Aethionema arabicum genome annotation using PacBio full-length transcripts provides a valuable resource for seed dormancy and Brassicaceae evolution research
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
FWF I1477
Austrian Science Fund FWF - Austria
FWF I3979
Austrian Science Fund FWF - Austria
BB/M00192X/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
33453123
PubMed Central
PMC8641386
DOI
10.1111/tpj.15161
Knihovny.cz E-zdroje
- Klíčová slova
- Aethionema arabicum, Brassicaceae evolution, Iso-seq, alternative splicing, genome annotation, seed germination, transcription factors,
- MeSH
- Brassicaceae genetika metabolismus fyziologie MeSH
- genom rostlinný genetika MeSH
- klíčení genetika fyziologie MeSH
- regulace genové exprese u rostlin genetika fyziologie MeSH
- semena rostlinná genetika metabolismus fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Aethionema arabicum is an important model plant for Brassicaceae trait evolution, particularly of seed (development, regulation, germination, dormancy) and fruit (development, dehiscence mechanisms) characters. Its genome assembly was recently improved but the gene annotation was not updated. Here, we improved the Ae. arabicum gene annotation using 294 RNA-seq libraries and 136 307 full-length PacBio Iso-seq transcripts, increasing BUSCO completeness by 11.6% and featuring 5606 additional genes. Analysis of orthologs showed a lower number of genes in Ae. arabicum than in other Brassicaceae, which could be partially explained by loss of homeologs derived from the At-α polyploidization event and by a lower occurrence of tandem duplications after divergence of Aethionema from the other Brassicaceae. Benchmarking of MADS-box genes identified orthologs of FUL and AGL79 not found in previous versions. Analysis of full-length transcripts related to ABA-mediated seed dormancy discovered a conserved isoform of PIF6-β and antisense transcripts in ABI3, ABI4 and DOG1, among other cases found of different alternative splicing between Turkey and Cyprus ecotypes. The presented data allow alternative splicing mining and proposition of numerous hypotheses to research evolution and functional genomics. Annotation data and sequences are available at the Ae. arabicum DB (https://plantcode.online.uni-marburg.de/aetar_db).
BIOSS Centre for Biological Signaling Studies University of Freiburg Freiburg Germany
Biosystematics Group Wageningen University Wageningen The Netherlands
LOEWE Center for Synthetic Microbiology University of Marburg Marburg Germany
Matthias Schleiden Institute Genetics Friedrich Schiller University Jena Jena Germany
Plant Cell Biology Department of Biology University of Marburg Marburg Germany
School of Biological Sciences Royal Holloway University of London Egham Surrey UK
Zobrazit více v PubMed
Altschul, S.F. , Gish, W. , Miller, W. , Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403–410. PubMed
Arora, R. , Agarwal, P. , Ray, S. , Singh, A.K. , Singh, V.P. , Tyagi, A.K. and Kapoor, S. (2007) MADS‐box gene family in rice: genome‐wide identification, organization and expression profiling during reproductive development and stress. BMC Genom. 8, 242. PubMed PMC
Arshad, W. , Sperber, K. , Steinbrecher, T. , Nichols, B. , Jansen, V.A.A. , Leubner‐Metzger, G. and Mummenhoff, K. (2019) Dispersal biophysics and adaptive significance of dimorphic diaspores in the annual Aethionema arabicum (Brassicaceae). New Phytol. 221, 1434–1446. PubMed PMC
Barros‐Galvao, T. , Dave, A. , Gilday, A.D. , Harvey, D. , Vaistij, F.E. and Graham, I.A. (2020) ABA INSENSITIVE4 promotes rather than represses PHYA‐dependent seed germination in Arabidopsis thaliana. New Phytol. 226, 953–956. PubMed PMC
