future study in these two species, even the genus Quercus, to facilitate their conservation.
- Adaptation,
- Quercus sichourensis,
- Quercus rex,
- Chromosome-scale genome assembly,
- Tandem duplication genes,
- Extremely small populations

FullText(HTML)

References(101)

References

Ai, W.F., Liu, Y.Q., Mei, M., Zhang, X.L., Tan, E.G., Liu, H.Z., Han, X.Y., Zhan, H., Lu, X.J., 2022. A chromosome-scale genome assembly of the Mongolian oak (Quercus mongolica). Mol. Ecol. Resour. 22, 2396-2410.

Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.

Barrett, J.C., Fry, B., Maller, J., Daly, M.J., 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265.

Benson, G., 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580.

Birney, E., Durbin, R., 2000. Using GeneWise in the Drosophila annotation experiment. Genome Res. 10, 547-548.

Browning, S.R., Browning, B.L., 2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084-1097.

Cai, L., Liu, D., Yang, F., Zhang, R., Yun, Q., Dao, Z., Ma, Y., Sun, W., 2024. The chromosome-scale genome of Magnolia sinica (Magnoliaceae) provides insights into the conservation of plant species with extremely small populations (PSESP). Gigascience 13, giad110.

Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T.L., 2009. BLAST+: architecture and applications. BMC Bioinformatics 10, 421.

Chen, C., Chen, H., Zhang, Y., Thomas, H.R., Frank, M.H., He, Y., Xia, R., 2020. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant. 13, 1194-1202.

Cingolani, P., Platts, A., Wang le, L., Coon, M., Nguyen, T., Wang, L., Land, S.J., Lu, X., Ruden, D.M., 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6, 80-92.

Crowl, A.A., Manos, P.S., McVay, J.D., Lemmon, A.R., Lemmon, E.M., Hipp, A.L., 2020. Uncovering the genomic signature of ancient introgression between white oak lineages (Quercus). New Phytol. 226, 1158-1170.

Cui, R., Wu, J., Yan, K., Luo, S., Hu, Y., Feng, W., Lu, B., Wang, J., 2024. Phased genome assemblies reveal haplotype-specific genetic load in the critically endangered Chinese Bahaba (Teleostei, Sciaenidae). Mol. Ecol. 33, e17250.

Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., Handsaker, R.E., Lunter, G., Marth, G.T., Sherry, S.T., et al., 2011. The variant call format and VCFtools. Bioinformatics 27, 2156-2158.

Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., Handsaker, R.E., Lunter, G., Marth, G.T., Sherry, S.T., et al, 2011. The variant call format and VCFtools. Bioinformatics 27, 2156-2158. del Pozo, J.C., Ramirez-Parra, E., 2015. Whole genome duplications in plants: an overview from. J. Exp. Bot. 66, 6991-7003.

Deng, M., Jiang, X.L., Hipp, A.L., Manos, P.S., Hahn, M., 2018. Phylogeny and biogeography of East Asian evergreen oaks (Quercus section Cyclobalanopsis; Fagaceae): Insights into the Cenozoic history of evergreen broad-leaved forests in subtropical Asia. Mol. Phylogenet. Evol. 119, 170-181.

DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C., Philippakis, A.A., del Angel, G., Rivas, et al, 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498.

Dudchenko, O., Batra, S.S., Omer, A.D., Nyquist, S.K., Hoeger, M., Durand, N.C., Shamim, M.S., Machol, I., Lander, E.S., Aiden, A.P., et al, 2017. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92-95.

Durand, N.C., Shamim, M.S., Machol, I., Rao, S.S., Huntley, M.H., Lander, E.S., Aiden, E.L., 2016. Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. Cell Syst. 3, 95-98.

Edgar, R.C., 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.

Ehlting, J., Buttner, D., Wang, Q., Douglas, C.J., Somssich, I.E., Kombrink, E., 1999. Three 4-coumarate: coenzyme A ligases in represent two evolutionarily divergent classes in angiosperms. Plant J. 19, 9-20.

Emms, D.M., Kelly, S., 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238.

