Pan-genome and genomic variation analyses of Populus

CHU Chenchen, SUN Mingsheng, WU Yuhan, YAN Zhenyu, LI Ting, FENG Yangfan, GUO Ying, YIN Tongming, XUE Liangjiao

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6) : 251-260.

PDF(22965 KB)
PDF(22965 KB)
JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6) : 251-260. DOI: 10.12302/j.issn.1000-2006.202209037

Pan-genome and genomic variation analyses of Populus

Author information +
History +

Abstract

【Objective】Poplar trees are important for timber production, ecological protection and carbon sequestration, and also serve as a model for forest genetic research. The construction of poplar pangenome and analysis of genomic variations will provide a theoretical guidance for poplar precision breeding and pan-genome research of forest trees. 【Method】All published high-quality poplar genome sequences were collected for a comparative genomic analysis. Both small genomic variations and large structural variations were identified and compared. Gene-based and graph-based pan-genomes were constructed, respectively. 【Result】Genomic sequences of eight poplar species and three diploid or triploid poplar hybrids were collected. The three hybrids contained seven haplotype subgenome sequences. These sequences represented the genomic characteristics of the four poplar Sections well. The comparative genomic analysis showed that there were many structural variations among poplar genomes. In the gene-based Populus pan-genomes, syntenic core genes, nonsyntenic core genes, softcore genes, dispensable genes, and private genes account for 12.5%, 34.9%, 31.4%, 16.5% and 4.7% of the total genes, respectively. Among them, dispensable genes exhibit a high functional diversity. Based on the variations of genome sequences, the graph-based poplar pangenome was constructed, which greatly improved the efficiency of variation detection using NGS data. Two genomic loci associated with phenology were identified through variation hotspot analysis of pan-genome. 【Conclusion】A large amount of genomic structural variations were observed in the genomes of Populus genus, which increase the diversity of gene regulation and thus affect the growth traits of poplar trees. The genomic structural variations among poplar Sections may be related to phenological adaptation. Due to the genomic complexity of forest trees, several aspects need to be considered during the construction of forest pangenomes, such as the agreement of included genomes and research objectives. The results from gene- and graph-based pan-genomes can be combined to explore the genomic variation and evolution of forest trees.

Key words

Populus / pan-genome / structural variation / phenological candidate genes

Cite this article

Download Citations
CHU Chenchen , SUN Mingsheng , WU Yuhan , et al . Pan-genome and genomic variation analyses of Populus[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY. 2022, 46(6): 251-260 https://doi.org/10.12302/j.issn.1000-2006.202209037