Bentsink, L. and Koornneef, M. (2008) Seed dormancy and germination. The Arabidopsis Book/American Society of Plant Biologists, 6, e0119. PubMed PMC
Bhattacharya, S. , Mayland‐Quellhorst, S. , Muller, C. and Mummenhoff, K. (2019a) Two‐tier morpho‐chemical defence tactic in Aethionema via fruit morph plasticity and glucosinolates allocation in diaspores. Plant Cell Environ. 42, 1381–1392. PubMed
Bhattacharya, S. , Sperber, K. , Ozudogru, B. , Leubner‐Metzger, G. and Mummenhoff, K. (2019b) Naturally‐primed life strategy plasticity of dimorphic Aethionema arabicum facilitates optimal habitat colonization. Sci Rep. 9, 16108. PubMed PMC
Boratyn, G.M. , Camacho, C. , Cooper, P.S. et al . (2013) BLAST: a more efficient report with usability improvements. Nucleic Acids Res. 41, W29–W33. PubMed PMC
Buels, R. , Yao, E. , Diesh, C.M. et al . (2016) JBrowse: a dynamic web platform for genome visualization and analysis. Genome Biol. 17, 66. PubMed PMC
Camacho, C. , Coulouris, G. , Avagyan, V. , Ma, N. , Papadopoulos, J. , Bealer, K. and Madden, T.L. (2009) BLAST+: architecture and applications. BMC Bioinform. 10, 421. PubMed PMC
Campbell, M.S. , Holt, C. , Moore, B. and Yandell, M. (2014) Genome annotation and curation using MAKER and MAKER‐P. Curr. Protoc. Bioinform. 48, 11–39. PubMed PMC
Capella‐Gutierrez, S. , Silla‐Martinez, J.M. and Gabaldon, T. (2009) trimAl: a tool for automated alignment trimming in large‐scale phylogenetic analyses. Bioinformatics, 25, 1972–1973. PubMed PMC
Carrillo‐Barral, N. , Rodriguez‐Gacio, M.D.C. and Matilla, A.J. (2020) Delay of germination‐1 (DOG1): a key to understanding seed dormancy. Plants (Basel), 9, 480. PubMed PMC
Cartolano, M. , Huettel, B. , Hartwig, B. , Reinhardt, R. and Schneeberger, K. (2016) cDNA library enrichment of full length transcripts for SMRT long read sequencing. PLoS One, 11, e0157779. PubMed PMC
Cheng, S. , van den Bergh, E. , Zeng, P. et al . (2013) The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers. Plant Cell, 25, 2813–2830. PubMed PMC
Christianson, J.A. , Wilson, I.W. , Llewellyn, D.J. and Dennis, E.S. (2009) The low‐oxygen‐induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low‐oxygen treatment. Plant Physiol. 149, 1724–1738. PubMed PMC
Del Carmen Martinez‐Ballesta, M. , Moreno, D.A. and Carvajal, M. (2013) The physiological importance of glucosinolates on plant response to abiotic stress in Brassica. Int. J. Mol. Sci. 14, 11607–11625. PubMed PMC
Dong, X. , Jiang, Y. and Hur, Y. (2019) Genome‐wide analysis of glycoside hydrolase family 1 beta‐glucosidase genes in brassica rapa and their potential role in pollen development. Int. J. Mol. Sci. 20, 1663. PubMed PMC
Eddy, S.R. (2011) Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195. PubMed PMC
El‐Gebali, S. , Mistry, J. , Bateman, A. et al . (2019) The Pfam protein families database in 2019. Nucleic Acids Res. 47, D427–D432. PubMed PMC
Emms, D.M. and Kelly, S. (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238. PubMed PMC
Fedak, H. , Palusinska, M. , Krzyczmonik, K. , Brzezniak, L. , Yatusevich, R. , Pietras, Z. , Kaczanowski, S. and Swiezewski, S. (2016) Control of seed dormancy in Arabidopsis by a cis‐acting noncoding antisense transcript. Proc. Natl Acad. Sci. USA, 113, E7846–E7855. PubMed PMC
Fernandez‐Pozo, N. , Haas, F.B. , Meyberg, R. et al . (2020) PEATmoss (Physcomitrella Expression Atlas Tool): a unified gene expression atlas for the model plant Physcomitrella patens . Plant J. 102, 165–177. PubMed