Etherington, G.J., Ramirez-Gonzalez, R.H., MacLean, D., 2015. bio-samtools 2: a package for analysis and visualization of sequence and alignment data with SAMtools in Ruby. Bioinformatics 31, 2565-2567.

Fu, R.R., Zhu, Y.X., Liu, Y., Feng, Y., Lu, R.S., Li, Y., Li, P., Kremer, A., Lascoux, M., Chen, J., 2022. Genome-wide analyses of introgression between two sympatric Asian oak species. Nat. Ecol. Evol. 6, 924.

Galimba, K.D., Di Stilio, V.S., 2015. Sub-functionalization to ovule development following duplication of a floral organ identity gene. Dev. Biol. 405, 158-172.

Gasteiger, E., Jung, E., Bairoch, A., 2001. SWISS-PROT: connecting biomolecular knowledge via a protein database. Curr. Issues Mol. Biol. 3, 47-55.

Gazal, S., Sahbatou, M., Perdry, H., Letort, S., Genin, E., Leutenegger, A.L., 2014. Inbreeding coefficient estimation with dense SNP data: comparison of strategies and application to HapMap III. Hum. Hered. 77, 49-62.

Goujon, T., Sibout, R., Pollet, B., Maba, B., Nussaume, L., Bechtold, N., Lu, F.C., Ralph, J., Mila, I., Barriere, Y., et al, 2003. A new mutant deficient in the expression of methyltransferase impacts lignins and sinapoyl esters. Plant Mol. Biol. 51, 973-989.

Guan, D., McCarthy, S.A., Wood, J., Howe, K., Wang, Y., Durbin, R., 2020. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896-2898.

Gugger, P.F., Fitz-Gibbon, S.T., Albarran-Lara, A., Wright, J.W., Sork, V.L., 2021. Landscape genomics of Quercus lobata reveals genes involved in local climate adaptation at multiple spatial scales. Mol. Ecol. 30, 406-423.

Gutenkunst, R.N., Hernandez, R.D., Williamson, S.H., Bustamante, C.D., 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5, e1000695.

Guo, L., Winzer, T., Yang, X., Li, Y., Ning, Z., He, Z., Teodor, R., Lu, Y., Bowser, T.A., Graham, I.A., Ye, K., 2018. The opium poppy genome and morphinan production. Science 362, 343-347.

Haas, B.J., Delcher, A.L., Mount, S.M., Wortman, J.R., Smith, R.K., Jr., Hannick, L.I., Maiti, R., Ronning, C.M., Rusch, D.B., Town, C.D., et al., 2003. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654-5666.

Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., et al., 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512.

Haas, B.J., Salzberg, S.L., Zhu, W., Pertea, M., Allen, J.E., Orvis, J., White, O., Buell, C.R., Wortman, J.R., 2008. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7.

Hahn, M.W., De Bie, T., Stajich, J.E., Nguyen, C., Cristianini, N., 2005. Estimating the tempo and mode of gene family evolution from comparative genomic data. Genome Res. 15, 1153-1160.

Han, B., Wang, L., Xian, Y., Xie, X.M., Li, W.Q., Zhao, Y., Zhang, R.G., Qin, X., Li, D.Z., Jia, K.H., 2022. A chromosome-level genome assembly of the Chinese cork oak (Quercus variabilis). Front. Plant Sci. 13, 1001583.

Hoffmann, N., Benske, A., Betz, H., Schuetz, M., Samuels, A.L., 2020. Laccases and Peroxidases Co-Localize in Lignified Secondary Cell Walls throughout Stem Development. Plant Physiol. 184, 806-822.

Hunter, S., Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Binns, D., Bork, P., Das, U., Daugherty, L., Duquenne, L., et al., 2009. InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211-215.

Innan, H., Kondrashov, F., 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97-108.

Kanehisa, M., Goto, S., 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30.

Kim, B.Y., Wei, X., Fitz-Gibbon, S., Lohmueller, K.E., Ortego, J., Gugger, P.F., Sork, V.L., 2018. RADseq data reveal ancient, but not pervasive, introgression between Californian tree and scrub oak species (Quercus sect. Quercus: Fagaceae). Mol. Ecol. 27, 4556-4571.

