The Gillenia trifoliata genome reveals dynamics correlated with growth and reproduction in Rosaceae

Hilary S. Ireland , Chen Wu , Cecilia H. Deng , Elena Hilario , Ali Saei , Sylvia Erasmuson , Ross N. Crowhurst , Karine M. David , Robert J. Schaffer , David Chagné

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 233

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :233 DOI: 10.1038/s41438-021-00662-4
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The Gillenia trifoliata genome reveals dynamics correlated with growth and reproduction in Rosaceae
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Abstract

The Rosaceae family has striking phenotypic diversity and high syntenic conservation. Gillenia trifoliata is sister species to the Maleae tribe of apple and ~1000 other species. Gillenia has many putative ancestral features, such as herb/sub-shrub habit, dry fruit-bearing and nine base chromosomes. This coalescence of ancestral characters in a phylogenetically important species, positions Gillenia as a ‘rosetta stone’ for translational science within Rosaceae. We present genomic and phenological resources to facilitate the use of Gillenia for this purpose. The Gillenia genome is the first fully annotated chromosome-level assembly with an ancestral genome complement (x = 9), and with it we developed an improved model of the Rosaceae ancestral genome. MADS and NAC gene family analyses revealed genome dynamics correlated with growth and reproduction and we demonstrate how Gillenia can be a negative control for studying fleshy fruit development in Rosaceae.

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Hilary S. Ireland, Chen Wu, Cecilia H. Deng, Elena Hilario, Ali Saei, Sylvia Erasmuson, Ross N. Crowhurst, Karine M. David, Robert J. Schaffer, David Chagné. The Gillenia trifoliata genome reveals dynamics correlated with growth and reproduction in Rosaceae. Horticulture Research, 2021, 8 (1) : 233 DOI:10.1038/s41438-021-00662-4

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References

[1]

Liu, Z., Ma, H., Jung, S., Main, D. & Guo, L. Developmental mechanisms of fleshy fruit diversity in Rosaceae. Annu. Rev. Plant Biol. 71, 547-573 (2020).

[2]

Potter, D. et al. Phylogeny and classification of Rosaceae. Plant Syst. Evol. 266, 5-43 (2007).

[3]

Alioto, T. et al. Transposons played a major role in the diversification between the closely related almond and peach genomes: results from the almond genome sequence. Plant J. 101, 455-472 (2020).

[4]

Buti, M. et al. The genome sequence and transcriptome of Potentilla micrantha and their comparison to Fragaria vesca (the woodland strawberry) . Gigascience 7, 1-14 (2018).

[5]

Velasco, R. et al. The genome of the domesticated apple (Malus x domestica Borkh.) . Nat. Genet. 42, 833-839 (2010).

[6]

Campbell, C. S., Evans, R. C., Morgan, D. R., Dickinson, T. A. & Arsenault, M. P. Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): limited resolution of a complex evolutionary history. Plant Syst. Evol. 266, 119-145 (2007).

[7]

Evans, R. C. & Campbell, C. S. The origin of the apple subfamily (Maloideae; Rosaceae) is clarified by DNA sequence data from duplicated GBSSI genes. Am. J. Bot. 89, 1478-1484 (2002).

[8]

Vilanova, S., Sargent, D. J., Arús, P. & Monfort, A. Synteny conservation between two distantly-related Rosaceae genomes: Prunus (the stone fruits) and Fragaria (the strawberry) . Bmc Plant Biol. 8, 8 (2008).

[9]

Illa, E. et al. Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. Bmc Evolut. Biol. 11, 11 (2011).

[10]

Jung, S. et al. Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies . Bmc Genomics 13, 13 (2012).

[11]

Zhang, Q. et al. The genome of Prunus mume . Nat. Commun. 3, 1318 (2012).

[12]

Griesmann, M. et al. Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science 361, 6398 (2018).

[13]

Meier, U. et al. The BBCH system to coding the phenological growth stages of plants - history and publications. J. f.ür. Kulturpflanzen 61, 41-52 (2009).

[14]

Meier, U. E. Growth stages of mono- and dicotyledonous plants: BBCH monograph. (Federal Biological Research Centre for Agriculture and Forestry, 2001).

[15]

Boyes, D. C. et al. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13, 1499-1510 (2001).

[16]

Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210-3212 (2015).

[17]

Verde, I. et al. The Peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics 18, 225 (2017).

