The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.
A pan-genome framework reveals structural variation and small RNA regulation underlying heterodichogamy in Pterocarya
Open accessPublished version of a preprint
Abstract
Heterodichogamy, characterized by reciprocal timing of male and female flowering, promotes disassortative mating yet remains poorly understood at the genomic level. Here, we investigated this mating system in Pterocarya, a genus within Juglandaceae, using a low-input pan-genome framework that integrates phased assemblies with population resequencing. We identified a deeply divergent 78-kb locus associated with mating morphs in P. stenoptera, marked by repeat-rich structural variants and containing a FAF-like gene linked to floral development. This region also produces small RNAs that potentially regulate key floral and hormonal pathways, suggesting pleiotropic trans-regulatory effects. Comparative analyses reveal that although the loci controlling heterodichogamy in Juglans, Carya, and Pterocarya are non-homologous, they appear to share convergent evolutionary solutions involving tandem repeats or transposable element (TE) insertions. Our study uncovers the genomic basis of heterodichogamy in Pterocarya and underscores the utility of pan-genome approaches for dissecting structural variation-associated traits.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
The design and construction of reference pangenome graphs with minigraph
Li, H., Feng, X., & Chu, C. (2020) · Genome Biology · doi:10.1186/s13059-020-02168-z · Cited by 455
Pangenomics enables genotyping of known structural variants in 5202 diverse genomes
Sirén, J., Monlong, J., Chang, X., Novak, A. M., Eizenga, J. M., Markello, C., Sibbesen, J. A., Hickey, G., Chang, P.-C., Carroll, A., et al. (2021) · Science · doi:10.1126/science.abg8871 · Cited by 400
Flagged first, then by citations
Research works printed but not linked: 87
- Studer, 2011, Identification of a functional transposon insertion in the maize domestication gene tb1, Nat. Genet., 43, 1160, 10.1038/ng.942 · DOI
- Todesco, 2020, Massive haplotypes underlie ecotypic differentiation in sunflowers, Nature, 584, 602, 10.1038/s41586-020-2467-6 · DOI · Paper page
- She, 2024, Pan-genome analysis of 13 Spinacia accessions reveals structural variations associated with sex chromosome evolution and domestication traits in spinach, Plant Biotechnol. J., 22, 3102, 10.1111/pbi.14433 · DOI
- Hu, 2022, Amborella gene presence/absence variation is associated with abiotic stress responses that may contribute to environmental adaptation, New Phytol., 233, 1548, 10.1111/nph.17658 · DOI
- Gutiérrez-Valencia, 2022, Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level, Curr. Biol., 32, 4360, 10.1016/j.cub.2022.08.042 · DOI
- Zervakis, 2025, Genomic studies in Linum shed light on the evolution of the distyly supergene and the molecular basis of convergent floral evolution, New Phytol., 247, 2964, 10.1111/nph.70392 · DOI
- Mora-Carrera, 2025, Genomic patterns of loss of distyly and polyploidization in primroses, Mol. Biol. Evol., 42, 10.1093/molbev/msaf162 · DOI
- Yuan, 2025, Genomic evidence unveils the genetic architecture and evolution of the S-locus controlling heterostyly in Rubiaceae, New Phytol., 247, 1925, 10.1111/nph.70311 · DOI
- Shang, 2025, Converging on long and short: The genetics, molecular biology and evolution of heterostyly, Curr. Opin. Plant Biol., 85, 10.1016/j.pbi.2025.102731 · DOI
- Kafkas, 2023, Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution, Plant Commun., 4, 10.1016/j.xplc.2022.100497 · DOI
- Akagi, 2025, Rapid and dynamic evolution of a giant Y chromosome in Silene latifolia, Science, 387, 637, 10.1126/science.adk9074 · DOI
- Xue, 2025, The genomic basis of the tristylous floral polymorphism – evidence for a role of gene duplications in a region of restricted recombination, Mol. Biol. Evol., 42, 10.1093/molbev/msaf170 · DOI
- Kimura, 2003, Flowering system of heterodichogamous Juglans ailanthifolia, Plant Species Biol., 18, 75, 10.1111/j.1442-1984.2003.00088.x · DOI