Fernandez‐Pozo, N. , Menda, N. , Edwards, J.D. et al . (2015) The Sol Genomics Network (SGN)–from genotype to phenotype to breeding. Nucleic Acids Res. 43, D1036–D1041. PubMed PMC
Finch‐Savage, W.E. and Leubner‐Metzger, G. (2006) Seed dormancy and the control of germination. New Phytol. 171, 501–523. PubMed
Flutre, T. , Duprat, E. , Feuillet, C. and Quesneville, H. (2011) Considering transposable element diversification in de novo annotation approaches. PLoS One, 6, e16526. PubMed PMC
Foissac, S. and Sammeth, M. (2007) ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets. Nucleic Acids Res. 35, W297–W299. PubMed PMC
Gagete, A.P. , Riera, M. , Franco, L. and Rodrigo, M.I. (2009) Functional analysis of the isoforms of an ABI3‐like factor of Pisum sativum generated by alternative splicing. J. Exp. Bot. 60, 1703–1714. PubMed PMC
Gao, R. , Wang, Y. , Gruber, M.Y. and Hannoufa, A. (2017) miR156/SPL10 modulates lateral root development, branching and leaf morphology in Arabidopsis by silencing AGAMOUS‐LIKE 79. Front. Plant Sci. 8, 2226. PubMed PMC
Gao, Y.F. , Liu, J.K. , Zhang, Z.G. , Sun, X.C. , Zhang, N. , Fan, J. , Niu, X.L. , Xiao, F.M. and Liu, Y.S. (2013) Functional characterization of two alternatively spliced transcripts of tomato ABSCISIC ACID INSENSITIVE3 (ABI3) gene. Plant Mol. Biol. 82, 131–145. PubMed
Golonka, D. , Fischbach, P. , Jena, S.G. , Kleeberg, J.R.W. , Essen, L.O. , Toettcher, J.E. , Zurbriggen, M.D. and Moglich, A. (2019) Deconstructing and repurposing the light‐regulated interplay between Arabidopsis phytochromes and interacting factors. Communications Biol. 2, 10.1038/s42003-019-0687-9. PubMed DOI PMC
Goodstein, D.M. , Shu, S. , Howson, R. et al . (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186. PubMed PMC
Gordon, S.P. , Tseng, E. , Salamov, A. et al . (2015) Widespread polycistronic transcripts in fungi revealed by single‐molecule mRNA sequencing. PLoS One, 10, e0132628. PubMed PMC
Grabherr, M.G. , Haas, B.J. , Yassour, M. et al . (2011) Full‐length transcriptome assembly from RNA‐Seq data without a reference genome. Nat. Biotechnol. 29, 644–652. PubMed PMC
Graeber, K. , Linkies, A. , Muller, K. , Wunchova, A. , Rott, A. and Leubner‐Metzger, G. (2010) Cross‐species approaches to seed dormancy and germination: conservation and biodiversity of ABA‐regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol. Biol. 73, 67–87. PubMed
Graeber, K. , Linkies, A. , Wood, A.T. and Leubner‐Metzger, G. (2011) A guideline to family‐wide comparative state‐of‐the‐art quantitative RT‐PCR analysis exemplified with a Brassicaceae cross‐species seed germination case study. Plant Cell, 23, 2045–2063. PubMed PMC
Graeber, K. , Voegele, A. , Buttner‐Mainik, A. , Sperber, K. , Mummenhoff, K. and Leubner‐Metzger, G. (2013) Spatiotemporal seed development analysis provides insight into primary dormancy induction and evolution of the Lepidium delay of germination1 genes. Plant Physiol. 161, 1903–1917. PubMed PMC
Gramzow, L. , Ritz, M.S. and Theißen, G. (2010) On the origin of MADS‐domain transcription factors. Trends Genet. 26, 149–153. PubMed
Gramzow, L. and Theißen, G. (2010) A hitchhiker's guide to the MADS world of plants. Genome Biol. 11, 214. PubMed PMC
Gramzow, L. and Theißen, G. (2015) Phylogenomics reveals surprising sets of essential and dispensable clades of MIKC(c)‐group MADS‐box genes in flowering plants. J. Exp. Zool. B Mol. Dev. Evol. 324, 353–362. PubMed
Gramzow, L. and Theissen, G. (2013) Phylogenomics of MADS‐Box genes in plants ‐ two opposing life styles in one gene family. Biology (Basel), 2, 1150–1164. PubMed PMC