References

[1]
TETTELIN H, MASIGNANI V, CIESLEWICZ M J, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae:implications for the microbial pan-genome[J]. Proc Natl Acad Sci USA, 2005, 102(39):13950-13955.DOI:10.1073/pnas.0506758102.
[2]
LI Y H, ZHOU G Y, MA J X, et al. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits[J]. Nat Biotechnol, 2014, 32(10):1045-1052.DOI:10.1038/nbt.2979.
[3]
HIRSCH C N, FOERSTER J M, JOHNSON J M, et al. Insights into the maize pan-genome and pan-transcriptome[J]. Plant Cell, 2014, 26(1):121-135.DOI:10.1105/tpc.113.119982.
[4]
SCHATZ M C, MARON L G, STEIN J C, et al. Whole genome de novo assemblies of three divergent strains of rice,Oryza sativa,document novel gene space of aus and indica[J]. Genome Biol, 2014, 15(11):506.DOI:10.1186/PREACCEPT-2784872521277375.
[5]
GOLICZ A A, BAYER P E, BARKER G C, et al. The pangenome of an agronomically important crop plant Brassica oleracea[J]. Nat Commun, 2016, 7:13390.DOI:10.1038/ncomms13390.
[6]
PINOSIO S, GIACOMELLO S, FAIVRE-RAMPANT P, et al. Characterization of the poplar pan-genome by genome-wide identification of structural variation[J]. Mol Biol Evol, 2016, 33(10):2706-2719.DOI:10.1093/molbev/msw161.
[7]
LIU Y C, DU H L, LI P C, et al. Pan-genome of wild and cultivated soybeans[J]. Cell, 2020, 182(1):162-176.e13.DOI:10.1016/j.cell.2020.05.023.
[8]
CAO K, PENG Z, ZHAO X, et al. Pan-genome analyses of peach and its wild relatives provide insights into the genetics of disease resistance and species adaptation[EB/OL]. (2020-09-13)[2022-10-05]. https://www.biorxiv.org/content/10.1101/2020.07.13.200204v1.abstract.
[9]
DIFAZIO S, SLAVOV G, JOSHI C. Populus:a premier pioneer system for plant genomics[C]// JOSHI C P,DIFAZIO S P,KOLE C. Genetics, Genomics and Breeding of Poplar. Enfield, USA: Science Publishers, 2011.
[10]
GA T, S D, S J, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray)[J]. Science, 2006, 313(5793): 1596-604.DOI:10.1126/science.1128691.
[11]
MA T, WANG J Y, ZHOU G K, et al. Genomic insights into salt adaptation in a desert poplar[J]. Nat Commun, 2013, 4:2797.DOI:10.1038/ncomms3797.
[12]
WANG J, DING J H, TAN B Y, et al. A major locus controls local adaptation and adaptive life history variation in a perennial plant[J]. Genome Biol, 2018, 19(1):72.DOI:10.1186/s13059-018-1444-y.
[13]
XUE L J, WU H T, CHEN Y N, et al. Evidences for a role of two Y-specific genes in sex determination in Populus deltoides[J]. Nat Commun, 2020, 11:5893.DOI:10.1038/s41467-020-19559-2.
[14]
BAI S J, WU H N, ZHANG J P, et al. Genome assembly of Salicaceae Populus deltoides (eastern cottonwood) I-69 based on nanopore sequencing and hi-C technologies[J]. J Hered, 2021, 112(3):303-310.DOI:10.1093/jhered/esab010.
[15]
WU H N, YAO D, CHEN Y H, et al. De novo genome assembly of Populus simonii further supports that Populus simonii and Populus trichocarpa belong to different sections[J]. G3 Genes|Genomes|Genetics, 2020, 10(2):455-466.DOI:10.1534/g3.119.400913.
[16]
YANG W L, WANG D Y, LI Y L, et al. A general model to explain repeated turnovers of sex determination in the Salicaceae[J]. Mol Biol Evol, 2020, 38(3):968-980.DOI:10.1093/molbev/msaa261.
[17]
LIU Y J, WANG X R, ZENG Q Y. De novo assembly of white poplar genome and genetic diversity of white poplar population in Irtysh River Basin in China[J]. Sci China Life Sci, 2019, 62(5):609-618.DOI:10.1007/s11427-018-9455-2.
[18]
ZHANG L, ZHAO J T, BI H, et al. Bioinformatic analysis of chromatin organization and biased expression of duplicated genes between two poplars with a common whole-genome duplication[J]. Hortic Res, 2021, 8:62.DOI:10.1038/s41438-021-00494-2.
[19]
LI Y, WANG D, WANG W, et al. A chromosome-level Populus qiongdaoensis genome assembly provides insights into tropical adaptation and a cryptic turnover of sex determination[J]. Mol Ecol, 2022:2022-06-17. DOI:10.1111/mec.16566.
[20]
QIU D Y, BAI S L, MA J C, et al. The genome of Populus alba × Populus tremula var.glandulosa clone 84K[J]. DNA Res, 2019, 26(5):423-431.DOI:10.1093/dnares/dsz020.
[21]
TONG S F, WANG Y B, CHEN N N, et al. PtoNF-YC9-SRMT-PtoRD26 module regulates the high saline tolerance of a triploid poplar[J]. Genome Biol, 2022, 23(1):148.DOI:10.1186/s13059-022-02718-7.
[22]
