The chromosome-scale reference genome and transcriptome analysis of Solanum torvum provides insights into resistance to root-knot nematodes

Solanum torvum (Swartz) (2n = 24) is a wild Solanaceae plant with high economic value that is used as a rootstock in grafting for Solanaceae plants to improve the resistance to a soil-borne disease caused by root-knot nematodes (RKNs). However, the lack of a high-quality reference genome of S. torvum hinders research on the genetic basis for disease resistance and application in horticulture. Herein, we present a chromosome-level assembly of genomic sequences for S. torvum combining PacBio long reads (HiFi reads), Illumina short reads and Hi-C scaffolding technology. The assembled genome size is ~1.25 Gb with a contig N50 and scaffold N50 of 38.65 Mb and 103.02 Mb, respectively as well as a BUSCO estimate of 98%. GO enrichment and KEGG pathway analysis of the unique S. torvum genes, including NLR and ABC transporters, revealed that they were involved in disease resistance processes. RNA-seq data also confirmed that 48 NLR genes were highly expressed in roots and fibrous roots and that three homologous NLR genes (Sto0288260.1, Sto0201960.1 and Sto0265490.1) in S. torvum were significantly upregulated after RKN infection. Two ABC transporters, ABCB9 and ABCB11 were identified as the hub genes in response to RKN infection. The chromosome-scale reference genome of the S. torvum will provide insights into RKN resistance.

[1]  Cuiping Zhang,et al.  Integration of multi-omics technologies for crop improvement: Status and prospects , 2022, Frontiers in Bioinformatics.

[2]  Jian-Min Zhou,et al.  Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae. , 2022, Journal of genetics and genomics = Yi chuan xue bao.

[3]  Jing Zhao,et al.  Genomic selection and genetic architecture of agronomic traits during modern rapeseed breeding , 2022, Nature Genetics.

[4]  C. Gleason,et al.  Rooting Out the Mechanisms of Root-Knot Nematode-Plant Interactions. , 2022, Annual review of phytopathology.

[5]  Zhibin Zhang,et al.  Genome sequence and transcriptome of Sorbus pohuashanensis provides insights into population evolution and leaf sunburn response. , 2022, Journal of genetics and genomics = Yi chuan xue bao.

[6]  H. Ohta,et al.  Transcriptomic Analysis of Resistant and Susceptible Responses in a New Model Root-Knot Nematode Infection System Using Solanum torvum and Meloidogyne arenaria , 2021, bioRxiv.

[7]  M. Zhang,et al.  Transcriptome Analysis of Eggplant Root in Response to Root-Knot Nematode Infection , 2021, Pathogens.

[8]  M. Le Paslier,et al.  Building a cluster of NLR genes conferring resistance to pests and pathogens: the story of the Vat gene cluster in cucurbits , 2021, Horticulture research.

[9]  Dandan Li,et al.  A high‐quality genome assembly of the eggplant provides insights into the molecular basis of disease resistance and chlorogenic acid synthesis , 2021, Molecular ecology resources.

[10]  T. Hu,et al.  A high-quality chromosome-level genome assembly reveals genetics for important traits in eggplant , 2020, Horticulture Research.

[11]  T. Hu,et al.  A high-quality chromosome-level genome assembly reveals genetics for important traits in eggplant , 2020, Horticulture Research.

[12]  Hongsheng Zhang,et al.  The ATP-binding cassette transporter OsPDR1 regulates plant growth and pathogen resistance by affecting jasmonates biosynthesis in rice. , 2020, Plant science : an international journal of experimental plant biology.

[13]  Y. Xuan,et al.  Transcriptome Analysis of Rice Roots in Response to Root-Knot Nematode Infection , 2020, International journal of molecular sciences.

[14]  Johnathan J. Dalzell,et al.  ABC transporter genes ABC-C6 and ABC-G33 alter plant-microbe-parasite interactions in the rhizosphere , 2019, Scientific Reports.

[15]  P. Qi,et al.  Fusarium graminearum ATP-Binding Cassette Transporter Gene FgABCC9 Is Required for Its Transportation of Salicylic Acid, Fungicide Resistance, Mycelial Growth and Pathogenicity towards Wheat , 2018, International journal of molecular sciences.

[16]  Hong Ma,et al.  Widespread Whole Genome Duplications Contribute to Genome Complexity and Species Diversity in Angiosperms. , 2018, Molecular plant.

[17]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[18]  Yan Yang,et al.  Molecular Cloning and Characterization of a Wild Eggplant Solanum aculeatissimum NBS-LRR Gene, Involved in Plant Resistance to Meloidogyne incognita , 2018, International journal of molecular sciences.

[19]  B. Xie,et al.  Transcriptome profiling of Cucumis metuliferus infected by Meloidogyne incognita provides new insights into putative defense regulatory network in Cucurbitaceae , 2017, Scientific Reports.

[20]  Ge Gao,et al.  CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features , 2017, Nucleic Acids Res..

[21]  S. Koren,et al.  Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation , 2016, bioRxiv.

[22]  Neva C. Durand,et al.  Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. , 2016, Cell systems.