Gramzow, L. , Weilandt, L. and Theißen, G. (2014) MADS goes genomic in conifers: towards determining the ancestral set of MADS‐box genes in seed plants. Ann. Bot. 114, 1407–1429. PubMed PMC
Grillo, G. , Turi, A. , Licciulli, F. et al . (2010) UTRdb and UTRsite (RELEASE 2010): a collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res. 38, D75–D80. PubMed PMC
Gu, Q. , Ferrandiz, C. , Yanofsky, M.F. and Martienssen, R. (1998) The FRUITFULL MADS‐box gene mediates cell differentiation during Arabidopsis fruit development. Development, 125, 1509–1517. PubMed
Haas, B.J. , Delcher, A.L. , Mount, S.M. et al . (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666. PubMed PMC
Hardwick, S.A. , Joglekar, A. , Flicek, P. , Frankish, A. and Tilgner, H.U. (2019) Getting the entire message: progress in isoform sequencing. Front. Genet. 10, 709. PubMed PMC
Haudry, A. , Platts, A.E. , Vello, E. et al . (2013) An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat. Genet. 45, 891–898. PubMed
Henschel, K. , Kofuji, R. , Hasebe, M. , Saedler, H. , Munster, T. and Theissen, G. (2002) Two ancient classes of MIKC‐type MADS‐box genes are present in the moss Physcomitrella patens . Mol. Biol. Evol. 19, 801–814. PubMed
Hoede, C. , Arnoux, S. , Moisset, M. , Chaumier, T. , Inizan, O. , Jamilloux, V. and Quesneville, H. (2014) PASTEC: an automatic transposable element classification tool. PLoS One, 9, e91929. PubMed PMC
Hoffmeier, A. , Gramzow, L. , Bhide, A.S. , Kottenhagen, N. , Greifenstein, A. , Schubert, O. , Mummenhoff, K. , Becker, A. and Theissen, G. (2018) A dead gene walking: convergent degeneration of a clade of MADS‐Box genes in crucifers. Mol. Biol. Evol. 35, 2618–2638. PubMed
Holdsworth, M.J. , Bentsink, L. and Soppe, W.J.J. (2008) Molecular networks regulating Arabidopsis seed maturation, after‐ripening, dormancy and germination. New Phytol. 179, 33–54. PubMed
Hwang, I.S. , Choi, D.S. , Kim, N.H. , Kim, D.S. and Hwang, B.K. (2014) The pepper cysteine/histidine‐rich DC1 domain protein CaDC1 binds both RNA and DNA and is required for plant cell death and defense response. New Phytol. 201, 518–530. PubMed
Iuchi, S. , Kobayashi, M. , Taji, T. , Naramoto, M. , Seki, M. , Kato, T. , Tabata, S. , Kakubari, Y. , Yamaguchi‐Shinozaki, K. and Shinozaki, K. (2001) Regulation of drought tolerance by gene manipulation of 9‐cis‐epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 27, 325–333. PubMed
Jiménez‐Ruiz, J. , Ramírez‐Tejero, J. , Fernández‐Pozo, N. et al . (2020) Transposon activation is a major driver in the genome evolution of cultivated olive trees (Olea europaea L.). Plant Genome, e20000. PubMed
Jones, P. , Binns, D. , Chang, H.Y. et al . (2014) InterProScan 5: genome‐scale protein function classification. Bioinformatics, 30, 1236–1240. PubMed PMC
Joseph, M.P. , Papdi, C. , Kozma‐Bognar, L. , Nagy, I. , Lopez‐Carbonell, M. , Rigo, G. , Koncz, C. and Szabados, L. (2014) The Arabidopsis ZINC FINGER PROTEIN3 interferes with abscisic acid and light signaling in seed germination and plant development. Plant Physiol. 165, 1203–1220. PubMed PMC
Keilwagen, J. , Wenk, M. , Erickson, J.L. , Schattat, M.H. , Grau, J. and Hartung, F. (2016) Using intron position conservation for homology‐based gene prediction. Nucleic Acids Res. 44, e89. PubMed PMC
Kelemen, O. , Convertini, P. , Zhang, Z. , Wen, Y. , Shen, M. , Falaleeva, M. and Stamm, S. (2013) Function of alternative splicing. Gene, 514, 1–30. PubMed PMC
Khanna, R. , Huq, E. , Kikis, E.A. , Al‐Sady, B. , Lanzatella, C. and Quail, P.H. (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix‐loop‐helix transcription factors. Plant Cell, 16, 3033–3044. PubMed PMC
