Wolfberry genomes and the evolution of Lycium (Solanaceae).
Africa
Asia
Chromosomes, Plant
/ genetics
Evolution, Molecular
Fruit
/ genetics
Gene Expression Regulation, Plant
Genome, Plant
/ genetics
Geography
Lycium
/ classification
North America
Phylogeny
Polyploidy
Polysaccharides
/ metabolism
Solanaceae
/ classification
Species Specificity
Whole Genome Sequencing
/ methods
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
03 06 2021
03 06 2021
Historique:
received:
03
12
2020
accepted:
26
04
2021
entrez:
4
6
2021
pubmed:
5
6
2021
medline:
17
8
2021
Statut:
epublish
Résumé
Wolfberry Lycium, an economically important genus of the Solanaceae family, contains approximately 80 species and shows a fragmented distribution pattern among the Northern and Southern Hemispheres. Although several herbaceous species of Solanaceae have been subjected to genome sequencing, thus far, no genome sequences of woody representatives have been available. Here, we sequenced the genomes of 13 perennial woody species of Lycium, with a focus on Lycium barbarum. Integration with other genomes provides clear evidence supporting a whole-genome triplication (WGT) event shared by all hitherto sequenced solanaceous plants, which occurred shortly after the divergence of Solanaceae and Convolvulaceae. We identified new gene families and gene family expansions and contractions that first appeared in Solanaceae. Based on the identification of self-incompatibility related-gene families, we inferred that hybridization hotspots are enriched for genes that might be functioning in gametophytic self-incompatibility pathways in wolfberry. Extremely low expression of LOCULE NUBER (LC) and COLORLESS NON-RIPENING (CNR) orthologous genes during Lycium fruit development and ripening processes suggests functional diversification of these two genes between Lycium and tomato. The existence of additional flowering locus C-like MADS-box genes might correlate with the perennial flowering cycle of Lycium. Differential gene expression involved in the lignin biosynthetic pathway between Lycium and tomato likely illustrates woody and herbaceous differentiation. We also provide evidence that Lycium migrated from Africa into Asia, and subsequently from Asia into North America. Our results provide functional insights into Solanaceae origins, evolution and diversification.
Identifiants
pubmed: 34083720
doi: 10.1038/s42003-021-02152-8
pii: 10.1038/s42003-021-02152-8
pmc: PMC8175696
doi:
Substances chimiques
Polysaccharides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
671Références
Zhang, Z. Y., Lu, A. M. & D’Arcy, W. G. In Flora of China (eds Wu, Z. Y. & Raven, P. H.) 300–332 (Science Press, Beijing & Missouri Botanical Garden Press, 1994).
Sierro, N. et al. The tobacco genome sequence and its comparison with those of tomato and potato. Nat. Commun. 5, 1–9 (2014).
doi: 10.1038/ncomms4833
Potato Genome Sequencing Consortium. Genome sequence and analysis of the tuber crop potato. Nature 475, 189 (2011).
doi: 10.1038/nature10158
Zhou, Q. et al. Haplotype-resolved genome analyses of a heterozygous diploid potato. Nat. Genet. 52, 1018–1023 (2020).
pubmed: 32989320
pmcid: 7527274
doi: 10.1038/s41588-020-0699-x
Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641 (2012).
doi: 10.1038/nature11119
Bolger, A. et al. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat. Genet. 46, 1034–1038 (2014).
pubmed: 25064008
pmcid: 7036041
doi: 10.1038/ng.3046
Wang, X. et al. Genome of Solanum pimpinellifolium provides insights into structural variants during tomato breeding. Nat. Commun. 11, 5817 (2020).
pubmed: 33199703
pmcid: 7670462
doi: 10.1038/s41467-020-19682-0
Kim, S. et al. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46, 270–279 (2014).
pubmed: 24441736
doi: 10.1038/ng.2877
Kim, S. et al. New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biol. 18, 210 (2017).
pubmed: 29089032
pmcid: 5664825
doi: 10.1186/s13059-017-1341-9
Hirakawa, H. et al. Draft genome sequence of eggplant (Solanum melongena L.): the representative solanum species indigenous to the old world. DNA Res. 21, 649–660 (2014).
