Autopolyploid inheritance and a heterozygous reciprocal translocation shape chromosome genetic behavior in tetraploid blueberry (Vaccinium corymbosum)

Summary Understanding chromosome recombination behavior in polyploidy species is key to advancing genetic discoveries. In blueberry, a tetraploid species, the line of evidences about its genetic behavior still remain poorly understood, owing to the inter‐specific, and inter‐ploidy admixture of its genome and lack of in depth genome‐wide inheritance and comparative structural studies. Here we describe a new high‐quality, phased, chromosome‐scale genome of a diploid blueberry, clone W85. The genome was integrated with cytogenetics and high‐density, genetic maps representing six tetraploid blueberry cultivars, harboring different levels of wild genome admixture, to uncover recombination behavior and structural genome divergence across tetraploid and wild diploid species. Analysis of chromosome inheritance and pairing demonstrated that tetraploid blueberry behaves as an autotetraploid with tetrasomic inheritance. Comparative analysis demonstrated the presence of a reciprocal, heterozygous, translocation spanning one homolog of chr‐6 and one of chr‐10 in the cultivar Draper. The translocation affects pairing and recombination of chromosomes 6 and 10. Besides the translocation detected in Draper, no other structural genomic divergences were detected across tetraploid cultivars and highly inter‐crossable wild diploid species. These findings and resources will facilitate new genetic and comparative genomic studies in Vaccinium and the development of genomic assisted selection strategy for this crop.

[1]  Amanda M. Hulse-Kemp,et al.  High-quality reference genome and annotation aids understanding of berry development for evergreen blueberry (Vaccinium darrowii) , 2021, Horticulture research.

[2]  E. Hilario,et al.  A chromosome‐scale assembly of the bilberry genome identifies a complex locus controlling berry anthocyanin composition , 2021, Molecular ecology resources.

[3]  Felipe A. Simão,et al.  BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes , 2021, Molecular biology and evolution.

[4]  Jessica L. Gilbert,et al.  High-Density Linkage Map Construction and QTL Identification in a Diploid Blueberry Mapping Population , 2021, Frontiers in Plant Science.

[5]  Zev N. Kronenberg,et al.  Extended haplotype-phasing of long-read de novo genome assemblies using Hi-C , 2021, Nature Communications.

[6]  A. Lemainque,et al.  Chromosome reciprocal translocations have accompanied subspecies evolution in bananas , 2020, The Plant journal : for cell and molecular biology.

[7]  N. Bassil,et al.  Development of a genetic framework to improve the efficiency of bioactive delivery from blueberry , 2020, Scientific Reports.

[8]  C. Bachem,et al.  Haplotype-resolved genome analyses of a heterozygous diploid potato , 2020, Nature Genetics.

[9]  E. Sanchez-Moran,et al.  Varietal variation and chromosome behaviour during meiosis in Solanum tuberosum , 2020, Heredity.

[10]  Weidong Bao,et al.  Bioinformatic and Molecular Analysis of Satellite Repeat Diversity in Vaccinium Genomes , 2020, Genes.

[11]  N. Bassil,et al.  Diversity in Metabolites and Fruit Quality Traits in Blueberry Enables Ploidy and Species Differentiation and Establishes a Strategy for Future Genetic Studies , 2020, Frontiers in Plant Science.

[12]  I. Leitch,et al.  The Plant DNA C-values database (release 7.1): an updated online repository of plant genome size data for comparative studies. , 2019, The New phytologist.

[13]  G. Copenhaver,et al.  Meiotic DNA Repair in the Nucleolus Employs a Nonhomologous End-Joining Mechanism[OPEN] , 2019, Plant Cell.

[14]  Xueyan Zhang,et al.  Extensive intraspecific gene order and gene structural variations in upland cotton cultivars , 2019, Nature Communications.

[15]  Thomas Peterson,et al.  Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline , 2019, Genome Biology.

[16]  Jennifer H. Wisecaver,et al.  Haplotype-phased genome and evolution of phytonutrient pathways of tetraploid blueberry , 2019, GigaScience.

[17]  Shujun Ou,et al.  Assessing genome assembly quality using the LTR Assembly Index (LAI) , 2018, Nucleic acids research.

[18]  Matthew Stephens,et al.  Genotyping Polyploids from Messy Sequencing Data , 2018, Genetics.

[19]  N. Mitsukawa,et al.  Phenotypic diversification by enhanced genome restructuring after induction of multiple DNA double-strand breaks , 2018, Nature Communications.

[20]  Richard G. F. Visser,et al.  polymapR—linkage analysis and genetic map construction from F1 populations of outcrossing polyploids , 2018, Bioinform..

[21]  J. Schmutz,et al.  Amplification and adaptation of centromeric repeats in polyploid switchgrass species. , 2018, The New phytologist.

[22]  Adam M. Phillippy,et al.  MUMmer4: A fast and versatile genome alignment system , 2018, PLoS Comput. Biol..

[23]  Andreu Paytuví Gallart,et al.  PRGdb 3.0: a comprehensive platform for prediction and analysis of plant disease resistance genes , 2017, Nucleic Acids Res..

[24]  Evan Bolton,et al.  Database resources of the National Center for Biotechnology Information , 2017, Nucleic Acids Res..

[25]  Shujun Ou,et al.  LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons1[OPEN] , 2017, Plant Physiology.

[26]  Zhou Du,et al.  agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update , 2017, Nucleic Acids Res..

[27]  J. Macas,et al.  TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads , 2017, Nucleic acids research.

