A syntelog-based pan-genome provides insights into rice domestication and de-domestication

Asian rice is one of the world’s most widely cultivated crops. Large-scale resequencing analyses have been undertaken to explore the domestication and de-domestication genomic history of Asian rice, but the evolution of rice is still under debate. Here, we construct a syntelog-based rice pan-genome by integrating and merging 74 high-accuracy genomes based on long-read sequencing, encompassing all ecotypes and taxa of Oryza sativa and Oryza rufipogon. Analyses of syntelog groups illustrate subspecies divergence in gene presence-and-absence and haplotype composition and identify massive genomic regions putatively introgressed from ancient Geng/japonica to ancient Xian/indica or its wild ancestor, including almost all well-known domestication genes and a 4.5-Mb centromere-spanning block, supporting a single domestication event in rice. Genomic comparisons between weedy and cultivated rice highlight the contribution from wild introgression to the emergence of de-domestication syndromes in weedy rice. This work highlights the significance of inter-taxa introgression in shaping diversification and divergence in rice evolution and provides an exploratory attempt by utilizing the advantages of pan-genomes in evolutionary studies.

[1]  Jian Sun,et al.  Regain flood adaptation in rice through a 14-3-3 protein OsGF14h , 2022, Nature Communications.

[2]  Jue Ruan,et al.  A super pan-genomic landscape of rice , 2022, Cell Research.

[3]  K. Olsen,et al.  Genomic signatures of domestication and adaptation during geographical expansions of rice cultivation , 2021, Plant biotechnology journal.

[4]  M. Xiong,et al.  Glucan, Water‐Dikinase 1 (GWD1), an ideal biotechnological target for potential improving yield and quality in rice , 2021, Plant biotechnology journal.

[5]  R. Wing,et al.  Two Gap-free Reference Genomes and a Global View of the Centromere Architecture in Rice. , 2021, Molecular plant.

[6]  Hongyu Zhang,et al.  Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations , 2021, Cell.

[7]  L. Fan,et al.  De-Domestication: An Extension of Crop Evolution. , 2021, Trends in plant science.

[8]  Chun-Chao Wang,et al.  The landscape of gene-CDS-haplotype diversity in rice (Oryza sativa L.): properties, population organization, footprints of domestication and breeding, and implications in genetic improvement. , 2021, Molecular plant.

[9]  Jiaqiang Sun,et al.  Transcription Factors Rc and OsVP1 Coordinately Regulate Preharvest Sprouting Tolerance in Red Pericarp Rice. , 2020, Journal of agricultural and food chemistry.

[10]  A. Fernie,et al.  Selection of a subspecies-specific diterpene gene cluster implicated in rice disease resistance , 2020, Nature Plants.

[11]  Jian Sun,et al.  Diverse genetic mechanisms underlie worldwide convergent rice feralization , 2020, Genome Biology.

[12]  Runan Yao,et al.  ShinyGO: a graphical gene-set enrichment tool for animals and plants , 2019, Bioinform..

[13]  Hongkun Zheng,et al.  Population Genomic Analysis and De Novo Assembly Reveal the Origin of Weedy Rice as an Evolutionary Game. , 2019, Molecular plant.

[14]  Andrew J. Blumberg,et al.  Genomic architecture and introgression shape a butterfly radiation , 2018, Science.

[15]  Chang-Hui Shen.  The Genome , 2019, Diagnostic Molecular Biology.

[16]  T. A. Brown,et al.  Misconceptions Regarding the Role of Introgression in the Origin of Oryza sativa subsp. indica , 2018, Front. Plant Sci..

[17]  S. Jackson,et al.  Parallel selection on a dormancy gene during domestication of crops from multiple families , 2018, Nature Genetics.

[18]  Xuehui Huang,et al.  Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice , 2018, Nature Genetics.

[19]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[20]  Most Humaira Sultana,et al.  Genomic variation associated with local adaptation of weedy rice during de-domestication , 2017, Nature Communications.

[21]  P. Civáň,et al.  Origin of rice (Oryza sativa L.) domestication genes , 2017, Genetic Resources and Crop Evolution.

[22]  Yan Li,et al.  Sequencing and de novo assembly of a near complete indica rice genome , 2017, Nature Communications.

[23]  Haiyang Wang,et al.  GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice , 2017, Nature Plants.

[24]  Langtao Xiao,et al.  LABA1, a Domestication Gene Associated with Long, Barbed Awns in Wild Rice[OPEN] , 2015, Plant Cell.

[25]  H. Ishida,et al.  Establishment of Monitoring Methods for Autophagy in Rice Reveals Autophagic Recycling of Chloroplasts and Root Plastids during Energy Limitation1[OPEN] , 2015, Plant Physiology.

[26]  B. Gross,et al.  Archaeological and genetic insights into the origins of domesticated rice , 2014, Proceedings of the National Academy of Sciences.

[27]  Xuehui Huang,et al.  An-1 Encodes a Basic Helix-Loop-Helix Protein That Regulates Awn Development, Grain Size, and Grain Number in Rice[C][W][OPEN] , 2013, Plant Cell.

[28]  A. Fujiyama,et al.  A map of rice genome variation reveals the origin of cultivated rice , 2012, Nature.

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

[30]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[31]  Mukesh Jain,et al.  NGS QC Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data , 2012, PloS one.

[32]  Q. Qian,et al.  Genetic Control of a Transition from Black to Straw-White Seed Hull in Rice Domestication1[C][W][OA] , 2011, Plant Physiology.

[33]  Qian Qian,et al.  Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice , 2010, Nature Genetics.

[34]  Philip L. F. Johnson,et al.  A Draft Sequence of the Neandertal Genome , 2010, Science.

[35]  Yaoguang Liu,et al.  Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes , 2008, Proceedings of the National Academy of Sciences.

[36]  T. Sang,et al.  Rice Domestication by Reducing Shattering , 2007 .

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

[38]  V. Solovyev,et al.  Ab initio gene finding in Drosophila genomic DNA. , 2000, Genome research.

[39]  J. Howe.  About Platinum , 1890, The Dental register.

[40]  Shujun Ou,et al.  LTR_retriever: a highly accurate and sensitive program for identification of LTR retrotransposons , 2017, bioRxiv.