Korf, I., 2004. Gene finding in novel genomes. BMC Bioinformatics 5, 59.

Li, G., Wang, L., Yang, J., He, H., Jin, H., Li, X., Ren, T., Ren, Z., Li, F., Han, X., et al., 2021. A high-quality genome assembly highlights rye genomic characteristics and agronomically important genes. Nat. Genet. 53, 574-584.

Li, H., Durbin, R., 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.

Li, H., Durbin, R., 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595.

Li, H., Durbin, R., 2011. Inference of human population history from individual whole-genome sequences. Nature 475, 493-496.

Li, Z., Tiley, G.P., Galuska, S.R., Reardon, C.R., Kidder, T.I., Rundell, R.J., Barker, M.S., 2018. Multiple large-scale gene and genome duplications during the evolution of hexapods. P. Natl. Acad. Sci. U. S. A. 115, 4713-4718.

Liepman, A.H., Nairn, C.J., Willats, W.G.T., Sorensen, I., Roberts, A.W., Keegstra, K., 2007. Functional genomic analysis supports conservation of function among cellulose synthase-like a gene family members and suggests diverse roles of mannans in plants. Plant Physiol. 143, 1881-1893.

Liu, X., Fu, Y.X., 2020. Stairway Plot 2: demographic history inference with folded SNP frequency spectra. Genome Biol. 21, 280.

Lynch, M., 2002. Genomics - Gene duplication and evolution. Science 297(5583), 945-947.

Ma, H., Liu, Y., Liu, D., Sun, W., Liu, X., Wan, Y., Zhang, X., Zhang, R., Yun, Q., Wang, J., et al., 2021. Chromosome-level genome assembly and population genetic analysis of a critically endangered rhododendron provide insights into its conservation. Plant J. 107, 1533-1545.

Ma, Y., Liu, D., Wariss, H.M., Zhang, R., Tao, L., Milne, R.I., Sun, W., 2022. Demographic history and identification of threats revealed by population genomic analysis provide insights into conservation for an endangered maple. Mol. Ecol. 31, 767-779.

Majoros, W.H., Pertea, M., Salzberg, S.L., 2004. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20(16), 2878-2879.

McDowell, J.M., Woffenden, B.J., 2003. Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol. 21, 178-183.

Meyer, S., Melzer, M., Truernit, E., Hummer, C., Besenbeck, R., Stadler, R., Sauer, N., 2000. A gene encoding a new sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. Plant J. 24, 869-882.

Moinuddin, S.G.A., Jourdes, M., Laskar, D.D., Ki, C., Cardenas, C.L., Kim, K.W., Zhang, D., Davin, L.B., Lewis, N.G., 2010. Insights into lignin primary structure and deconstruction from COMT (caffeic acid-methyl transferase) mutant. Org. Biomol. Chem. 8, 3928-3946.

Muzac, I., Wang, J., Auzellotti, D., Zhang, H., Ibrahim, R.K., 2000. Functional expression of an cDNA clone encoding a flavonol 3'-methyltransferase and characterization of the gene product. Arch. Biochem. Biophys. 375, 385-388.

Nei, M., Gojobori, T., 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418-426.

Ng, P.C., Henikoff, S., 2003. SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res. 31, 3812-3814.

Nguyen, L.T., Schmidt, H.A., von Haeseler, A., Minh, B.Q., 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274.

Ou, S., Chen, J., Jiang, N., 2018. Assessing genome assembly quality using the LTR Assembly Index (LAI). Nucleic Acids Res. 46, e126.

Ou, S.J., Su, W.J., Liao, Y., Chougule, K., Agda, J.R.A., Hellinga, A.J., Lugo, C.S.B., Elliott, T.A., Ware, D., Peterson, T., et al., 2019. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20, 275.

Petit, R.J., Carlson, J., Curtu, A.L., Loustau, M.L., Plomion, C., Gonzalez-Rodriguez, A., Sork, V., Ducousso, A., 2013. Fagaceae trees as models to integrate ecology, evolution and genomics. New Phytol. 197, 369-371.

