A telomere-to-telomere gap-free reference genome assembly of avocado provides useful resources for identifying genes related to fatty acid biosynthesis and disease resistance

Tianyu Yang , Yifan Cai , Tianping Huang , Danni Yang , Xingyu Yang , Xin Yin , Chengjun Zhang , Yunqiang Yang , Yongping Yang

Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) : 119

PDF (2788KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) :119 DOI: 10.1093/hr/uhae119
Article
research-article
A telomere-to-telomere gap-free reference genome assembly of avocado provides useful resources for identifying genes related to fatty acid biosynthesis and disease resistance
Author information +
History +
PDF (2788KB)

Abstract

Avocado (Persea americana Mill.) is an economically valuable plant because of the high fatty acid content and unique flavor of its fruits. Its fatty acid content, especially the relatively high unsaturated fatty acid content, provides significant health benefits. We herein present a telomere-to-telomere gapless genome assembly (841.6 Mb) of West Indian avocado. The genome contains 40 629 predicted protein-coding genes. Repeat sequences account for 57.9% of the genome. Notably, all telomeres, centromeres, and a nucleolar organizing region are included in this genome. Fragments from these three regions were observed via fluorescence in situ hybridization. We identified 376 potential disease resistance-related nucleotide-binding leucine-rich repeat genes. These genes, which are typically clustered on chromosomes, may be derived from gene duplication events. Five NLR genes (Pa11g0262, Pa02g4855, Pa07g3139, Pa07g0383, and Pa02g3196) were highly expressed in leaves, stems, and fruits, indicating they may be involved in avocado disease responses in multiple tissues. We also identified 128 genes associated with fatty acid biosynthesis and analyzed their expression patterns in leaves, stems, and fruits. Pa02g0113, which encodes one of 11 stearoyl-acyl carrier protein desaturases mediating C18 unsaturated fatty acid synthesis, was more highly expressed in the leaves than in the stems and fruits. These findings provide valuable insights that enhance our understanding of fatty acid biosynthesis in avocado.

Cite this article

Download citation ▾
Tianyu Yang, Yifan Cai, Tianping Huang, Danni Yang, Xingyu Yang, Xin Yin, Chengjun Zhang, Yunqiang Yang, Yongping Yang. A telomere-to-telomere gap-free reference genome assembly of avocado provides useful resources for identifying genes related to fatty acid biosynthesis and disease resistance. Horticulture Research, 2024, 11 (7) : 119 DOI:10.1093/hr/uhae119

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

We thank all the members of the laboratory for their technical and analysis assistance. We thank Liwen Bianji (Edanz) (www.liwenbianji.cn/ac) for editing the English text of a draft of this manuscript. This research was supported by Yunling Scholar Project (to Yongping Yang), the Major Science and Technology Projects (202202AE090016), Yunnan Revitalization Talents Support Plan (to Yunqiang Yang), the Digitalization, development and application of biotic resource (202002AA100007), the Postdoctoral Research Funding Projects of Yunnan Province (to Xin Yin), the National Natural Science Foundation of China (32100315, 31601999, 41771123, 31590820, and 31590823), the West Light Foundation of the Chinese Academy of Sciences (to Yunqiang Yang), and the 13th Five-year Informatization Plan of Chinese Academy of Sciences, Grant No. XXH13506. The funders had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Author contributions

YQY and YPY designed the research. TYY, YFC, XYY, DNY, and XY analyzed the data. TPH, CJZ, YWD, YQY, and YPY contributed reagents/materials/analysis tools. TYY, YFC, and YQY wrote and reviewed the paper.

Data availability statement

The raw sequencing data, including ONT Ultra-long reads, PacBio HiFi reads, NGS reads, Pore-C reads, and RNA-seq reads, assembly, and annotation data are accessible in Science Data Bank (https://doi.org/10.57760/sciencedb.07602).

Conflict of interests

The authors declare no conflict of interest.

Supplementary information

Supplementary data is available at Horticulture Research online.