pubmed: 25233906
pmcid: 4263298
doi: 10.1093/dnares/dsu027
Bombarely, A. et al. Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nat. Plants 2, 16074 (2016).
pubmed: 27255838
doi: 10.1038/nplants.2016.74
Levin, R. A. & Miller, J. S. Relationships within tribe Lycieae (Solanaceae): paraphyly of Lycium and multiple origins of gender dimorphism. Am. J. Bot. 92, 2044–2053 (2005).
pubmed: 21646122
doi: 10.3732/ajb.92.12.2044
Symon, D. E. In Solanaceae III: Taxonomy–Chemistry–Evolution (eds Hawks., J. G., Laster, R. N., Nee, M. & Estrada, N., 139–150 (Royal Botanic Garden, Kew and the Linnean Society of London, 1991).
Raven, P. H. & Axelrod, D. I. Angiosperm biogeography and past continental movements. Ann. Mo. Bot. Gard. 61, 539–673 (1974).
doi: 10.2307/2395021
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).
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351
De Bie, T., Cristianini, N., Demuth, J. P. & Hahn, M. W. CAFÉ: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271 (2006).
pubmed: 16543274
doi: 10.1093/bioinformatics/btl097
Walters, R. G. et al. Identification of mutants of Arabidopsis defective in acclimation of photosynthesis to the light environment. Plant Physiol. 131, 472–481 (2003).
pubmed: 12586872
pmcid: 166824
doi: 10.1104/pp.015479
Jakab, G. et al. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol. 139, 267–274 (2005).
pubmed: 16113213
pmcid: 1203376
doi: 10.1104/pp.105.065698
Wu, S. et al. Genome sequences of two diploid wild relatives of cultivated sweet potato reveal targets for genetic improvement. Nat. Commun. 9, 4580 (2018).
pubmed: 30389915
pmcid: 6214957
doi: 10.1038/s41467-018-06983-8
Sims, T. L. & Robbins, T. P. In Petunia (eds Gerats, T. & Strommer, J.) 85–106 (Springer, 2009).
Igic, B. & Kohn, J. R. Evolutionary relationships among self-incompatibility RNases. Proc. Natl Acad. Sci. USA 98, 13167–13171 (2001).
pubmed: 11698683
doi: 10.1073/pnas.231386798
pmcid: 60842
Niu, S. C. et al. Lack of S-RNase-based gametophytic self-incompatibility in orchids suggests that this system evolved after the monocot-eudicot split. Front. Plant Sci. 8, 1106 (2017).
pubmed: 28690630
pmcid: 5479900
doi: 10.3389/fpls.2017.01106
Miller, J. S. & Kostyun, J. L. Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae). Heredity 107, 30–39 (2011).
pubmed: 21119705
doi: 10.1038/hdy.2010.151
Hillwig, M. S., Liu, X. & Macintosh, G. C. Petunia nectar proteins have ribonuclease activity. J. Exp. Bot. 61, 2951–2965 (2010).
pubmed: 20460362
pmcid: 2892141
doi: 10.1093/jxb/erq119
Cai, J. et al. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 47, 65–72 (2015).
pubmed: 25420146
doi: 10.1038/ng.3149
Ming, R. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47, 1435–1442 (2015).
pubmed: 26523774
pmcid: 4867222
doi: 10.1038/ng.3435
Li, X. et al. Systematic analysis of MYB family genes in potato and their multiple roles in development and stress responses. Biomolecules 9, 317 (2019).
pmcid: 6723670
doi: 10.3390/biom9080317
Chen, C. et al. Characterization of the Lycium barbarum fruit transcriptome and development of EST-SSR markers. PLoS ONE 12, e0187738 (2017).
pubmed: 29125846
pmcid: 5695279
doi: 10.1371/journal.pone.0187738
Qian, D., Zhao, Y., Yang, G. & Huang, L. Systematic review of chemical constituents in the genus Lycium (Solanaceae). Molecules 22, 911 (2017).
pmcid: 6152755
doi: 10.3390/molecules22060911
Zhao, Q. & Dixon, R. A. Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci. 16, 227–233 (2011).