- Bai, 2007, Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae), New Phytol., 176, 699, 10.1111/j.1469-8137.2007.02202.x · DOI
- Bai, 2006, Flowering phenology and wind-pollination efficacy of heterodichogamous Juglans mandshurica (Juglandaceae), Ann. Bot., 98, 397, 10.1093/aob/mcl111 · DOI
- Liu, 2016, A review on flowering mechanism in heterodichogamous plants, J. Nanjing For. Univ. Nat. Sci. Ed., 40, 147
- Endress, 2020, Structural and temporal modes of heterodichogamy and similar patterns across angiosperms, Bot. J. Linn. Soc., 193, 5, 10.1093/botlinnean/boaa001 · DOI
- Renner, 2001, How common is heterodichogamy?, Trends Ecol. Evol., 16, 595, 10.1016/S0169-5347(01)02280-7 · DOI
- Gleeson, 1982, Heterodichogamy in walnuts: Inheritance and stable ratios, Evolution, 36, 892, 10.1111/j.1558-5646.1982.tb05461.x · DOI
- Groh, 2025, Ancient structural variants control sex-specific flowering time morphs in walnuts and hickories, Science, 387, 10.1126/science.ado5578 · DOI
- Manos, 2007, Phylogeny of extant and fossil Juglandaceae inferred from the integration of molecular and morphological data sets, Syst. Biol., 56, 412, 10.1080/10635150701408523 · DOI
- Li, 2021, Physiological and transcriptional changes provide insights into the effect of root waterlogging on the aboveground part of Pterocarya stenoptera, Genomics, 113, 2583, 10.1016/j.ygeno.2021.06.005 · DOI
- Song, 2020, Phylogeny, taxonomy, and biogeography of Pterocarya (Juglandaceae), Plants (Basel), 9
- Song, 2021, Past, present and future suitable areas for the relict tree Pterocarya fraxinifolia (Juglandaceae): Integrating fossil records, niche modeling, and phylogeography for conservation, Eur. J. Forest. Res., 140, 1323, 10.1007/s10342-021-01397-6 · DOI
- Wang, 2023, Adaptive divergence and genetic vulnerability of relict species under climate change: a case study of Pterocarya macroptera, Ann. Bot., 132, 241, 10.1093/aob/mcad083 · DOI
- Thompson, 1985, Inheritance of heterodichogamy in pecan, J. Hered., 76, 456, 10.1093/oxfordjournals.jhered.a110144 · DOI
- Yu, 2023, Genomic insights into biased allele loss and increased gene numbers after genome duplication in autotetraploid Cyclocarya paliurus, BMC Biol., 21
- Zhang, 2024, Multi-omics analyses provide insights into the evolutionary history and the synthesis of medicinal components of the Chinese wingnut, Plant Divers., 46, 309, 10.1016/j.pld.2024.03.010 · DOI
- Manni, 2021, BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes, Mol. Biol. Evol., 38, 4647, 10.1093/molbev/msab199 · DOI · Paper page
- Ou, 2018, Assessing genome assembly quality using the LTR Assembly Index (LAI), Nucleic Acids Res., 46
- Wahl, 2010, The FANTASTIC FOUR proteins influence shoot meristem size in Arabidopsis thaliana, BMC Plant Biol., 10, 10.1186/1471-2229-10-285 · DOI
- Shang, 2024, CRISPR/Cas9-mediated mutations of FANTASTIC FOUR gene family for creating early flowering mutants in tomato, Plant Biotechnol. J., 22, 774, 10.1111/pbi.14223 · DOI
- Zhang, 2024, EARLY FLOWERING is a dominant gain-of-function allele of FANTASTIC FOUR 1/2c that promotes early flowering in tomato, Plant Biotechnol. J., 22, 698, 10.1111/pbi.14217 · DOI
- Bousios, 2016, A role for palindromic structures in the cis-region of maize Sirevirus LTRs in transposable element evolution and host epigenetic response, Genome Res., 26, 226, 10.1101/gr.193763.115 · DOI
- Xing, 2018, Arabidopsis O-GlcNAc transferase SEC activates histone methyltransferase ATX1 to regulate flowering, EMBO J., 37, 10.15252/embj.201798115 · DOI
- Chowdhury, 2022, How Arabidopsis receptor-like kinase 7 (RLK7) manifests: delineating its structure and function, Adv. Agric., 2022, 1
- Cui, 2022, Receptor-like protein kinases in plant reproduction: Current understanding and future perspectives, Plant Commun., 3, 10.1016/j.xplc.2021.100273 · DOI
- Xu, 2023, ETHYLENE INSENSITIVE3/EIN3-LIKE1 modulate FLOWERING LOCUS C expression via histone demethylase interaction, Plant Physiol., 192, 2290, 10.1093/plphys/kiad131 · DOI
