The pan-tandem repeat map highlights multiallelic variants underlying gene expression and agronomic traits in rice.

Oryza / genetics Quantitative Trait Loci Alleles Gene Expression Regulation, Plant Genome, Plant Tandem Repeat Sequences / genetics Chromosome Mapping Polymorphism, Single Nucleotide Phenotype Genetic Variation

Journal

Nature communications

ISSN: 2041-1723

Titre abrégé: Nat Commun

Pays: England

ID NLM: 101528555

Informations de publication

Date de publication:
24 Aug 2024

Historique:

received: 23 06 2023

accepted: 20 08 2024

medline: 26 8 2024

pubmed: 26 8 2024

entrez: 24 8 2024

Statut: epublish

Résumé

Tandem repeats (TRs) are genomic regions that tandemly change in repeat number, which are often multiallelic. Their characteristics and contributions to gene expression and quantitative traits in rice are largely unknown. Here, we survey rice TR variations based on 231 genome assemblies and the rice pan-genome graph. We identify 227,391 multiallelic TR loci, including 54,416 TR variations that are absent from the Nipponbare reference genome. Only 1/3 TR variations show strong linkage with nearby bi-allelic variants (SNPs, Indels and PAVs). Using 193 panicle and 202 leaf transcriptomic data, we reveal 485 and 511 TRs act as QTLs independently of other bi-allelic variations to nearby gene expression, respectively. Using plant height and grain width as examples, we identify and validate TRs contributions to rice agronomic trait variations. These findings would enhance our understanding of the functions of multiallelic variants and facilitate rice molecular breeding.

Identifiants

DOI: 10.1038/s41467-024-51854-0 PMID: 39181885

pubmed: 39181885

doi: 10.1038/s41467-024-51854-0

pii: 10.1038/s41467-024-51854-0

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

7291

Subventions

Organisme : Youth Innovation Promotion Association of the Chinese Academy of Sciences (Youth Innovation Promotion Association CAS)

ID : Y2023QC36

Informations de copyright

Références

Albert, F. W. & Leonid, K. The role of regulatory variation in complex traits and disease. Nat. Rev. Genet. 16, 197–212 (2015).

pubmed: 25707927 doi: 10.1038/nrg3891

Song, X. G. et al. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res. 27, 1128–1141 (2017).

pubmed: 28809396 pmcid: 5587847 doi: 10.1038/cr.2017.102

Zhang, L. et al. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat. Commun. 8, 14789 (2017).

pubmed: 28317902 pmcid: 5364388 doi: 10.1038/ncomms14789

Zhou, J. P. et al. An efficient CRISPR-Cas12a promoter editing system for crop improvement. Nat. Plants 9, 588–604 (2023).

pubmed: 37024659 doi: 10.1038/s41477-023-01384-2

Xue, C. X. et al. Tuning plant phenotypes by precise, graded downregulation of gene expression. Nat. Biotechnol. 41, 1758–1764 (2023).

pubmed: 36894598 doi: 10.1038/s41587-023-01707-w

Wainschtein, P. et al. Assessing the contribution of rare variants to complex trait heritability from whole-genome sequence data. Nat. Genet. 54, 263–273 (2022).

pubmed: 35256806 pmcid: 9119698 doi: 10.1038/s41588-021-00997-7

Tautz, D. Notes on the definition and nomenclature of tandemly repetitive DNA sequences. Exs 67, 21–28 (1993).

pubmed: 8400689

Depienne, C. & Mandel, J. L. 30 years of repeat expansion disorders: What have we learned and what are the remaining challenges? Am. J. Hum. Genet. 108, 764–785 (2021).

pubmed: 33811808 pmcid: 8205997 doi: 10.1016/j.ajhg.2021.03.011

Fotsing, S. F. et al. The impact of short tandem repeat variation on gene expression. Nat. Genet. 51, 1652–1659 (2019).

pubmed: 31676866 pmcid: 6917484 doi: 10.1038/s41588-019-0521-9

Bakhtiari, M. et al. Variable number tandem repeats mediate the expression of proximal genes. Nat. Commun. 12, 2075 (2021).

pubmed: 33824302 pmcid: 8024321 doi: 10.1038/s41467-021-22206-z

Wu, Z. Z. et al. Mapping short tandem repeats for liver gene expression traits helps prioritize potential causal variants for complex traits in pigs. J. Anim. Sci. Biotechnol. 13, 8 (2022).