Kodama, Y. , Shumway, M. and Leinonen, R. and International Nucleotide Sequence Database, C. (2012) The Sequence Read Archive: explosive growth of sequencing data. Nucleic Acids Res. 40, D54–D56. PubMed PMC
Korf, I. (2004) Gene finding in novel genomes. BMC Bioinform. 5, 59. PubMed PMC
Lefebvre, V. , North, H. , Frey, A. , Sotta, B. , Seo, M. , Okamoto, M. , Nambara, E. and Marion‐Poll, A. (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J. 45, 309–319. PubMed
Lenser, T. , Graeber, K. , Cevik, O.S. et al . (2016) Developmental control and plasticity of fruit and seed dimorphism in Aethionema arabicum . Plant Physiol. 172, 1691–1707. PubMed PMC
Lenser, T. , Tarkowska, D. , Novak, O. , Wilhelmsson, P.K.I. , Bennett, T. , Rensing, S.A. , Strnad, M. and Theissen, G. (2018) When the BRANCHED network bears fruit: how carpic dominance causes fruit dimorphism in Aethionema. Plant J. 94, 352–371. PubMed
Lyons, E. and Freeling, M. (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53, 661–673. PubMed
Majee, M. , Kumar, S. , Kathare, P.K. et al . (2018) KELCH F‐BOX protein positively influences Arabidopsis seed germination by targeting PHYTOCHROME‐INTERACTING FACTOR1. Proc Natl Acad Sci USA, 115, E4120–E4129. PubMed PMC
Marella, H.H. and Quatrano, R.S. (2007) The B2 domain of VIVIPAROUS1 is bi‐functional and regulates nuclear localization and transactivation. Planta, 225, 863–872. PubMed
Martinez‐Andujar, C. , Ordiz, M.I. , Huang, Z. , Nonogaki, M. , Beachy, R.N. and Nonogaki, H. (2011) Induction of 9‐cis‐epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proc. Natl Acad. Sci. USA, 108, 17225–17229. PubMed PMC
Maumus, F. and Quesneville, H. (2014) Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLoS One, 9, e94101. PubMed PMC
McCarty, D.R. , Hattori, T. , Carson, C.B. , Vasil, V. , Lazar, M. and Vasil, I.K. (1991) The Viviparous‐1 developmental gene of maize encodes a novel transcriptional activator. Cell, 66, 895–905. PubMed
McGinnis, K.M. , Thomas, S.G. , Soule, J.D. , Strader, L.C. , Zale, J.M. , Sun, T.P. and Steber, C.M. (2003) The Arabidopsis SLEEPY1 gene encodes a putative F‐box subunit of an SCF E3 ubiquitin ligase. Plant Cell, 15, 1120–1130. PubMed PMC
McKibbin, R.S. , Wilkinson, M.D. , Bailey, P.C. , Flintham, J.E. , Andrew, L.M. , Lazzeri, P.A. , Gale, M.D. , Lenton, J.R. and Holdsworth, M.J. (2002) Transcripts of Vp‐1 homeologues are misspliced in modern wheat and ancestral species. Proc. Natl Acad. Sci. USA, 99, 10203–10208. PubMed PMC
Mérai, Z. , Graeber, K. , Wilhelmsson, P. et al . (2019) Aethionema arabicum: a novel model plant to study the light control of seed germination. J. Exp. Bot. 70, 3313–3328. PubMed PMC
Miller, M.A. , Pfeiffer, W. and Schwartz, T. (2011) The CIPRES science gateway: a community resource for phylogenetic analyses. In Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery. Salt Lake City, Utah: Association for Computing Machinery, pp. Article 41
Ming, R. , Hou, S. , Feng, Y. et al . (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature, 452, 991–996. PubMed PMC
Mohammadin, S. , Nguyen, T.P. , van Weij, M.S. , Reichelt, M. and Schranz, M.E. (2017) Flowering Locus C (FLC) is a potential major regulator of glucosinolate content across developmental stages of Aethionema arabicum (Brassicaceae). Front. Plant Sci. 8, 876. PubMed PMC
Mohammadin, S. , Wang, W. , Liu, T. et al . (2018) Genome‐wide nucleotide diversity and associations with geography, ploidy level and glucosinolate profiles in Aethionema arabicum (Brassicaceae). Plant Syst. Evol. 304, 619–630.