Plomion, C., Aury, J.M., Amselem, J., Alaeitabar, T., Barbe, V., Belser, C., Berges, H., Bodenes, C., Boudet, N., Boury, C., et al., 2016. Decoding the oak genome: public release of sequence data, assembly, annotation and publication strategies. Mol. Ecol. Resour. 16, 254-265.

Plomion, C., Aury, J.M., Amselem, J., Leroy, T., Murat, F., Duplessis, S., Faye, S., Francillonne, N., Labadie, K., Le Provost, G., et al., 2018. Oak genome reveals facets of long lifespan. Nat. Plants 4, 440-452.

Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J., et al., 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575.

Qi, X., Bakht, S., Leggett, M., Maxwell, C., Melton, R., Osbourn, A., 2004. A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc. Natl. Acad. Sci. U. S. A. 101, 8233-8238.

Qiao, X., Zhang, S.L., Paterson, A.H., 2022. Pervasive genome duplications across the plant tree of life and their links to major evolutionary innovations and transitions. Comput. Struct. Biotec. 20, 3248-3256.

Quinlan, A.R., Hall, I.M., 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842.

Ramos, A.M., Usie, A., Barbosa, P., Barros, P.M., Capote, T., Chaves, I., Simoes, F., Abreu, I., Carrasquinho, I., Faro, C., et al., 2018. The draft genome sequence of cork oak. Sci. Data 5,180069.

Salojarvi, J., Smolander, O.P., Nieminen, K., Rajaraman, S., Safronov, O., Safdari, P., Lamminmaki, A., Immanen, J., Lan, T., Tanskanen, J., et al., 2017. Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat. Genet. 49, 904-912.

Seppey, M., Manni, M., Zdobnov, E.M., 2019. BUSCO: Assessing Genome Assembly and Annotation Completeness. Methods Mol. Biol. 1962, 227-245.

Sork, V.L., Cokus, S.J., Fitz-Gibbon, S.T., Zimin, A.V., Puiu, D., Garcia, J.A., Gugger, P.F., Henriquez, C.L., Zhen, Y., Lohmueller, K.E., et al., 2022. High-quality genome and methylomes illustrate features underlying evolutionary success of oaks. Nature Communications 13, 2047.

Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313.

Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S., Morgenstern, B., 2006. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435-439.

Sun, C., Xie, Y.H., Li, Z., Liu, Y.J., Sun, X.M., Li, J.J., Quan, W.P., Zeng, Q.Y., van de Peer, Y., Zhang, S.G., 2022. The genome reveals new insights into wood properties. J. Integr. Plant Biol. 64, 1364-1373.

Sun, G., Xu, Y., Liu, H., Sun, T., Zhang, J., Hettenhausen, C., Shen, G., Qi, J., Qin, Y., Li, J., et al., 2018. Large-scale gene losses underlie the genome evolution of parasitic plant Cuscuta australis. Nat. Commun. 9, 2683.

Sun, P., Jiao, B., Yang, Y., Shan, L., Li, T., Li, X., Xi, Z., Wang, X., Liu, J., 2022. WGDI: A user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Mol. Plant 15, 1841-1851.

Suyama, M., Torrents, D., Bork, P., 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609-612.

Takezaki, N., Rzhetsky, A., Nei, M., 1995. Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12, 823-833.

Tarailo-Graovac, M., Chen, N., 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics Chapter 4, Unit 4.10.

Terhorst, J., Kamm, J.A., Song, Y.S., 2017. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303-309.

Teufel, A.I., Liu, L., Liberles, D.A., 2016. Models for gene duplication when dosage balance works as a transition state to subsequent neo-or sub-functionalization. Bmc Evol. Biol. 16, 45.

Vurture, G.W., Sedlazeck, F.J., Nattestad, M., Underwood, C.J., Fang, H., Gurtowski, J., Schatz, M.C., 2017. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202-2204.

Wade, E.M., Nadarajan, J., Yang, X., Ballesteros, D., Sun, W., Pritchard, H.W., 2016. Plant species with extremely small populations (PSESP) in China: A seed and spore biology perspective. Plant Divers. 38, 209-220.