References

[1]

Kilaru A, Cao X, Dabbs PB. et al. Oil biosynthesis in a basal angiosperm: transcriptome analysis of Persea Americana mesocarp. BMC Plant Biol. 2015; 15:203

[2]

Cowan AK, Wolstenholme BN. Avocados. In: Caballero B,ed. Encyclopedia of Food Sciences and Nutrition. 2nd ed. Oxford: Academic Press, 2003,348-53

[3]

Mahmassani HA, Avendano EE, Raman G. et al. Avocado consumption and risk factors for heart disease: a systematic review and meta-analysis. Am J Clin Nutr. 2018; 107:523-36

[4]

Food and Agriculture Organization of the United Nations. FAOSTAT Statistical Database. Rome, 2021

[5]

Kimaru KS, Muchemi KP, Mwangi JW. et al. Effects of anthracnose disease on avocado production in Kenya. Cogent Food Agric. 2020; 6:6

[6]

Ramírez-Gil JG, Gilchrist Ramelli E, Morales Osorio JG. Economic impact of the avocado (cv. Hass) wilt disease complex in Antioquia, Colombia, crops under different technological management levels. Crop Prot. 2017; 101:103-15

[7]

Gil GR, Osorio JM. First report of Cylindrocarpon destructans (Zinss) Scholten affecting avocado (Persea americana Mill) seedling in Colombia. Rev Protección Veg. 2013; 28:27-35

[8]

Dann EK, Cooke AW, Forsberg LI. et al. Pathogenicity studies in avocado with three nectriaceous fungi, Calonectria ilicicola, Gliocladiopsis sp. and Ilyonectria liriodendri. Plant Pathol. 2012; 61:896-902

[9]

Vitale A, Aiello D, Guarnaccia V. et al. First report of root rot caused by Ilyonectria (= Neonectria) macrodidyma on avocado (Persea americana) in Italy. J Phytopathol. 2011; 160:156-9

[10]

Zilberstein M, Elkind G, Zeidan M. et al. Wilting disease of young avocado trees caused by Neonectria radicicola in Israel. Proceedings VI World Avocado Congress. 2007:12-16

[11]

Besoain X, Piontelli E.Black root rot in avocado plants (Persea americana Mill.) by Cylindrocarpon destructans: Pathogenicity and epi-demiological aspects. Bol Micol. 1999; 14:41-7

[12]

Perez-Torres CA, Ibarra-Laclette E, Hernandez-Dominguez EE. et al. Molecular evidence of the avocado defense response to Fusarium kuroshium infection: a deep transcriptome analysis using RNA-Seq. PeerJ. 2021; 9:e11215

[13]

Li-Beisson Y, Shorrosh B, Beisson F. et al. Acyl-lipid metabolism. The Arabidopsis Book. 2010; 8:e0133

[14]

Harwood JL. Recent advances in the biosynthesis of plant fatty acids. Biochim Biophys Acta. 1996; 1301:7-56

[15]

Cerone M, Smith TK. Desaturases: structural and mechanistic insights into the biosynthesis of unsaturated fatty acids. IUBMB Life. 2022; 74:1036-51

[16]

Hou X, Wang D, Cheng Z. et al. A near-complete assembly of an Arabidopsis thaliana genome. Mol Plant. 2022; 15:1247-50

[17]

Naish M, Alonge M, Wlodzimierz P. et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science. 2021; 374:eabi7489

[18]

Song JM, Xie WZ, Wang S. et al. Two gap-free reference genomes and a global view of the centromere architecture in rice. Mol Plant. 2021; 14:1757-67

[19]

Li K, Jiang W, Hui Y. et al. Gapless indica rice genome reveals synergistic contributions of active transposable elements and segmental duplications to rice genome evolution. Mol Plant. 2021; 14:1745-56

[20]

Zhang L, Liang J, Chen H. et al. A near-complete genome assembly of Brassica rapa provides new insights into the evolution of centromeres. Plant Biotechnol J. 2023; 21:1022-32

[21]

Yue J, Chen Q, Wang Y. et al. Telomere-to-telomere and gap-free reference genome assembly of the kiwifruit Actinidia chinensis. Hortic Res. 2023; 10:uhac264

[22]

