Bioinformatic analysis of chromatin organization and biased expression of duplicated genes between two poplars with a common whole-genome duplication

Le Zhang , Jingtian Zhao , Hao Bi , Xiangyu Yang , Zhiyang Zhang , Yutao Su , Zhenghao Li , Lei Zhang , Brian J. Sanderson , Jianquan Liu , Tao Ma

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 62

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :62 DOI: 10.1038/s41438-021-00494-2
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Bioinformatic analysis of chromatin organization and biased expression of duplicated genes between two poplars with a common whole-genome duplication
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Abstract

The nonrandom three-dimensional organization of chromatin plays an important role in the regulation of gene expression. However, it remains unclear whether this organization is conserved and whether it is involved in regulating gene expression during speciation after whole-genome duplication (WGD) in plants. In this study, high-resolution interaction maps were generated using high-throughput chromatin conformation capture (Hi-C) techniques for two poplar species, Populus euphratica and Populus alba var. pyramidalis, which diverged ~14 Mya after a common WGD. We examined the similarities and differences in the hierarchical chromatin organization between the two species, including A/B compartment regions and topologically associating domains (TADs), as well as in their DNA methylation and gene expression patterns. We found that chromatin status was strongly associated with epigenetic modifications and gene transcriptional activity, yet the conservation of hierarchical chromatin organization across the two species was low. The divergence of gene expression between WGD-derived paralogs was associated with the strength of chromatin interactions, and colocalized paralogs exhibited strong similarities in epigenetic modifications and expression levels. Thus, the spatial localization of duplicated genes is highly correlated with biased expression during the diploidization process. This study provides new insights into the evolution of chromatin organization and transcriptional regulation during the speciation process of poplars after WGD.

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Le Zhang, Jingtian Zhao, Hao Bi, Xiangyu Yang, Zhiyang Zhang, Yutao Su, Zhenghao Li, Lei Zhang, Brian J. Sanderson, Jianquan Liu, Tao Ma. Bioinformatic analysis of chromatin organization and biased expression of duplicated genes between two poplars with a common whole-genome duplication. Horticulture Research, 2021, 8 (1) : 62 DOI:10.1038/s41438-021-00494-2

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References

[1]

Dekker, J., Rippe, K., Dekker, M. & Kleckner, N. Capturing chromosome conformation. Science 295, 1306-1311 (2002).

[2]

Simonis, M. et al. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 38, 1348-1354 (2006).

[3]

Rao, S. S. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680 (2014).

[4]

Gibcus, J. H. & Dekker, J. The Hierarchy of the 3D Genome. Mol. Cell 49, 773-782 (2013).

[5]

Bonev, B. & Cavalli, G. Organization and function of the 3D genome. Nat. Rev. Genet. 17, 661 (2016).

[6]

Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).

[7]

Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380 (2012).

[8]

Rudan, M. V. et al. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 10, 1297-1309 (2015).

[9]

Rowley, M. J. et al. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell 67, 837-852.e7 (2017).

[10]

Koch, L . Toppling TAD tenets. Nat. Rev. Genet. 20, 565- 565 (2019).

[11]

Lazar, N. H. et al. The genomic false shuffle: epigenetic maintenance of topological domains in the rearranged gibbon genome. Preprint at bioRxiv https://doi.org/10.1101/238360 (2017).

[12]

Eres, I. E., Luo, K., Hsiao, C. J., Blake, L. E. & Gilad, Y. Reorganization of 3D genome structure may contribute to gene regulatory evolution in primates. PLoS Genet. 15, e1008278 (2019).

[13]

Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10, 725-732 (2009).

[14]

Initiative, O. T. P. T. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574, 679 (2019).

[15]

Feng, S. et al. Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell 55, 694-707 (2014).

[16]

Grob, S., Schmid, M. W. & Grossniklaus, U. Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol. Cell 55, 678-693 (2014).

[17]

Wang, C. et al. Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res. 25, 246-256 (2015).

[18]

Liu, C. et al. Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res. 26, 1057-1068 (2016).

[19]

Dong, P. et al. 3D chromatin architecture of large plant genomes determined by local A/B compartments. Mol. Plant 10, 1497-1509 (2017).

[20]

Liu, C., Cheng, Y.-J., Wang, J.-W. & Weigel, D. Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat. Plants 3, 742-748 (2017).

[21]

Wang, M. et al. Evolutionary dynamics of 3D genome architecture following polyploidization in cotton. Nat. Plants 4, 90 (2018).

[22]

Zhang, H. et al. The effects of Arabidopsis genome duplication on the chromatin organization and transcriptional regulation. Nucleic Acids Res. 47, 7857-7869 (2019).