Monke, G. , Altschmied, L. , Tewes, A. , Reidt, W. , Mock, H.P. , Baumlein, H. and Conrad, U. (2004) Seed‐specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta, 219, 158–166. PubMed
Nakabayashi, K. , Bartsch, M. , Ding, J. and Soppe, W.J. (2015) Seed dormancy in Arabidopsis requires self‐binding ability of DOG1 protein and the presence of multiple isoforms generated by alternative splicing. PLoS Genet. 11, e1005737. PubMed PMC
Nakamura, S. , Lynch, T.J. and Finkelstein, R.R. (2001) Physical interactions between ABA response loci of Arabidopsis. Plant J. 26, 627–635. PubMed
Narsai, R. , Gouil, Q. , Secco, D. , Srivastava, A. , Karpievitch, Y.V. , Liew, L.C. , Lister, R. , Lewsey, M.G. and Whelan, J. (2017) Extensive transcriptomic and epigenomic remodelling occurs during Arabidopsis thaliana germination. Genome Biol. 18, 172. PubMed PMC
Nee, G. , Kramer, K. , Nakabayashi, K. , Yuan, B. , Xiang, Y. , Miatton, E. , Finkemeier, I. and Soppe, W.J.J. (2017) DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nat. Commun. 8, 72. PubMed PMC
Nguyen, T.P. , Muhlich, C. , Mohammadin, S. , van den Bergh, E. , Platts, A.E. , Haas, F.B. , Rensing, S.A. and Schranz, M.E. (2019) Genome improvement and genetic map construction for Aethionema arabicum, the first divergent branch in the Brassicaceae family. G3: Genes ‐ Genomes ‐ Genetics, 9, 3521–3530. PubMed PMC
Nikolov, L.A. , Shushkov, P. , Nevado, B. , Gan, X. , Al‐Shehbaz, I.A. , Filatov, D. , Bailey, C.D. and Tsiantis, M. (2019) Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytol. 222, 1638–1651. PubMed
Nishimura, N. , Tsuchiya, W. , Moresco, J.J. et al . (2018) Control of seed dormancy and germination by DOG1‐AHG1 PP2C phosphatase complex via binding to heme. Nat. Commun. 9, 2132. PubMed PMC
Nonogaki, H. (2017) Seed biology updates ‐ highlights and new discoveries in seed dormancy and germination research. Front. Plant Sci. 8, 524. PubMed PMC
Nonogaki, H. (2019) Seed germination and dormancy: the classic story, new puzzles, and evolution. J. Integr. Plant Biol. 61, 541–563. PubMed
Nyiko, T. , Auber, A. , Szabadkai, L. , Benkovics, A. , Auth, M. , Merai, Z. , Kerenyi, Z. , Dinnyes, A. , Nagy, F. and Silhavy, D. (2017) Expression of the eRF1 translation termination factor is controlled by an autoregulatory circuit involving readthrough and nonsense‐mediated decay in plants. Nucleic Acids Res. 45, 4174–4188. PubMed PMC
Oh, E. , Kang, H. , Yamaguchi, S. , Park, J. , Lee, D. , Kamiya, Y. and Choi, G. (2009) Genome‐wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3‐LIKE5 during seed germination in Arabidopsis. Plant Cell, 21, 403–419. PubMed PMC
Onate‐Sanchez, L. and Vicente‐Carbajosa, J. (2008) DNA‐free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res Notes, 1, 93. PubMed PMC
Paik, I. , Kathare, P.K. , Kim, J.I. and Huq, E. (2017) Expanding roles of PIFs in signal integration from multiple processes. Mol. Plant, 10, 1035–1046. PubMed PMC
Papi, M. , Sabatini, S. , Bouchez, D. , Camilleri, C. , Costantino, P. and Vittorioso, P. (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev. 14, 28–33. PubMed PMC