Han X, Zhang Y, Zhang Q. et al. Two haplotype-resolved, gap-free genome assemblies of Actinidia latifolia and Actinidia chinensis shed light on regulation mechanisms of vitamin C and sucrose metabolism in kiwifruit. Mol Plant. 2022; 16:452-70

[23]

Nie S, Zhao SW, Shi TL. et al. Gapless genome assembly of azalea and multi-omics investigation into divergence between two species with distinct flower color. Hortic Res. 2023; 10:uhac241

[24]

Li F, Xu S, Xiao Z. et al. Gap-free genome assembly and comparative analysis reveal the evolution and anthocyanin accumulation mechanism of Rhodomyrtus tomentosa. Hortic Res. 2023; 10:uhad005

[25]

Zhong CX, Marshall JB, Topp C. et al. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell. 2002; 14:2825-36

[26]

Comai L, Maheshwari S, Marimuthu MPA. Plant centromeres. Curr Opin Plant Biol. 2017; 36:158-67

[27]

Talbert PB, Henikoff S. The genetics and epigenetics of satellite centromeres. Genome Res. 2022; 32:608-15

[28]

Walkowiak S, Gao L, Monat C. et al. Multiple wheat genomes reveal global variation in modern breeding. Nature. 2020; 588:277-83

[29]

Copenhaver GP, Nickel K, Kuromori T. et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science. 1999; 286:2468-74

[30]

Cheng Z, Dong F, Langdon T. et al. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell. 2002; 14:1691-704

[31]

Ananiev EV, Phillips RL, Rines HW. Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA. 1998; 95:13073-8

[32]

Su H, Liu Y, Liu C. et al. Centromere satellite repeats have undergone rapid changes in Polyploid wheat subgenomes. Plant Cell. 2019; 31:2035-51

[33]

Rendon-Anaya M, Ibarra-Laclette E, Mendez-Bravo A. et al. The avocado genome informs deep angiosperm phylogeny, highlights introgressive hybridization, and reveals pathogen-influenced gene space adaptation. Proc Natl Acad Sci USA. 2019; 116:17081-9

[34]

Nath O, Fletcher SJ, Hayward A. et al. A haplotype resolved chromosomal level avocado genome allows analysis of novel avocado genes. Hortic Res. 2022; 9:uhac157

[35]

Rubinstein M, Eshed R, Rozen A. et al. Genetic diversity of avocado (Persea americana mill.) germplasm using pooled sequencing. BMC Genomics. 2019; 20:379

[36]

Talavera A, Soorni A, Bombarely A. et al. Genome-wide SNP discovery and genomic characterization in avocado (Persea americana mill.). Sci Rep. 2019; 9:20137

[37]

Castillo-Argaez R, Konkol JL, Vargas AI. et al. Disease severity and ecophysiology of rootstock/scion combinations of different avocado (Persea americana Mill.) genotypes in response to laurel wilt. Sci Hortic. 2021; 287:110250

[38]

Solares E, Morales-Cruz A, Balderas RF. et al. Insights into the domestication of avocado and potential genetic contributors to heterodichogamy. G3 (Bethesda). 2023; 13:jkac323

[39]

Cheng H, Jarvis ED, Fedrigo O. et al. Haplotype-resolved assembly of diploid genomes without parental data. Nat Biotechnol. 2022; 40:1332-5

[40]

Deshpande AS, Ulahannan N, Pendleton M. et al. Identifying synergistic high-order 3D chromatin conformations from genome-scale nanopore concatemer sequencing. Nat Biotechnol. 2022; 40:1488-99

[41]

Durand NC, Robinson JT, Shamim MS. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 2016; 3:99-101

[42]

Lin Y, Ye C, Li X. et al. quarTeT: a telomere-to-telomere toolkit for gap-free genome assembly and centromeric repeat identification. Hortic Res. 2023; 10:uhad127

[43]

Ou S, Su W, Liao Y. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 2019; 20:275

[44]

Bruna T, Lomsadze A, Borodovsky MA. A new gene finding tool GeneMark-ETP significantly improves the accuracy of automatic annotation of large eukaryotic genomes. bioRxiv. 2024

[45]

Blum M, Chang H-Y, Chuguransky S. et al. The InterPro protein families and domains database:20 years on. Nucleic Acids Res. 2021; 49:D344-54