[18]

Zhang, L. et al. A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat. Commun. 10, 1494 (2019).

[19]

Linsmith, G. et al. Pseudo-chromosome-length genome assembly of a double haploid “Bartlett” pear (Pyrus communis L.) . Gigascience 8, 12 (2019).

[20]

VanBuren, R. et al. A near complete, chromosome-scale assembly of the black raspberry (Rubus occidentalis) genome . Gigascience 7, 8 (2018).

[21]

Barker, M.S., Baute, G. J. & Liu, S-.L. in Plant Genome Diversity (ed. Wendel, J. F.) (Springer-Verlag, Vienna, 2012).

[22]

Daccord, N. et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat. Genet. 49, 1099-1106 (2017).

[23]

Parenicová, L. et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15, 1538-1551 (2003).

[24]

Alvarez-Buylla, E. R. et al. MADS-box genes underground becoming mainstream: plant root developmental mechanisms. N. Phytol. 223, 1143-1158 (2019).

[25]

Guitton, B. et al. Genetic control of biennial bearing in apple. J. Exp. Bot. 63, 131-149 (2012).

[26]

Wu, R. et al. SVP-like MADS box genes control dormancy and budbreak in apple. Front. Plant Sci. 8, 477 (2017).

[27]

Kumar, G. et al. Comparative phylogenetic analysis and transcriptional profiling of MADS-box gene family identified DAM and FLC-like genes in apple (Malusx domestica) . Sci. Rep. 6, 20695 (2016).

[28]

Chen, D., Yan, W., Fu, L. Y. & Kaufmann, K. Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana . Nat. Commun. 9, 4534 (2018).

[29]

Li, Y. et al. Transcriptomic analysis reveals the regulatory module of apple (Malus x domestica) floral transition in response to 6-BA . BMC Plant Biol. 19, 93 (2019).

[30]

Li, R. et al. Genomewide analysis of homeobox gene family in apple (Malus domestica Borkh.) and their response to abiotic stress . J. Genet. 98, 98 (2019).

[31]

Chen, X. et al. Sequencing of a wild apple (Malus baccata) genome unravels the differences between cultivated and wild apple species regarding disease resistance and cold tolerance . G3 (Bethesda) 9, 2051-2060 (2019).

[32]

Dong, X. et al. De novo assembly of a wild pear (Pyrus betuleafolia) genome . Plant Biotechnol. J. 18, 581-595 (2020).

[33]

Kamiuchi, Y., Yamamoto, K., Furutani, M., Tasaka, M. & Aida, M. The CUC1 and CUC2 genes promote carpel margin meristem formation during Arabidopsis gynoecium development. Front. Plant Sci. 5, 165 (2014).

[34]

Moyano, E. et al. Genome-wide analysis of the NAC transcription factor family and their expression during the development and ripening of the Fragaria x ananassa fruits . PLoS ONE 13, e0196953 (2018).

[35]

Busatto, N., Tadiello, A., Trainotti, L. & Costa, F. Climacteric ripening of apple fruit is regulated by transcriptional circuits stimulated by cross-talks between ethylene and auxin. Plant Signal Behav. 12, e1268312 (2017).

[36]

Chagné, D. et al. The draft genome sequence of European pear (Pyrus communis L. ‘Bartlett’) . PLoS ONE 9, e92644 (2014).

[37]

Pilkington, S. M. et al. A manually annotated Actinidia chinensis var. chinensis (kiwifruit) genome highlights the challenges associated with draft genomes and gene prediction in plants . BMC Genomics 19, 257 (2018).

[38]

Theissen, G. & Saedler, H. Plant biology. Floral quartets. Plant Biol. Flor. Quartets Nat. 409, 469-471 (2001).

[39]

Ireland, H. S. et al. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J. 73, 1044-1056 (2013).

[40]

Seymour, G. B. et al. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria x ananassa Duch.) fruit, a non-climacteric tissue . J. Exp. Bot. 62, 1179-1188 (2011).

[41]

Rumpler, F., Theissen, G. & Melzer, R. A conserved leucine zipper-like motif accounts for strong tetramerization capabilities of SEPALLATA-like MADS-domain transcription factors. J. Exp. Bot. 69, 1943-1954 (2018).

[42]

Xiang, Y. et al. Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Mol. Biol. Evol. 34, 262-281 (2017).