pubmed: 21227733
doi: 10.1016/j.tplants.2010.12.005
Zhong, R. & Ye, Z. H. Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol. 56, 195–214 (2015).
pubmed: 25294860
doi: 10.1093/pcp/pcu140
Ruprecht, C. & Persson, S. Co-expression of cell-wall related genes: new tools and insights. Front. Plant Sci. 3, 83 (2012).
pubmed: 22645599
pmcid: 3355730
doi: 10.3389/fpls.2012.00083
Wei, Y., Xu, X., Tao, H. & Wang, P. Growth performance and physiological response in the halophyte Lycium barbarum grown at salt-affected soil. Ann. Appl. Biol. 149, 263–269 (2006).
doi: 10.1111/j.1744-7348.2006.00092.x
Zhao, J. H. et al. Physiological response of four wolfberry (Lycium Linn.) species under drought stress. J. Integr. Agric. 17, 603–612 (2018).
doi: 10.1016/S2095-3119(17)61754-4
Hu, Y. et al. Differential expression of candidate genes for lignin biosynthesis under drought stress in maize leaves. J. Appl. Genet. 50, 213–223 (2009).
pubmed: 19638676
doi: 10.1007/BF03195675
Moura, J. C. M. S., Bonine, C. A. V., de Oliveira Fernandes Viana, J., Dornelas, M. C. & Mazzafera, P. Abiotic and biotic stresses and changes in the lignin content and composition in plants. J. Integr. Plant Biol. 52, 360–376 (2010).
pubmed: 20377698
doi: 10.1111/j.1744-7909.2010.00892.x
Par̆enicová, 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).
pubmed: 12837945
pmcid: 165399
doi: 10.1105/tpc.011544
Gramzow, L. & Theißen, G. Phylogenomics reveals surprising sets of essential and dispensable clades of MIKCc‐group MADS‐box genes in flowering plants. J. Exp. Zool. B Mol. Dev. Evol. 324, 353–362 (2015).
pubmed: 25678468
doi: 10.1002/jez.b.22598
Whittaker, C. & Dean, C. The FLC locus: a platform for discoveries in epigenetics and adaption. Annu. Rev. Cell Dev. Biol. 33, 555–575 (2017).
pubmed: 28693387
doi: 10.1146/annurev-cellbio-100616-060546
Wang, R. et al. PEP1 regulates perennial flowering in Arabis alpine. Nature 459, 423–427 (2009).
pubmed: 19369938
doi: 10.1038/nature07988
Karlova, R. et al. Transcriptional control of fleshy fruit development and ripening. J. Exp. Bot. 65, 4527–4541 (2014).
pubmed: 25080453
doi: 10.1093/jxb/eru316
Giovannoni, J. J. Fruit ripening mutants yield insights into ripening control. Curr. Opin. Plant Biol. 10, 283–289 (2007).
pubmed: 17442612
doi: 10.1016/j.pbi.2007.04.008
Seymour, G. B. et al. Fruit development and ripening. Annu. Rev. Plant Biol. 64, 219–241 (2013).
pubmed: 23394500
doi: 10.1146/annurev-arplant-050312-120057
Giovannoni, J. J. Genetic regulation of fruit development and ripening. Plant Cell 16, S170–S180 (2004).
pubmed: 15010516
pmcid: 2643394
doi: 10.1105/tpc.019158
Rodríguez, G. R. et al. Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiol. 156, 275–285 (2011).
pubmed: 21441384
pmcid: 3091046
doi: 10.1104/pp.110.167577
Manning, K. et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38, 948–952 (2006).
pubmed: 16832354
doi: 10.1038/ng1841
Liu, W. et al. Structure characterization, chemical and enzymatic degradation, and chain conformation of an acidic polysaccharide from Lycium barbarum L. Carbohydr. Polym. 147, 114–124 (2016).
pubmed: 27178915
doi: 10.1016/j.carbpol.2016.03.087
Zong, Y. et al. Functional MYB transcription factor encoding gene AN2 is associated with anthocyanin biosynthesis in Lycium ruthenicum Murray. BMC Plant Biol. 19, 169 (2019).