[46]

Jones P, Binns D, Chang HY. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014; 30:1236-40

[47]

Huerta-Cepas J, Szklarczyk D, Heller D. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019; 47:D309-14

[48]

Cantalapiedra CP, Hernandez-Plaza A, Letunic I. et al. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol. 2021; 38:5825-9

[49]

Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013; 29:2933-5

[50]

Griffiths-Jones S, Moxon S, Marshall M. et al. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 2005; 33:D121-4

[51]

Chandrasekhara C, Mohannath G, Blevins T. et al. Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Genes Dev. 2016; 30:177-90

[52]

Rhie A, Walenz BP, Koren S. et al. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 2020; 21:245

[53]

Ou S, Chen J, Jiang N. Assessing genome assembly quality using the LTR assembly index (LAI). Nucleic Acids Res. 2018; 46:e126

[54]

Manni M, Berkeley MR, Seppey M. et al. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021; 38:4647-54

[55]

Rognes T, Flouri T, Nichols B. et al. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016; 4:e2584

[56]

Araújo RG, Rodriguez-Jasso RM, Ruiz HA. et al. Avocado by-products: nutritional and functional properties. Trends Food Sci Technol. 2018; 80:51-60

[57]

Navratilova P, Toegelova H, Tulpova Z. et al. Prospects of telomere-to-telomere assembly in barley: analysis of sequence gaps in the MorexV3 reference genome. Plant Biotechnol J. 2022; 20:1373-86

[58]

Wang T, Wang B, Hua X. et al. A complete gap-free diploid genome in Saccharum complex and the genomic footprints of evolution in the highly polyploid Saccharum genus. Nat Plants. 2023; 9:554-71

[59]

Huang Y, Ding W, Zhang M. et al. The formation and evolution of centromeric satellite repeats in Saccharum species. Plant J. 2021; 106:616-29

[60]

Kapos P, Devendrakumar KT, Li X. Plant NLRs: from discovery to application. Plant Sci. 2019; 279:3-18

[61]

Barragan AC, Weigel D. Plant NLR diversity: the known unknowns of pan-NLRomes. Plant Cell. 2021; 33:814-31

[62]

Okada A, Okada K, Miyamoto K. et al. OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice. J Biol Chem. 2009; 284:26510-8

[63]

Zhan C, Shen S, Yang C. et al. Plant metabolic gene clusters in the multi-omics era. Trends Plant Sci. 2022; 27:981-1001

[64]

Kim T-H, Kunz H-H, Bhattacharjee S. et al. Natural variation in small molecule-induced TIR-NB-LRR signaling induces root growth arrest via EDS1- and PAD4-complexed R protein VICTR inArabidopsis. Plant Cell. 2012; 24:5177-92

[65]

Moreno AO, Dorantes L, Galindez J. et al. Effect of different extraction methods on fatty acids, volatile compounds, and physical and chemical properties of avocado (Persea americana mill.) oil. J Agric Food Chem. 2003; 51:2216-21

[66]

Andre C, Haslam RP, Shanklin J. Feedback regulation of plastidic acetyl-CoA carboxylase by 18:1 -acyl carrier protein in Brassica napus. Proc Natl Acad Sci USA. 2012; 109:10107-12

[67]

Snapp AR, Lu C. Engineering industrial fatty acids in oilseeds. Front Biol. 2012; 8:323-32

[68]

Damude HG, Kinney AJ. Engineering oilseeds to produce nutritional fatty acids. Physiol Plant. 2007; 132:1-10

[69]

Kachroo A, Shanklin J, Whittle E. et al. The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol. 2006; 63:257-71

[70]

Chen S, Zhou Y, Chen Y. et al. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34:i884-90

[71]

Ranallo-Benavidez TR, Jaron KS, Schatz MC. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 2020; 11:1432

[72]

Rautiainen M, Nurk S, Walenz BP. et al. Telomere-to-telomere assembly of diploid chromosomes with Verkko. Nat Biotechnol. 2023; 41:1474-82

[73]