Wang, P., Burley, J.T., Liu, Y., Chang, J., Chen, D., Lu, Q., Li, S.H., Zhou, X., Edwards, S., Zhang, Z., 2021. Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant. Mol. Biol. Evol. 38, 263-273.

Wang, R., Liu, C.N., Segar, S.T., Jiang, Y.T., Zhang, K.J., Jiang, K., Wang, G., Cai, J., Chen, L.F., Chen, S.,et al., 2024. Dipterocarpoidae genomics reveal their demography and adaptations to Asian rainforests. Nat. Commun. 15, 1683.

Wang, W.B., He, X.F., Yan, X.M., Ma, B., Lu, C.F., Wu, J., Zheng, Y., Wang, W.H., Xue, W.B., Tian, X.C., Guo, J.F., El-Kassaby, Y.A., Porth, I., Leng, P.S., Hu, Z.H., Mao, J.F., 2023. Chromosome-scale genome assembly and insights into the metabolome and gene regulation of leaf color transition in an important oak species. New Phytol. 238, 2016-2032.

Wang, Y., Chen, F., Ma, Y.C., Zhang, T.K., Sun, P.C.A., Lan, M.F., Li, F., Fang, W.P., 2021. An ancient whole-genome duplication event and its contribution to flavor compounds in the tea plant (Camellia sinensis). Hortic Res. 8, 176.

Wang, Y., Tang, H., Debarry, J.D., Tan, X., Li, J., Wang, X., Lee, T.H., Jin, H., Marler, B., Guo, H., et al., 2012. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49.

Whittemore, A.T., Schaal, B.A., 1991. Interspecific gene flow in sympatric oaks. Proc Natl. Acad. Sci. U. S. A. 88, 2540-2544.

Wick, R.R., Holt, K.E., 2019. Benchmarking of long-read assemblers for prokaryote whole genome sequencing. F1000Res 8, 2138.

Xu, Y., Lei, Y., Su, Z., Zhao, M., Zhang, J., Shen, G., Wang, L., Li, J., Qi, J., Wu, J., 2021. A chromosome-scale Gastrodia elata genome and large-scale comparative genomic analysis indicate convergent evolution by gene loss in mycoheterotrophic and parasitic plants. Plant J. 108, 1609-1623.

Xu, Y., Zhang, J., Ma, C., Lei, Y., Shen, G., Jin, J., Eaton, D.A.R., Wu, J., 2022. Comparative genomics of orobanchaceous species with different parasitic lifestyles reveals the origin and stepwise evolution of plant parasitism. Mol. Plant. 15, 1384-1399.

Yang, Y., Ma, T., Wang, Z., Lu, Z., Li, Y., Fu, C., Chen, X., Zhao, M., Olson, M.S., Liu, J., 2018. Genomic effects of population collapse in a critically endangered ironwood tree Ostrya rehderiana. Nat. Commun. 9, 5449.

Yang, Z., 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.

Yu, D.S., Lee, D.H., Kim, S.K., Lee, C.H., Song, J.Y., Kong, E.B., Kim, J.F., 2012. Algorithm for predicting functionally equivalent proteins from BLAST and HMMER searches. J. Microbiol. Biotechnol. 22, 1054-1058.

Zhang, C., Rabiee, M., Sayyari, E., Mirarab, S., 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19, 153.

Zhou, B.F., Yuan, S., Crowl, A.A., Liang, Y.Y., Shi, Y., Chen, X.Y., An, Q.Q., Kang, M., Manos, P.S., Wang, B., 2022. Phylogenomic analyses highlight innovation and introgression in the continental radiations of Fagaceae across the Northern Hemisphere. Nat. Commun. 13, 1320.

Zhou, X., Liu, N., Jiang, X.L., Qin, Z.K., Farooq, T.H., Cao, F.L., Li, H., 2022. A chromosome-scale genome assembly of: Insights into the evolution of section (Fagaceae). Front. Plant Sci. 13, 1012277.

Zhang, Y., Lu, H.W., Ruan, J., 2023. GAEP: a comprehensive genome assembly evaluating pipeline. J. Genet. Genomics.

Relative Articles

Supplements(0)

Cited By

Proportional views