pubmed: 31035916
pmcid: 6489258
doi: 10.1186/s12870-019-1752-8
Morrone, L. A. et al. Natural compounds and retinal ganglion cell neuroprotection. Prog. Brain Res. 220, 257–281 (2015).
pubmed: 26497795
doi: 10.1016/bs.pbr.2015.05.004
Zhou, L. et al. A pectin from fruits of Lycium barbarum L. decreases β-amyloid peptide production through modulating APP processing. Carbohydr. Polym. 201, 65–74 (2018).
pubmed: 30241864
doi: 10.1016/j.carbpol.2018.08.050
Takenaka, Y. et al. Pectin RG-I rhamnosyl transferases represent a novel plant-specific glycosyltransferase family. Nat. Plants 4, 669–676 (2018).
pubmed: 30082766
doi: 10.1038/s41477-018-0217-7
Kong, Y. et al. Molecular analysis of a family of Arabidopsis genes related to galacturonosyl transferases. Plant Physiol. 155, 1791–1805 (2011).
pubmed: 21300919
pmcid: 3091093
doi: 10.1104/pp.110.163220
Atmodjo, M. A., Hao, Z. & Mohnen, D. Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol. 64, 747–779 (2013).
pubmed: 23451775
doi: 10.1146/annurev-arplant-042811-105534
Su, S. & Higashiyama, T. Arabinogalactan proteins and their sugar chains: functions in plant reproduction, research methods, and biosynthesis. Plant Reprod. 31, 67–75 (2018).
pubmed: 29470639
doi: 10.1007/s00497-018-0329-2
Ebert, B. et al. The three members of the Arabidopsis glycosyltransferase family 92 are functional β-1,4-galactan synthases. Plant Cell Physiol. 59, 2624–2636 (2018).
pubmed: 30184190
doi: 10.1093/pcp/pcy180
Dilokpimol, A. et al. Galactosyltransferases from Arabidopsis thaliana in the biosynthesis of type II arabinogalactan: molecular interaction enhances enzyme activity. BMC Plant Biol. 14, 90 (2014).
pubmed: 24693939
pmcid: 4234293
doi: 10.1186/1471-2229-14-90
Yan, Y. et al. Composition and in vitro antioxidant activity of anthocyanins extracted from Lycium ruthenicum Murr. with different fruits and vegetables. Sci. Tech. Food Ind. 35, 133–136 (2014).
Wang, Z. et al. Comparison and multivariate statistical analysis of anthocyanin composition in Lycium ruthenicum Murray from different regions to trace geographical origins: the case of China. Food Chem. 246, 233–241 (2018).
pubmed: 29291844
doi: 10.1016/j.foodchem.2017.11.030
Albert, N. W. et al. A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26, 962–980 (2014).
pubmed: 24642943
pmcid: 4001404
doi: 10.1105/tpc.113.122069
Liu, Y. et al. Comparative analysis of carotenoid accumulation in two goji (Lycium barbarum L. and L. ruthenicum Murr.) fruits. BMC Plant Biol. 14, 269 (2014).
pubmed: 25511605
pmcid: 4276078
doi: 10.1186/s12870-014-0269-4
Karioti, A., Bergonzi, M. C., Vincieri, F. F. & Bilia, A. R. Validated method for the analysis of goji berry, a rich source of zeaxanthin dipalmitate. Agric. Food Chem. 62, 12529–12535 (2014).
doi: 10.1021/jf503769s
Jiang, Y., Chan, C. H. & Cronan, J. E. The soluble acyl-acyl carrier protein synthetase of Vibrio harveyi B392 is a member of the medium chain acyl-CoA synthetase family. Biochemistry 45, 10008–10019 (2006).
pubmed: 16906759
doi: 10.1021/bi060842w
Weimar, J. D., DiRusso, C. C., Delio, R. & Black, P. N. Functional role of fatty acyl-coenzyme A synthetase in the transmembrane movement and activation of exogenous long-chain fatty acids. Amino acid residues within the ATP/AMP signature motif of Escherichia coli FadD are required for enzyme activity and fatty acid transport. J. Biol. Chem. 277, 29369–29376 (2002).