Hu J, Wang Z, Sun Z. et al. An efficient error correction and accurate assembly tool for noisy long reads. bioRxiv. 2023

[74]

Nurk S, Walenz BP, Rhie A. et al. HiCanu: accurate assembly of segmental duplications, satellites, and allelic variants from high-fidelity long reads. Genome Res. 2020; 30:1291-305

[75]

Guan D, Mccarthy SA, Wood J. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics. 2020; 36:2896-8

[76]

Dudchenko O, Batra SS, Omer AD. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017; 356:92-5

[77]

Hu J, Fan J, Sun Z. et al. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics. 2020; 36:2253-5

[78]

Li H. New strategies to improve minimap2 alignment accuracy. Bioinformatics. 2021; 37:4572-4

[79]

Danecek P, Bonfield JK, Liddle J. et al. Twelve years of SAMtools and BCFtools. GigaScience. 2021; 10:giab008

[80]

Hu J, Wang Z, Liang F. et al. NextPolish2: A repeat-aware polishing tool for genomes assembled using HiFi long reads. Genom Proteom Bioinform. 2024;qzad009

[81]

Zhang RG, Li GY, Wang XL. et al. TEsorter: an accurate and fast method to classify LTR-retrotransposons in plant genomes. Hortic Res. 2022; 9:uhac017

[82]

Novak P, Avila Robledillo L, Koblizkova A. et al. TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res. 2017; 45:e111

[83]

Bruna T, Hoff KJ, Lomsadze A. et al. BRAKER2:automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom Bioinform. 2021; 3:lqaa108

[84]

Gabriel L, Hoff KJ, Bruna T. et al. TSEBRA: transcript selector for BRAKER. BMC Bioinformatics. 2021; 22:566

[85]

Campbell MS, Holt C, Moore B. et al. Genome annotation and curation using MAKER and MAKER-P. Curr Protoc Bioinform. 2014; 48:4.11.11-14.11.39

[86]

Pertea G, Pertea M. GFF utilities: GffRead and GffCompare. F1000Res. 2020; 9:9

[87]

Gremme G, Steinbiss S, Kurtz S. GenomeTools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans Comput Biol Bioinform. 2013; 10:645-56

[88]

Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021; 18:366-8

[89]

Zheng Z, Li S, Su J. et al. Symphonizing pileup and full-alignment for deep learning-based long-read variant calling. Nat Comput Sci. 2022; 2:797-803

[90]

Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010; 38:e164-4

[91]

Komuro S, Endo R, Shikata K. et al. Genomic and chromosomal distribution patterns of various repeated DNA sequences in wheat revealed by a fluorescence in situ hybridization procedure. Genome. 2013; 56:131-7

[92]

Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012; 9:357-9

[93]

Kim D, Paggi JM, Park C. et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37:907-15

[94]

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26:841-2

[95]

Chen C, Chen H, Zhang Y. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13:1194-202

[96]

Ou S, Jiang N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 2018; 176:1410-22

[97]

Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999; 27:573-80

[98]

Ramirez F, Bhardwaj V, Arrigoni L. et al. High-resolution TADs reveal DNA sequences underlying genome organization in flies. Nat Commun. 2018; 9:189

[99]

Goel M, Sun H, Jiao W-B. et al. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 2019; 20:277

[100]

Goel M, Schneeberger K, Robinson P. Plotsr: visualizing structural similarities and rearrangements between multiple genomes. Bioinformatics. 2022; 38:2922-6

[101]

Steuernagel B, Witek K, Krattinger SG. et al. The NLR-annotator tool enables annotation of the intracellular immune receptor repertoire. Plant Physiol. 2020; 183:468-82

[102]

Van De Weyer AL, Monteiro F, Furzer OJ. et al. A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana. Cell. 2019; 178:1260-1272.e14

[103]

Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323

[104]

Dobin A, Davis CA, Schlesinger F. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013; 29:15-21

[105]

Rozewicki J, Li S, Amada KM. et al. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 2019; 47:W5-10

[106]

Vilella AJ, Severin J, Ureta-Vidal A. et al. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 2009; 19:327-35

PDF (2788KB)

119

Accesses

0

Citation

Detail

Sections
Recommended

/