- Okushima, 2007, ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis, Plant Cell, 19, 118, 10.1105/tpc.106.047761 · DOI
- Wang, 2015, Salt-related MYB1 coordinates abscisic acid biosynthesis and signaling during salt stress in Arabidopsis, Plant Physiol., 169, 1027, 10.1104/pp.15.00962 · DOI
- Raimondeau, 2024, A hemizygous supergene controls homomorphic and heteromorphic self-incompatibility systems in Oleaceae, Curr. Biol., 34, 1977, 10.1016/j.cub.2024.03.029 · DOI
- Hyden, 2023, Structural variation of a sex-linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea, New Phytol., 238, 2512, 10.1111/nph.18853 · DOI
- Groh, 2025, Distinct haplotypes and reversed dominance at a single-gene balanced polymorphism controlling heterodichogamous flowering in two genera of wingnuts, Curr. Biol., 10.1016/j.cub.2025.09.061 · DOI
- Muyle, 2017, The evolution of sex chromosomes and dosage compensation in plants, Genome Biol. Evol., 9, 627, 10.1093/gbe/evw282 · DOI
- Billiard, 2011, Evidence for Fisher’s dominance theory: how many ‘special cases’?, Trends Genet., 27, 441, 10.1016/j.tig.2011.06.005 · DOI
- Llaurens, 2009, Evolution of dominance in sporophytic self-incompatibility systems: I. Genetic load and coevolution of levels of dominance in pollen and pistil, Evolution, 63, 2427, 10.1111/j.1558-5646.2009.00709.x · DOI
- Tarutani, 2010, Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility, Nature, 466, 983, 10.1038/nature09308 · DOI
- Durand, 2014, Dominance hierarchy arising from the evolution of a complex small RNA regulatory network, Science, 346, 1200, 10.1126/science.1259442 · DOI
- Luo, 2022, Domestication and selection footprints in Persian walnuts (Juglans regia), PLoS Genet., 18, 10.1371/journal.pgen.1010513 · DOI
- Stevens, 2018, Genomic variation among and within six Juglans species, G3 (Bethesda), 8, 2153, 10.1534/g3.118.200030 · DOI
- Cheng, 2022, Haplotype-resolved assembly of diploid genomes without parental data, Nat. Biotechnol., 40, 1332, 10.1038/s41587-022-01261-x · DOI
- Cheng, 2021, Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm, Nat. Methods, 18, 170, 10.1038/s41592-020-01056-5 · DOI · Paper page
- Durand, 2016, Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments, Cell Syst., 3, 95, 10.1016/j.cels.2016.07.002 · DOI
- Dudchenko, 2017, De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds, Science, 356, 92, 10.1126/science.aal3327 · DOI
- Lin, 2023, quarTeT: a telomere-to-telomere toolkit for gap-free genome assembly and centromeric repeat identification, Hortic. Res., 10, 10.1093/hr/uhad127 · DOI
- Alonge, 2022, Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing, Genome Biol., 23, 10.1186/s13059-022-02823-7 · DOI
- Ou, 2019, Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline, Genome Biol., 20, 10.1186/s13059-019-1905-y · DOI
- Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 · DOI · Paper page
- Li, 2013, Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM, arXiv
- Danecek, 2021, Twelve years of SAMtools and BCFtools, GigaScience, 10, 10.1093/gigascience/giab008 · DOI
- McKenna, 2010, The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res., 20, 1297, 10.1101/gr.107524.110 · DOI · Paper page
- Zheng, 2024, A sequence-aware merger of genomic structural variations at population scale, Nat. Commun., 15
- Garrison, 2018, Variation graph toolkit improves read mapping by representing genetic variation in the reference, Nat. Biotechnol., 36, 875, 10.1038/nbt.4227 · DOI · Paper page
- Hickey, 2020, Genotyping structural variants in pangenome graphs using the vg toolkit, Genome Biol., 21, 10.1186/s13059-020-1941-7 · DOI · Paper page
- Sayers, 2022, Database resources of the national center for biotechnology information, Nucleic Acids Res., 50, D20, 10.1093/nar/gkab1112 · DOI · Paper page
- Lorenz, 2011, ViennaRNA Package 2.0, Algorithms Mol. Biol., 6, 10.1186/1748-7188-6-26 · DOI · Paper page
- Marçais, 2018, MUMmer4: A fast and versatile genome alignment system, PLoS Comput. Biol., 14, 10.1371/journal.pcbi.1005944 · DOI · Paper page