pubmed: 12034706
doi: 10.1074/jbc.M107022200
Shockey, J. M., Fulda, M. S. & Browse, J. A. Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol. 129, 1710–1722 (2002).
pubmed: 12177484
pmcid: 166759
doi: 10.1104/pp.003269
Fukuda, T., Yokoyama, J. & Ohashi, H. Phylogeny and biogeography of the genus Lycium (Solanaceae): inferences from chloroplast DNA sequences. Mol. Phylogenet. Evol. 19, 246–258 (2001).
pubmed: 11341807
doi: 10.1006/mpev.2001.0921
Miller, J. S., Kamath, A., Damashek, J. & Levin, R. A. Out of America to Africa or Asia: inference of dispersal histories using nuclear and plastid DNA and the S-RNase self-incompatibility locus. Mol. Biol. Evol. 28, 793–801 (2011).
pubmed: 20855430
doi: 10.1093/molbev/msq253
Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).
pubmed: 28502977
doi: 10.1038/nrg.2017.26
Vurture, G. W. et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202–2204 (2017).
pubmed: 28369201
pmcid: 5870704
doi: 10.1093/bioinformatics/btx153
Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive kmer weighting and repeat separation. Genome Res. 27, 722–736 (2017).
Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).
pubmed: 11932250
pmcid: 187518
Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
pubmed: 20644199
pmcid: 2928508
doi: 10.1101/gr.107524.110
Jurka, J. et al. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110, 462–467 (2005).
pubmed: 16093699
doi: 10.1159/000084979
Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265–W268 (2007).
pubmed: 17485477
pmcid: 1933203
doi: 10.1093/nar/gkm286
Birney, E., Clamp, M. & Durbin, R. GeneWise and genomewise. Genome Res. 14, 988–995 (2004).
pubmed: 15123596
pmcid: 479130
doi: 10.1101/gr.1865504
Stanke, M., Schoffmann, O., Morgenstern, B. & Waack, S. Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7, 62 (2006).
pubmed: 16469098
pmcid: 1409804
doi: 10.1186/1471-2105-7-62
Salamov, A. A. & Solovyev, V. V. Ab initio gene finding in Drosophila genomic DNA. Genome Res 10, 516–522 (2000).
pubmed: 10779491
pmcid: 310882
doi: 10.1101/gr.10.4.516
Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).
pubmed: 15145805
doi: 10.1093/bioinformatics/bth315
Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111 (2009).
pubmed: 19289445
pmcid: 2672628
doi: 10.1093/bioinformatics/btp120
Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq. experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).
pubmed: 22383036
pmcid: 3334321
doi: 10.1038/nprot.2012.016
Ogata, H. et al. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27, 29–34 (1999).
pubmed: 9847135
pmcid: 148090
doi: 10.1093/nar/27.1.29
Hunter, S. et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211–D215 (2009).
pubmed: 18940856
doi: 10.1093/nar/gkn785
Griffiths, J. S. et al. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 33, D121–D124 (2005).
doi: 10.1093/nar/gki081
Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964 (1997).
pubmed: 9023104
pmcid: 146525
doi: 10.1093/nar/25.5.955
Li, L., Stoeckert, C. J. Jr. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189 (2003).
pubmed: 12952885
pmcid: 403725
doi: 10.1101/gr.1224503
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
pubmed: 17483113
doi: 10.1093/molbev/msm088
Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555–556 (1997).
pubmed: 9367129
Zwaenepoel, A. & Van de Peer, Y. wgd—simple command line tools for the analysis of ancient whole-genome duplications. Bioinformatics 35, 2153–2155 (2019).
pubmed: 30398564
doi: 10.1093/bioinformatics/bty915
Moreno-Hagelsieb, G. & Latimer, K. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 24, 319–324 (2008).
pubmed: 18042555
doi: 10.1093/bioinformatics/btm585
Proost, S. et al. i-ADHoRe 3.0-fast and sensitive detection of genomic homology in extremely large data sets. Nucleic Acids Res. 40, e11 (2012).