pubmed: 35034641 pmcid: 8762894 doi: 10.1186/s40104-021-00658-z

Zhang, G. T. & Andersen, E. C. Interplay Between Polymorphic Short Tandem Repeats and Gene Expression Variation in Caenorhabditis elegans. Mol. Biol. Evol. 40, msad067 (2023).

pubmed: 36999565 pmcid: 10075192 doi: 10.1093/molbev/msad067

Ranathunge, C. et al. Transcribed microsatellite allele lengths are often correlated with gene expression in natural sunflower populations. Mol. Ecol. 29, 1704–1716 (2020).

pubmed: 32285554 doi: 10.1111/mec.15440

Reinar, W. B., Lalun VO, Reitan, T., Jakobsen, K. S. & Butenko, M. A. Length variation in short tandem repeats affects gene expression in natural populations of Arabidopsis thaliana. Plant Cell 33, 2221–2234 (2021).

pubmed: 33848350 pmcid: 8364236 doi: 10.1093/plcell/koab107

Shi, Y. et al. Characterization of genome-wide STR variation in 6487 human genomes. Nat. Commun. 14, 2092 (2023).

pubmed: 37045857 pmcid: 10097659 doi: 10.1038/s41467-023-37690-8

Mukamel, R. E. et al. Protein-coding repeat polymorphisms strongly shape diverse human phenotypes. Science 373, 1499–1505 (2021).

pubmed: 34554798 pmcid: 8549062 doi: 10.1126/science.abg8289

Kaur, S., Panesar, P. S., Bera, M. B. & Kaur, V. Simple Sequence Repeat Markers in Genetic Divergence and Marker-Assisted Selection of Rice Cultivars: A Review. Crit. Rev. Food Sci. Nutr. 55, 41–49 (2015).

pubmed: 24915404 doi: 10.1080/10408398.2011.646363

Si, L. Z. et al. OsSPL13 controls grain size in cultivated rice. Nat. Genet. 48, 447–456 (2016).

pubmed: 26950093 doi: 10.1038/ng.3518

Bai, X. et al. Duplication of an upstream silencer of FZP increases grain yield in rice. Nat. Plants 3, 885–893 (2017).

pubmed: 29085070 doi: 10.1038/s41477-017-0042-4

Huang, Y. Y. et al. Variation in the regulatory region of FZP causes increases in secondary inflorescence branching and grain yield in rice domestication. Plant J. 96, 716–733 (2018).

pubmed: 30101570 doi: 10.1111/tpj.14062

Li, Z. et al. Natural variation of codon repeats in COLD11 endows rice with chilling resilience. Sci. Adv. 9, eabq5506 (2023).

pubmed: 36608134 pmcid: 9821855 doi: 10.1126/sciadv.abq5506

Zhao, F. et al. A genome-wide survey of copy number variations reveals an asymmetric evolution of duplicated genes in rice. BMC Biol. 18, 73 (2020).

pubmed: 32591023 pmcid: 7318451 doi: 10.1186/s12915-020-00798-0

Qin, P. et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell 184, 3542–3558 e3516 (2021).

pubmed: 34051138 doi: 10.1016/j.cell.2021.04.046

Rajan-Babu IS, Dolzhenko, E., Eberle, M. A. & Friedman, J. M. Sequence composition changes in short tandem repeats: heterogeneity, detection, mechanisms and clinical implications. Nat. Rev. Genet. 25, 476–499 (2024).

pubmed: 38467784 doi: 10.1038/s41576-024-00696-z

Willems, T. et al. Genome-wide profiling of heritable and de novo STR variations. Nat. Methods 14, 590–592 (2017).

pubmed: 28436466 pmcid: 5482724 doi: 10.1038/nmeth.4267

Gymrek, M., Golan, D., Rosset, S. & Erlich, Y. lobSTR: A short tandem repeat profiler for personal genomes. Genome Res. 22, 1154–1162 (2012).

pubmed: 22522390 pmcid: 3371701 doi: 10.1101/gr.135780.111

Kristmundsdóttir, S., Sigurpálsdóttir, B. D., Kehr, B. & Halldórsson, B. V. popSTR: population-scale detection of STR variants. Bioinformatics 33, 4041–4048 (2017).

pubmed: 27591079 doi: 10.1093/bioinformatics/btw568

Mousavi, N., Shleizer-Burko, S., Yanicky, R. & Gymrek, M. Profiling the genome-wide landscape of tandem repeat expansions. Nucleic Acids Res. 47, e90 (2019).