[28]  Chris Maliepaard,et al.  Partial preferential chromosome pairing is genotype dependent in tetraploid rose , 2017, The Plant journal : for cell and molecular biology.

[29]  Jeffrey T Leek,et al.  Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown , 2016, Nature Protocols.

[30]  C. Hackett,et al.  A rapid marker ordering approach for high-density genetic linkage maps in experimental autotetraploid populations using multidimensional scaling , 2016, Theoretical and Applied Genetics.

[31]  M. Schatz,et al.  Phased diploid genome assembly with single-molecule real-time sequencing , 2016, Nature Methods.

[32]  C. Hackett,et al.  Probabilistic Multilocus Haplotype Reconstruction in Outcrossing Tetraploids , 2016, Genetics.

[33]  Brendan L. O’Connell,et al.  Chromosome-scale shotgun assembly using an in vitro method for long-range linkage , 2015, Genome research.

[34]  R. Visser,et al.  The Double-Reduction Landscape in Tetraploid Potato as Revealed by a High-Density Linkage Map , 2015, Genetics.

[35]  Christina A. Cuomo,et al.  Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement , 2014, PloS one.

[36]  Robert J. Elshire,et al.  TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline , 2014, PloS one.

[37]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[38]  Thomas R. Gingeras,et al.  STAR: ultrafast universal RNA-seq aligner , 2013, Bioinform..

[39]  Gabor T. Marth,et al.  Haplotype-based variant detection from short-read sequencing , 2012, 1207.3907.

[40]  Pablo Cingolani,et al.  © 2012 Landes Bioscience. Do not distribute. , 2022 .

[41]  Jeremy D. DeBarry,et al.  MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity , 2012, Nucleic acids research.

[42]  J. Olmstead,et al.  The Use of Inter-Sectional Hybrids in Blueberry Breeding , 2012 .

[43]  I. Romagosa,et al.  Genetic characterization of a reciprocal translocation present in a widely grown barley variety , 2012, Molecular Breeding.

[44]  Gonçalo R. Abecasis,et al.  The variant call format and VCFtools , 2011, Bioinform..

[45]  P. Krysan,et al.  Chromosomal translocations are a common phenomenon in Arabidopsis thaliana T-DNA insertion lines. , 2010, The Plant journal : for cell and molecular biology.

[46]  A. Reymond,et al.  The effect of translocation-induced nuclear reorganization on gene expression. , 2010, Genome research.

[47]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[48]  Sean R. Eddy,et al.  Infernal 1.0: inference of RNA alignments , 2009, Bioinform..

[49]  Jiming Jiang,et al.  Chromatin Structure and Physical Mapping of Chromosome 6 of Potato and Comparative Analyses With Tomato , 2008, Genetics.

[50]  N. Bassil,et al.  Impact of Wide Hybridization on Highbush Blueberry Breeding , 2008 .

[51]  M. Robles,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .

[52]  Sofia M. C. Robb,et al.  MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. , 2007, Genome research.

[53]  Robert S. Harris Improved Pairwise Alignmnet of Genomic DNA , 2007 .

[54]  Laurent Gueguen,et al.  MareyMap: an R-based tool with graphical interface for estimating recombination rates , 2007, Bioinform..

[55]  Burkhard Morgenstern,et al.  AUGUSTUS: ab initio prediction of alternative transcripts , 2006, Nucleic Acids Res..

[56]  Zhongfu Ni,et al.  Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[57]  K. Livingstone,et al.  An algorithm for analyzing linkages affected by heterozygous translocations: QuadMap. , 2006, The Journal of heredity.

[58]  Thomas D. Wu,et al.  GMAP: a genomic mapping and alignment program for mRNA and EST sequence , 2005, Bioinform..

[59]  R. Arora,et al.  Inheritance of Cold Hardiness and Dehydrin Genes in Diploid Mapping Populations of Blueberry , 2004 .

[60]  Ian Korf,et al.  Gene finding in novel genomes , 2004, BMC Bioinformatics.

[61]  N. Vorsa,et al.  Polyploidy and sexual polyploidization in the genus Vaccinium , 2003, Euphytica.

[62]  J. Hancock,et al.  Nature of 2n gamete formation and mode of inheritance in interspecific hybrids of diploid Vaccinium darrowi and tetraploid V. corymbosum , 1995, Theoretical and Applied Genetics.

[63]  D. Costich,et al.  Determination of ploidy level and nuclear DNA content in blueberry by flow cytometry , 1993, Theoretical and Applied Genetics.

[64]  J. Hancock,et al.  Early-acting inbreeding depression and reproductive success in the highbush blueberry, Vaccinium corymbosum L. , 1990, Theoretical and Applied Genetics.

[65]  Mario Stanke,et al.  Gene prediction with a hidden Markov model and a new intron submodel , 2003, ECCB.

[66]  J. Hancock,et al.  Detecting and mapping repulsion-phase linkage in polyploids with polysomic inheritance , 2001, Theoretical and Applied Genetics.

[67]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[68]  N. Vorsa,et al.  Genetic Differentiation of Diploid Blueberry, Vaccinium sect. Cyanococcus (Ericaceae) , 1994 .

[69]  N. Vorsa Quantitative analysis of meiotic chromosome pairing in triploid blueberry: evidence for preferential pairing , 1990 .

[70]  H. B. M. Jonkers,et al.  Inheritance in COLD , 1989, Algebraic Methods.

[71]  G. Jelenkovic,et al.  Chromosome associations in the first meiotic division in three tetraploid clones of Vaccinium corymbosum L. , 1970 .

[72]  LTR_retriever: a highly accurate and sensitive program for of , 2022 .