pubmed: 22102584
doi: 10.1093/nar/gkr955
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Andrews, S. FastQC: a quality control tool for high throughput sequence data http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).
pubmed: 22728672
pmcid: 3679285
doi: 10.4161/fly.19695
Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).
doi: 10.1093/bioinformatics/bti610
pubmed: 16081474
Fujii, S., Kubo, K. & Takayama, S. Non-self- and self-recognition models in plant self-incompatibility. Nat. Plants 2, 16130 (2016).
pubmed: 27595657
doi: 10.1038/nplants.2016.130
Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).
pubmed: 22039361
pmcid: 3197634
doi: 10.1371/journal.pcbi.1002195
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Wang, X. et al. Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. Plant Physiol. 125, 1012–1022 (2001).
pubmed: 11161057
pmcid: 64901
doi: 10.1104/pp.125.2.1012
Kubo, K., Paape, T. & Hatakeyama, M. Gene duplication and genetic exchange drive the evolution of S-RNase based self-incompatibility in Petunia. Nat. Plants 1, 14005 (2015).
pubmed: 27246052
doi: 10.1038/nplants.2014.5
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. systmatic. Biology 59, 307–321 (2010).
Vieira, J., Fonseca, N. A. & Vieira, C. P. An S-RNase-based gametophytic self-incompatibility system evolved only once in Eudicots. J. Mol. Evol. 67, 179–190 (2008).
pubmed: 18626680
doi: 10.1007/s00239-008-9137-x
Ramanauskas, K. & Igi¢, B. The evolutionary history of plant T2/S-type ribonucleases. Peer J. 5, e3790 (2017).
pubmed: 28924504
doi: 10.7717/peerj.3790
pmcid: 5598434
Roalson, E. S-RNases and sexual incompatibility: structure, functions, and evolutionary. perspectives. Mol. Phylogenet. Evol. 29, 490–506 (2003).
pubmed: 14615188
doi: 10.1016/S1055-7903(03)00195-7
Zdobnov, E. M. & Apweiler, R. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847–848 (2001).
pubmed: 11590104
doi: 10.1093/bioinformatics/17.9.847
Letunic, L., Doerks, T. & Bork, P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 43, D257–D260 (2014).
pubmed: 25300481
pmcid: 4384020
doi: 10.1093/nar/gku949
Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony method. Mol. Biol. Evol. 28, 2731–2739 (2011).
pubmed: 21546353
pmcid: 3203626
doi: 10.1093/molbev/msr121
Chen, C. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194–1202 (2020).
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Yang, J., Lee, S. H., Goddard, M. E. & Visscher, P. M. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76–82 (2011).
pubmed: 21167468
pmcid: 3014363
doi: 10.1016/j.ajhg.2010.11.011
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Chang, C. C. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4, 7 (2015).
pubmed: 25722852
pmcid: 4342193
doi: 10.1186/s13742-015-0047-8
Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493 (2011).
pubmed: 21753753
pmcid: 3154645
doi: 10.1038/nature10231
Amborella Genome Project. The Amborella genome and the evolution of flowering plants. Science 342, 1241089 (2013).
doi: 10.1126/science.1241089
Wang, Y. et al. Genome-wide analysis of the MADS-box transcription factor family in Solanum lycopersicum. Int. J. Mol. Sci. 20, 2961 (2019).
pmcid: 6627509
doi: 10.3390/ijms20122961
Gao, H. et al. Genome-wide survey of potato MADS-box genes reveals that StMADS1 and StMADS13 are putative downstream targets of tuberigen StSP6A. BMC Genomics 19, 726 (2018).
pubmed: 30285611
pmcid: 6171223
doi: 10.1186/s12864-018-5113-z
Leseberg, C. H. et al. Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378, 84–94 (2006).
pubmed: 16831523
doi: 10.1016/j.gene.2006.05.022
Arora, R. et al. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8, 242 (2007).
pubmed: 17640358
pmcid: 1947970
doi: 10.1186/1471-2164-8-242
Zhang, G. et al. The Apostasia genome and the evolution of orchid. Nature 549, 379–383 (2017).
pubmed: 28902843
pmcid: 7416622
doi: 10.1038/nature23897