pubmed: 31194863 pmcid: 6735967 doi: 10.1093/nar/gkz501

Dolzhenko, E. et al. ExpansionHunter: a sequence-graph-based tool to analyze variation in short tandem repeat regions. Bioinformatics 35, 4754–4756 (2019).

pubmed: 31134279 pmcid: 6853681 doi: 10.1093/bioinformatics/btz431

Bakhtiari, M., Shleizer-Burko, S., Gymrek, M., Bansal, V. & Bafna, V. Targeted genotyping of variable number tandem repeats with adVNTR. Genome Res. 28, 1709–1719 (2018).

pubmed: 30352806 pmcid: 6211647 doi: 10.1101/gr.235119.118

Lu, T. Y., Chaisson, M. J. P. & Human Genome Struct Variation C. Profiling variable-number tandem repeat variation across populations using repeat-pangenome graphs. Nat. Commun. 12, 4250 (2021).

pubmed: 34253730 pmcid: 8275641 doi: 10.1038/s41467-021-24378-0

Chintalaphani, S. R., Pineda, S. S., Deveson, I. W. & Kumar, K. R. An update on the neurological short tandem repeat expansion disorders and the emergence of long-read sequencing diagnostics. Acta Neuropathol. Commun. 9, 2–20 (2021).

doi: 10.1186/s40478-021-01201-x

De Coster, W., Weissensteiner, M. H. & Sedlazeck, F. J. Towards population-scale long-read sequencing. Nat. Rev. Genet. 22, 572–587 (2021).

pubmed: 34050336 pmcid: 8161719 doi: 10.1038/s41576-021-00367-3

Shang, L. et al. A super pan-genomic landscape of rice. Cell Res. 32, 878–896 (2022).

pubmed: 35821092 pmcid: 9525306 doi: 10.1038/s41422-022-00685-z

Kawahara, Y. et al. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6, 2–10 (2013).

doi: 10.1186/1939-8433-6-4

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

pubmed: 9862982 pmcid: 148217 doi: 10.1093/nar/27.2.573

Olson, D. & Wheeler, T. ULTRA: A model based tool to detect tandem repeats. ACM BCB 2018, 37–46 (2018).

pubmed: 31080962 pmcid: 6508075

Yu, J. et al. The genomes of Oryza sativa: A history of duplications. Plos Biol. 3, 266–281 (2005).

doi: 10.1371/journal.pbio.0030038

Mei, H. et al. Population-scale polymorphic short tandem repeat provides an alternative strategy for allele mining in cotton. Front. Plant Sci. 13, 916830 (2022).

pubmed: 35599867 pmcid: 9120961 doi: 10.3389/fpls.2022.916830

Zhang, G. T., Wang, Y. & Andersen, E. C. Natural variation in C. elegans short tandem repeats. Genome Res. 32, 1852–1861 (2022).

pubmed: 36195344 pmcid: 9712632

Zhang, H. et al. Population-level exploration of alternative splicing and its unique role in controlling agronomic traits of rice. Plant Cell, koae181, https://doi.org/10.1093/plcell/koae181 (2024).

Liu, T. Z. et al. Dwarf and High Tillering1 represses rice tillering through mediating the splicing of D14 pre-mRNA. Plant Cell 34, 3301–3318 (2022).

pubmed: 35670739 pmcid: 9421477 doi: 10.1093/plcell/koac169

Song, X. J. et al. Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc. Natl Acad. Sci. USA 112, 76–81 (2015).

pubmed: 25535376 doi: 10.1073/pnas.1421127112

Dong, N. Q. et al. UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice. Nat. Commun. 11, 2629 (2020).

pubmed: 32457405 pmcid: 7250897 doi: 10.1038/s41467-020-16403-5

Rabello, A. R. et al. Identification of drought-responsive genes in roots of upland rice (Oryza sativa L). BMC Genomics 9, 485 (2008).

pubmed: 18922162 pmcid: 2605477 doi: 10.1186/1471-2164-9-485

Wang, G., Sarkar, A., Carbonetto, P. & Stephens, M. A simple new approach to variable selection in regression, with application to genetic fine mapping. J. R. Stat. Soc. Ser. B Stat. Methodol. 82, 1273–1300 (2020).