[43]

Naim, F. et al. Advanced engineering of lipid metabolism in Nicotiana benthamiana using a draft genome and the V2 viral silencing-suppressor protein. PLoS ONE 7, e52717 (2012).

[44]

Hilario, E. Plant nuclear genomic DNA preps. protocols.io (2018).

[45]

Hilario, E. Plant nuclei enrichment for chromatin capture-based Hi-C library protocols. Protocols.io (2019).

[46]

McCartney, A. et al. An exploration of assembly strategies and quality metrics on the accuracy of the Knightia excelsa (rewarewa) genome. bioRxiv 2020.10.28.358903 (2020).

[47]

Zhong, S. et al. High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb. Protoc. 2011, 940-949 (2011).

[48]

Chagné, D. et al. Polyploid and aneuploid detection in apple using a single nucleotide polymorphism array. Tree Genet. Genomes 11, 5 (2015).

[49]

Andrews, S, FastQC: a quality control tool for high throughput sequence data www.bioinformatics.babraham.ac.uk/projects/fastqc. (Babraham Bioinformatics, Babraham Institute, Cambridge, UK, 2010).

[50]

Leger, A. & Leonardi, T. pycoQC, interactive quality control for Oxford Nanopore Sequencing. J. Open Source Softw. 4, 1236 (2019).

[51]

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).

[52]

Marcais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764-770 (2011).

[53]

Vurture, G. W. et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202-2204 (2017).

[54]

Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M. & Jaffe, D. B. Direct determination of diploid genome sequences. Genome Res. 27, 757-767 (2017).

[55]

Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257 (2019).

[56]

O'leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733-D745 (2016).

[57]

Roach, M. J., Schmidt, S. A. & Borneman, A. R. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinforma. 19, 460 (2018).

[58]

Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540-546 (2019).

[59]

Alonge, M. et al. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20, 224 (2019).

[60]

Xu, M. et al. TGS-GapCloser: a fast and accurate gap closer for large genomes with low coverage of error-prone long reads. Gigascience 9, giaa094 (2020).

[61]

Zhang, X., Zhang, S., Zhao, Q., Ming, R. & Tang, H. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nat. Plants 5, 833-845 (2019).

[62]

Marçais, G. et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput. Biol. 14, e1005944 (2018).

[63]

Gremme, G., Steinbiss, S. & Kurtz, S. GenomeTools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans. Comput. Biol. Bioinform 10, 645-656 (2013).

[64]

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).

[65]

Ou, S. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20, 275 (2019).

[66]

Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).

[67]

Brůna, T., Hoff, K. J., Lomsadze, A., Stanke, M. & Borodovsky, M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom. Bioinform 3, lqaa108 (2021).

[68]

Chan, P. P. & Lowe, T. M. tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. Methods Mol. Biol. 1962, 1-14 (2019).

[69]

Voorrips, R. E. MapChart: software for the graphical presentation of linkage maps and QTLs. J. Hered. 93, 77-78 (2002).

[70]

Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).

[71]

Xu, L. et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 47, W52-W58 (2019).

[72]

Li, Y., Pi, M., Gao, Q., Liu, Z. & Kang, C. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Hortic. Res. 6, 61 (2019).

[73]

Bailey, T. L. & Elkan, C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int Conf. Intell. Syst. Mol. Biol. 2, 28-36 (1994).

[74]

Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003).

[75]

Raymond, O. et al. The Rosa genome provides new insights into the domestication of modern roses. Nat. Genet. 50, 772-777 (2018).

[76]

Sánchez-Pérez, R. et al. Mutation of a bHLH transcription factor allowed almond domestication. Science 364, 1095-1098 (2019).

[77]

Wang, J. et al. A de novo assembly of the sweet cherry (Prunus avium cv. Tieton) genome using linked-read sequencing technology . PeerJ 8, e9114 (2020).

[78]

Shirasawa, K. et al. Phased genome sequence of an interspecific hybrid flowering cherry, ‘Somei-Yoshino’ (Cerasus x yedoensis) . DNA Res. 26, 379-389 (2019).

[79]

Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).

[80]

Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).

[81]

Zhu, T., Nevo, E., Sun, D. & Peng, J. Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution 66, 1833-1848 (2012).

[82]

Ooka, H. et al. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana . DNA Res. 10, 239-247 (2003).

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