Penfield, S. , Josse, E.M. and Halliday, K.J. (2010) A role for an alternative splice variant of PIF6 in the control of Arabidopsis primary seed dormancy. Plant Mol. Biol. 73, 89–95. PubMed
Peng, J. , Yu, D. , Wang, L. , Xie, M. , Yuan, C. , Wang, Y. , Tang, D. , Zhao, X. and Liu, X. (2012) Arabidopsis F‐box gene FOA1 involved in ABA signaling. Sci. China Life Sci. 55, 497–506. PubMed
Pertea, M. , Pertea, G.M. , Antonescu, C.M. , Chang, T.C. , Mendell, J.T. and Salzberg, S.L. (2015) StringTie enables improved reconstruction of a transcriptome from RNA‐seq reads. Nat. Biotechnol. 33, 290–295. PubMed PMC
Pracana, R. , Priyam, A. , Levantis, I. , Nichols, R.A. and Wurm, Y. (2017) The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB. Mol. Ecol. 26, 2864–2879. PubMed PMC
Priya, R. and Siva, R. (2015) Analysis of phylogenetic and functional diverge in plant nine‐cis epoxycarotenoid dioxygenase gene family. J. Plant Res. 128, 519–534. PubMed
Punzo, P. , Ruggiero, A. , Possenti, M. , Perrella, G. , Nurcato, R. , Costa, A. , Morelli, G. , Grillo, S. and Batelli, G. (2020) DRT111/SFPS splicing factor controls abscisic acid sensitivity during seed development and germination. Plant Physiol. 183, 793–807. PubMed PMC
Quesneville, H. , Bergman, C.M. , Andrieu, O. , Autard, D. , Nouaud, D. , Ashburner, M. and Anxolabehere, D. (2005) Combined evidence annotation of transposable elements in genome sequences. PLoS Comput. Biol. 1, 166–175. PubMed PMC
Quinlan, A.R. and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841–842. PubMed PMC
Raineri, J. , Hartman, M.D. , Chan, R.L. , Iglesias, A.A. and Ribichich, K.F. (2016) A sunflower WRKY transcription factor stimulates the mobilization of seed‐stored reserves during germination and post‐germination growth. Plant Cell Rep. 35, 1875–1890. PubMed
Rice, P. , Longden, I. and Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277. PubMed
Rodriguez‐Gacio Mdel, C. , Matilla‐Vazquez, M.A. and Matilla, A.J. (2009) Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal Behav. 4, 1035–1049. PubMed PMC
Roshan, U. and Livesay, D.R. (2006) Probalign: multiple sequence alignment using partition function posterior probabilities. Bioinformatics, 22, 2715–2721. PubMed
Salamov, A.A. and Solovyev, V.V. (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res. 10, 516–522. PubMed PMC
Salmela, L. and Rivals, E. (2014) LoRDEC: accurate and efficient long read error correction. Bioinformatics, 30, 3506–3514. PubMed PMC
Santamaria, M.E. , Diaz‐Mendoza, M. , Diaz, I. and Martinez, M. (2014) Plant protein peptidase inhibitors: an evolutionary overview based on comparative genomics. BMC Genom. 15, 812. PubMed PMC
Schranz, M.E. , Mohammadin, S. and Edger, P.P. (2012) Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag‐Time Model. Curr. Opin. Plant Biol. 15, 147–153. PubMed
Seppey, M. , Manni, M. and Zdobnov, E.M. (2019) BUSCO: assessing genome assembly and annotation completeness. Methods Mol. Biol. 1962, 227–245. PubMed
Shao, M. and Kingsford, C. (2017) Accurate assembly of transcripts through phase‐preserving graph decomposition. Nat. Biotechnol. 35, 1167–1169. PubMed PMC
Simao, F.A. , Waterhouse, R.M. , Ioannidis, P. , Kriventseva, E.V. and Zdobnov, E.M. (2015) BUSCO: assessing genome assembly and annotation completeness with single‐copy orthologs. Bioinformatics, 31, 3210–3212. PubMed