[23]  Daisy E. Pagete.  An end-to-end assembly of the Aedes aegypti genome , 2016, 1605.04619.

[24]  Heng Li,et al.  Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences , 2015, Bioinform..

[25]  Philip A. Ewels,et al.  HiCUP: pipeline for mapping and processing Hi-C data , 2015, F1000Research.

[26]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[27]  H. Abé,et al.  Sclareol induces plant resistance to root-knot nematode partially through ethylene-dependent enhancement of lignin accumulation. , 2015, Molecular plant-microbe interactions : MPMI.

[28]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[29]  S. Salzberg,et al.  StringTie enables improved reconstruction of a transcriptome from RNA-seq reads , 2015, Nature Biotechnology.

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

[31]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[32]  Hideki Hirakawa,et al.  Draft Genome Sequence of Eggplant (Solanum melongena L.): the Representative Solanum Species Indigenous to the Old World , 2014, DNA research : an international journal for rapid publication of reports on genes and genomes.

[33]  Florent Murat,et al.  Paleo-evolutionary plasticity of plant disease resistance genes , 2014, BMC Genomics.

[34]  Yeisoo Yu,et al.  Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species , 2014, Nature Genetics.

[35]  P. Bagnaresi,et al.  Solanum torvum responses to the root-knot nematode Meloidogyne incognita , 2013, BMC Genomics.

[36]  Mira V. Han,et al.  Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. , 2013, Molecular biology and evolution.

[37]  M. Plazas,et al.  Breeding for chlorogenic acid content in eggplant: interest and prospects. , 2013 .

[38]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[39]  G. Gheysen,et al.  Transcriptional reprogramming by root knot and migratory nematode infection in rice. , 2012, The New phytologist.

[40]  Chi Song,et al.  Whole genome duplication of intra- and inter-chromosomes in the tomato genome. , 2012, Journal of genetics and genomics = Yi chuan xue bao.

[41]  Daniel W. A. Buchan,et al.  The tomato genome sequence provides insights into fleshy fruit evolution , 2012, Nature.

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

[43]  David M. A. Martin,et al.  Genome sequence and analysis of the tuber crop potato , 2011, Nature.

[44]  P. Abad,et al.  The Ma Gene for Complete-Spectrum Resistance to Meloidogyne Species in Prunus Is a TNL with a Huge Repeated C-Terminal Post-LRR Region1[C][W] , 2011, Plant Physiology.

[45]  Robert D. Finn,et al.  Rfam: Wikipedia, clans and the “decimal” release , 2010, Nucleic Acids Res..

[46]  Jun Yu,et al.  KaKs_Calculator 2.0: A Toolkit Incorporating Gamma-Series Methods and Sliding Window Strategies , 2010, Genom. Proteom. Bioinform..

[47]  Nansheng Chen,et al.  Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences , 2009, Current protocols in bioinformatics.

[48]  S. Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

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

[50]  Zhao Xu,et al.  LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons , 2007, Nucleic Acids Res..

[51]  V. Williamson,et al.  Nematode resistance in plants: the battle underground. , 2006, Trends in genetics : TIG.

[52]  Patrice Koehl,et al.  Plant NBS-LRR proteins: adaptable guards , 2006, Genome Biology.

[53]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[54]  P. Besse,et al.  Solanum torvum, as a useful source of resistance against bacterial and fungal diseases for improvement of eggplant (S. melongena L.) , 2005 .

[55]  Steven Salzberg,et al.  TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders , 2004, Bioinform..

[56]  M. Caboche,et al.  High-resolution mapping and chromosome landing at the root-knot nematode resistance locus Ma from Myrobalan plum using a large-insert BAC DNA library , 2004, Theoretical and Applied Genetics.

[57]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[58]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[59]  Cédric Feschotte,et al.  Plant transposable elements: where genetics meets genomics , 2002, Nature Reviews Genetics.

[60]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[61]  P. Abad,et al.  High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me3 and Me4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.) , 2001, Theoretical and Applied Genetics.

[62]  P. Vos,et al.  The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids , 1998, Nature Biotechnology.

[63]  J. Bodeau,et al.  The Root Knot Nematode Resistance Gene Mi from Tomato Is a Member of the Leucine Zipper, Nucleotide Binding, Leucine-Rich Repeat Family of Plant Genes , 1998, Plant Cell.

[64]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[65]  W. Stiekema,et al.  Positional Cloning of a Gene for Nematode Resistance in Sugar Beet , 1997, Science.

[66]  M. Stanke,et al.  Multi-Genome Annotation with AUGUSTUS. , 2019, Methods in molecular biology.

[67]  Philip A. Ewels,et al.  HiCUP: pipeline for mapping and processing Hi-C data , 2015, F1000Research.

[68]  P. Sánchez-Torres,et al.  Resistance of pepper germplasm to Meloidogyne incognita , 2013 .

[69]  K. Govindaraju,et al.  Antimicrobial activity of silver nanoparticles Biogenic silver nanoparticles by Solanum torvum and their promising antimicrobial activity , 2010 .

[70]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.