doi: 10.1111/rssb.12388

Wang, Y. P. et al. Clock component OsPRR59 delays heading date by repressing transcription of Ehd3 in rice. Crop J. 10, 1570–1579 (2022).

doi: 10.1016/j.cj.2022.04.007

Yan, W. H. et al. Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice. Cell Res. 23, 969–971 (2013).

pubmed: 23507971 pmcid: 3698629 doi: 10.1038/cr.2013.43

Duan, P. G. et al. Natural Variation in the Promoter of GSE5 Contributes to Grain Size Diversity in Rice. Mol. Plant 10, 685–694 (2017).

pubmed: 28366824 doi: 10.1016/j.molp.2017.03.009

Rook, F. et al. Impaired sucrose induction1 encodes a conserved plant-specific protein that couples carbohydrate availability to gene expression and plant growth. Plant J. 46, 1045–1058 (2006).

pubmed: 16805736 doi: 10.1111/j.1365-313X.2006.02765.x

Malik, I., Kelley, C. P., Wang, E. T. & Todd, P. K. Molecular mechanisms underlying nucleotide repeat expansion disorders. Nat. Rev. Mol. Cell Biol. 22, 589–607 (2021).

pubmed: 34140671 pmcid: 9612635 doi: 10.1038/s41580-021-00382-6

Ming, L. et al. Transcriptome-wide association analyses reveal the impact of regulatory variants on rice panicle architecture and causal gene regulatory networks. Nat. Commun. 14, 7501 (2023).

pubmed: 37980346 pmcid: 10657423 doi: 10.1038/s41467-023-43077-6

Liu, C. et al. eQTLs play critical roles in regulating gene expression and identifying key regulators in rice. Plant Biotechnol. J. 19, 2357 (2022).

doi: 10.1111/pbi.13912

Elden, A. C. et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 466, 1069–U1077 (2010).

pubmed: 20740007 pmcid: 2965417 doi: 10.1038/nature09320

Lee, T. et al. Ataxin-2 intermediate-length polyglutamine expansions in European ALS patients. Hum. Mol. Genet. 20, 1697–1700 (2011).

pubmed: 21292779 pmcid: 3071667 doi: 10.1093/hmg/ddr045

Quinlan, A. R. BEDTools: The Swiss-Army Tool for Genome Feature Analysis. Curr. Protoc. Bioinforma. 47, 11.12.11–34 (2014).

doi: 10.1002/0471250953.bi1112s47

Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191

Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).

pubmed: 33590861 pmcid: 7931819 doi: 10.1093/gigascience/giab008

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

pubmed: 2231712 doi: 10.1016/S0022-2836(05)80360-2

Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).

pubmed: 21988835 pmcid: 3261699 doi: 10.1038/msb.2011.75

Kendig, K. I. et al. Sentieon DNASeq Variant Calling Workflow Demonstrates Strong Computational Performance and Accuracy. Front. Genet. 10, 736 (2019).

pubmed: 31481971 pmcid: 6710408 doi: 10.3389/fgene.2019.00736

Sedlazeck, F. J. et al. Accurate detection of complex structural variations using single-molecule sequencing. Nat. Methods 15, 461 (2018).

pubmed: 29713083 pmcid: 5990442 doi: 10.1038/s41592-018-0001-7

Jeffares, D. C. et al. Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast. Nat. Commun. 8, 14061 (2017).

pubmed: 28117401 pmcid: 5286201 doi: 10.1038/ncomms14061

Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

pubmed: 23618408 pmcid: 4053844 doi: 10.1186/gb-2013-14-4-r36

Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).

pubmed: 22383036 pmcid: 3334321 doi: 10.1038/nprot.2012.016

Gymrek, M. et al. Abundant contribution of short tandem repeats to gene expression variation in humans. Nat. Genet. 48, 22–29 (2016).

pubmed: 26642241 doi: 10.1038/ng.3461

Stegle, O., Parts, L., Piipari, M., Winn, J. & Durbin, R. Using probabilistic estimation of expression residuals (PEER) to obtain increased power and interpretability of gene expression analyses. Nat. Protoc. 7, 500–507 (2012).

pubmed: 22343431 pmcid: 3398141 doi: 10.1038/nprot.2011.457

Ma, X. L. et al. A Robust CRISPR/Cas9 System for Convenient, High-Efficiency Multiplex Genome Editing in Monocot and Dicot Plants. Mol. Plant 8, 1274–1284 (2015).

pubmed: 25917172 doi: 10.1016/j.molp.2015.04.007