- Ginestet, 2011, ggplot2: elegant graphics for data analysis, J. R. Stat. Soc. A, 174, 245, 10.1111/j.1467-985X.2010.00676_9.x · DOI
- Darling, 2004, Mauve: multiple alignment of conserved genomic sequence with rearrangements, Genome Res., 14, 1394, 10.1101/gr.2289704 · DOI · Paper page
- Chang, 2015, Second-generation PLINK: rising to the challenge of larger and richer datasets, GigaScience, 4, 10.1186/s13742-015-0047-8 · DOI · Paper page
- Yin, 2021, rMVP: A memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study, Genomics Proteomics Bioinformatics, 19, 619, 10.1016/j.gpb.2020.10.007 · DOI
- Danecek, 2011, The variant call format and VCFtools, Bioinformatics., 27, 2156, 10.1093/bioinformatics/btr330 · DOI
- Katoh, 2013, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol., 30, 772, 10.1093/molbev/mst010 · DOI · Paper page
- Minh, 2020, IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era, Mol. Biol. Evol., 37, 1530, 10.1093/molbev/msaa015 · DOI · Paper page
- Bouckaert, 2019, BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis, PLoS Comput. Biol., 15, 10.1371/journal.pcbi.1006650 · DOI · Paper page
- Chen, 2018, Fastp: an ultra-fast all-in-one FASTQ preprocessor, Bioinformatics, 34, i884, 10.1093/bioinformatics/bty560 · DOI · Paper page
- Kim, 2019, Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype, Nat. Biotechnol., 37, 907, 10.1038/s41587-019-0201-4 · DOI · Paper page
- Liao, 2014, FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 · DOI · Paper page
- Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 · DOI · Paper page
- Langmead, 2009, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome, Genome Biol., 10, 10.1186/gb-2009-10-3-r25 · DOI · Paper page
- Fahlgren, 2007, High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes, PLoS One, 2, 10.1371/journal.pone.0000219 · DOI
- Huang, 2019, The genomes of pecan and Chinese hickory provide insights into Carya evolution and nut nutrition, GigaScience, 8, 10.1093/gigascience/giz036 · DOI
- Zhang, 2020, A high-quality walnut genome assembly reveals extensive gene expression divergences after whole-genome duplication, Plant Biotechnol. J., 18, 1848, 10.1111/pbi.13350 · DOI
- Wang, 2021, Hybrid speciation via inheritance of alternate alleles of parental isolating genes, Mol. Plant, 14, 208, 10.1016/j.molp.2020.11.008 · DOI
- Weir, 1984, Estimating F-statistics for the analysis of population structure, Evolution, 38, 1358
- Geng, 2025, Genome assembly and winged fruit gene regulation of Chinese Wingnut: insights from genomic and transcriptomic analyses, Genomics Proteomics Bioinformatics, 22, 10.1093/gpbjnl/qzae087 · DOI
- Heřmanová, 2011, Budvaricarpus serialis Knobloch & Mai, An unusual new member of the Normapolles complex from the Late Cretaceous of the Czech Republic, Int. J. Plant Sci., 172, 285, 10.1086/657278 · DOI
Metadata
- Authors
- Liu, H.-S., Wang, W.-H., Song, Y.-F., Yang, Y., Zhang, D.-Y., Bai, W.-N., & Zhang, B.-W.
- Affiliations
- Beijing Normal University (CN)
- Corresponding author
- Zhang, Da-Yong
- Bai, Wei-Ning
- Zhang, Bo-Wen
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2025-11
- Volume
- 35
- Issue
- 21
- Pages
- 5179-5191.e5
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W4415259312
- Cited by
- 5
- References
- 3
- Citations by year
- 2026: 3 · 2025: 2
- FWCI
- 2.72
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- Fundamental Research Funds for the Central Universities
- National Natural Science Foundation of China
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Reproductive Biology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Keywords
- heterodichogamy, Pterocarya stenoptera, pan-genome, structural variants, small RNA regulation, flower development, transposable elements, tandem repeats, convergent evolution, disassortative mating, Juglandaceae
- MeSH terms
- Genome, Plant, RNA, Plant, Flowers, Genomic Structural Variation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review