[23]

Xie, T. et al. Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization. Nat. Plants 5, 822-832 (2019).

[24]

Doğan, E. S. & Liu, C. Three-dimensional chromatin packing and positioning of plant genomes. Nat. Plants 4, 521 (2018).

[25]

Jansson, S. & Douglas, C. J. Populus: a model system for plant biology. Annu. Rev. Plant Biol. 58, 435-458 (2007).

[26]

Wang, M. et al. Phylogenomics of the genus Populus reveals extensive interspecific gene flow and balancing selection. New Phytol. 225, 1370-1382 (2020).

[27]

Tuskan, G. A. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604 (2006).

[28]

Ma, T. et al. Genomic insights into salt adaptation in a desert poplar. Nat. Commun. 4, 1-9 (2013).

[29]

Yang, W. et al. The draft genome sequence of a desert tree Populus pruinosa. GigaScience 6, gix075 (2017).

[30]

Xin, H. et al. An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting. Plant J. 101, 253-264 (2020).

[31]

Chen, Z. et al. Survival in the Tropics despite isolation, inbreeding and asexual reproduction: insights from the genome of the world’s southernmost poplar (Populus ilicifolia). Plant J. 103, 430-442 (2020).

[32]

Rodgers-Melnick, E. et al. Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res. 22, 95-105 (2012).

[33]

Liu, Y. et al. Two highly similar poplar paleo-subgenomes suggest an autotetraploid ancestor of Salicaceae plants. Front. Plant Sci. 8, 571 (2017).

[34]

Zhang, L., Xi, Z., Wang, M., Guo, X. & Ma, T. Plastome phylogeny and lineage diversification of Salicaceae with focus on poplars and willows. Ecol. Evol. 8, 7817-7823 (2018).

[35]

Ma, J. et al. Genome sequence and genetic transformation of a widely distributed and cultivated poplar. Plant Biotechnol. J. 17, 451-460 (2019).

[36]

Yang, W. et al. A general model to explain repeated turnovers of sex determination in the Salicaceae. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msaa261 (2020).

[37]

Zhang, Z. et al. Improved genome assembly provides new insights into genome evolution in a desert poplar (Populus euphratica). Mol. Ecol. Res. 20, 781-794 (2020).

[38]

Tiang, C.-L., He, Y. & Pawlowski, W. P. Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants. Plant Physiol. 158, 26-34 (2012).

[39]

Schmitt, A. D., Hu, M. & Ren, B. Genome-wide mapping and analysis of chromosome architecture. Nat. Rev. Mol. Cell Biol. 17, 743 (2016).

[40]

Sexton, T. et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458-472 (2012).

[41]

Shin, H. et al. TopDom: an efficient and deterministic method for identifying topological domains in genomes. Nucleic Acids Res. 44, e70- e70 (2016).

[42]

Sotelo-Silveira, M., Montes, R. A. C., Sotelo-Silveira, J. R., Marsch-Martínez, N. & De Folter, S. Entering the next dimension: plant genomes in 3D. Trends Plant Sci. 23, 598-612 (2018).

[43]

Su, Y. et al. Single-base-resolution methylomes of Populus euphratica reveal the association between DNA methylation and salt stress. Tree Genet. Genomes 14, 86 (2018).

[44]

Porebski, S., Bailey, L. G. & Baum, B. R. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol. Biol. Report. 15, 8-15 (1997).

[45]

Chin, C. S. et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods 13, 1050-1054 (2016).

[46]

Chin, C. S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563 (2013).

[47]

Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).

[48]

Roach, M. J., Schmidt, S. A. & Borneman, A. R. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinformatics. 19, 460 (2018).

[49]

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357 (2012).

[50]

Servant, N. et al. HiC-Pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 16, 259 (2015).

[51]

Akdemir, K. C. & Chin, L. HiCPlotter integrates genomic data with interaction matrices. Genome Biol. 16, 198 (2015).

[52]

Servant, N. et al. HiTC: exploration of high-throughput ‘C’ experiments. Bioinformatics 28, 2843-2844 (2012).

[53]

Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 1-9 (2009).

[54]

Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49- e49 (2012).

[55]

Fischer, S. et al. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr. Protoc. Bioinformatics Chapter 6, Unit 6.12.1 (2011).

[56]

Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571-1572 (2011).

[57]

Wan, D. et al. Genome-wide identification of long noncoding RNAs (lncRNAs) and their responses to salt stress in two closely related poplars. Front. Genet. 10, 777 (2019).

[58]

Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357-360 (2015).

[59]

Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290 (2015).

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