ZHANG B Y, ZHU W X, DIAO S, et al. The poplar pangenome provides insights into the evolutionary history of the genus[J]. Commun Biol, 2019, 2:215.DOI:10.1038/s42003-019-0474-7.
[23]
LI H, FENG X W, CHU C. The design and construction of reference pangenome graphs with minigraph[J]. Genome Biol, 2020, 21(1):265.DOI:10.1186/s13059-020-02168-z.
[24]
QIN P, LU H W, DU H L, et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations[J]. Cell, 2021, 184(13):3542-3558.e16.DOI:10.1016/j.cell.2021.04.046.
[25]
TAO Y F, LUO H, XU J B, et al. Extensive variation within the pan-genome of cultivated and wild sorghum[J]. Nat Plants, 2021, 7(6):766-773.DOI:10.1038/s41477-021-00925-x.
[26]
ZHOU Y, ZHANG Z Y, BAO Z G, et al. Graph pangenome captures missing heritability and empowers tomato breeding[J]. Nature, 2022, 606(7914):527-534.DOI:10.1038/s41586-022-04808-9.
[27]
ZHANG Z Y, CHEN Y, ZHANG J L, et al. Improved genome assembly provides new insights into genome evolution in a desert poplar (Populus euphratica)[J]. Mol Ecol Resour, 2020, 20(3):781-794.DOI:10.1111/1755-0998.13142.
[28]
EVANS L M, SLAVOV G T, RODGERS-MELNICK E, et al. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations[J]. Nat Genet, 2014, 46(10):1089-1096.DOI:10.1038/ng.3075.
[29]
AN X M, GAO K, CHEN Z, et al. High quality haplotype-resolved genome assemblies of Populus tomentosa Carr.: a stabilized interspecific hybrid species widespread in Asia[J]. Mol Ecol Resour, 2022, 22(2):786-802.DOI:10.1111/1755-0998.13507.
[30]
BOLGER A M, LOHSE M, USADEL B. Trimmomatic: a flexible trimmer for Illumina sequence data[J]. Bioinformatics, 2014, 30(15):2114-2120.DOI:10.1093/bioinformatics/btu170.
[31]
SIMÃO F A, WATERHOUSE R M, IOANNIDIS P, et al. BUSCO:assessing genome assembly and annotation completeness with single-copy orthologs[J]. Bioinformatics, 2015, 31(19):3210-3212.DOI:10.1093/bioinformatics/btv351.
[32]
EMMS D M, KELLY S. OrthoFinder:solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy[J]. Genome Biol, 2015, 16(1):157.DOI:10.1186/s13059-015-0721-2.
[33]
SANDERSON M J. Estimating absolute rates of molecular evolution and divergence times:a penalized likelihood approach[J]. Mol Biol Evol, 2002, 19(1):101-9.
[34]
DE BIE T, CRISTIANINI N, DEMUTH J P, et al. CAFE:a computational tool for the study of gene family evolution[J]. Bioinformatics, 2006, 22(10):1269-1271.DOI:10.1093/bioinformatics/btl097.
[35]
TANG D, JIA Y X, ZHANG J Z, et al. Addendum:genome evolution and diversity of wild and cultivated potatoes[J]. Nature, 2022, 609(7929):E14.DOI:10.1038/s41586-022-05298-5.
[36]
WANG Y P, TANG H B, DEBARRY J D, et al. MCScanX:a toolkit for detection and evolutionary analysis of gene synteny and collinearity[J]. Nucleic Acids Res, 2012, 40(7):e49.DOI:10.1093/nar/gkr1293.
[37]
ALEXA A, RAHNENFUHRER J. topGO: enrichment analysis for gene ontology. R package version 2.36.0.[EB/OL].[2022-09-12]. https://bioconductor.org/packages/release/bioc/html/topGO.html
[38]
YU G C, WANG L G, HAN Y Y, et al. clusterProfiler:an R package for comparing biological themes among gene clusters[J]. OMICS, 2012, 16(5):284-287.DOI:10.1089/omi.2011.0118.
[39]
MARÇAIS G, DELCHER A L, PHILLIPPY A M, et al. MUMmer4:a fast and versatile genome alignment system[J]. PLoS Comput Biol, 2018, 14(1):e1005944.DOI:10.1371/journal.pcbi.1005944.
[40]
GOEL M, SUN H Q, JIAO W B, et al. SyRI:finding genomic rearrangements and local sequence differences from whole-genome assemblies[J]. Genome Biol, 2019, 20(1):277.DOI:10.1186/s13059-019-1911-0.
[41]
GARRISON E, SIRÉN J, NOVAK A M, et al. Variation graph toolkit improves read mapping by representing genetic variation in the reference[J]. Nat Biotechnol, 2018, 36(9):875-879.DOI:10.1038/nbt.4227.
[42]
CHEN K Y. Type Ⅱ Mads-box genes associated with poplar apical bud development and dormancy[D]. Maryland: University of Maryland, 2008.
[43]
LI W, LIU J N, ZHANG H Y, et al. Plant pan-genomics:recent advances,new challenges,and roads ahead[J]. J Genet Genom, 2022, 49(9):833-846.DOI:10.1016/j.jgg.2022.06.004.
[44]
GUI S T, WEI W J, JIANG C L, et al. A pan-Zea genome map for enhancing maize improvement[J]. Genome Biol, 2022, 23(1):178.DOI:10.1186/s13059-022-02742-7.
PDF(22965 KB)

Accesses

Citation

Detail

Sections
Recommended
The full text is translated into English by AI, aiming to facilitate reading and comprehension. The core content is subject to the explanation in Chinese.

/