Singh, D.K. , Calvino, M. , Brauer, E.K. et al . (2014) The tomato kinome and the tomato kinase library ORFeome: novel resources for the study of kinases and signal transduction in tomato and Solanaceae species. Mol. Plant Microbe Interact. 27, 7–17. PubMed
Smaczniak, C. , Immink, R.G. , Angenent, G.C. and Kaufmann, K. (2012) Developmental and evolutionary diversity of plant MADS‐domain factors: insights from recent studies. Development, 139, 3081–3098. PubMed
Solovyev, V. , Kosarev, P. , Seledsov, I. and Vorobyev, D. (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7(Suppl 1), S10 11–12. PubMed PMC
Song, S. , Dai, X. and Zhang, W.H. (2012) A rice F‐box gene, OsFbx352, is involved in glucose‐delayed seed germination in rice. J. Exp. Bot. 63, 5559–5568. PubMed PMC
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics, 30, 1312–1313. PubMed PMC
Stanke, M. , Keller, O. , Gunduz, I. , Hayes, A. , Waack, S. and Morgenstern, B. (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439. PubMed PMC
Sugliani, M. , Brambilla, V. , Clerkx, E.J.M. , Koornneef, M. and Soppe, W.J.J. (2010) The conserved splicing factor SUA controls alternative splicing of the developmental regulator ABI3 in Arabidopsis. Plant Cell, 22, 1936–1946. PubMed PMC
Suzuki, M. , Kao, C.Y. and McCarty, D.R. (1997) The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell, 9, 799–807. PubMed PMC
Suzuki, M. and McCarty, D.R. (2008) Functional symmetry of the B3 network controlling seed development. Curr. Opin. Plant Biol. 11, 548–553. PubMed
Tan, B.C. , Joseph, L.M. , Deng, W.T. , Liu, L. , Li, Q.B. , Cline, K. and McCarty, D.R. (2003) Molecular characterization of the Arabidopsis 9‐cis epoxycarotenoid dioxygenase gene family. Plant J. 35, 44–56. PubMed
Theißen, G. , Rumpler, F. and Gramzow, L. (2018) Array of MADS‐box genes: facilitator for rapid adaptation? Trends Plant Sci. 23, 563–576. PubMed
Thiruppathi, D. (2020) SPLICEd in the seeds: integration of abscisic acid and light signaling in Arabidopsis. Plant Physiol. 183, 445–446. PubMed PMC
Thomas, B.C. , Rapaka, L. , Lyons, E. , Pedersen, B. and Freeling, M. (2007) Arabidopsis intragenomic conserved noncoding sequence. Proc. Natl Acad. Sci. USA, 104, 3348–3353. PubMed PMC
Toh, S. , Imamura, A. , Watanabe, A. et al . (2008) High temperature‐induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol. 146, 1368–1385. PubMed PMC
Tripathi, S. , Hoang, Q.T.N. , Han, Y.J. and Kim, J.I. (2019) Regulation of photomorphogenic development by plant phytochromes. Int. J. Mol. Sci. 20, 6165. PubMed PMC
UniProt Consortium (2019) UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 47, D506–D515. PubMed PMC
Walden, N. , Nguyen, T.‐P. , Mandáková, T. , Lysak, M.A. and Schranz, M.E. (2020) Genomic blocks in Aethionema arabicum support Arabideae as next diverging clade in Brassicaceae. Front. Plant Sci. 11, 10.3389/fpls.2020.00719. PubMed DOI PMC
Wang, Y. , Zhang, T. , Song, X. , Zhang, J. , Dang, Z. , Pei, X. and Long, Y. (2018) Identification and functional analysis of two alternatively spliced transcripts of ABSCISIC ACID INSENSITIVE3 (ABI3) in linseed flax (Linum usitatissimum L.). PLoS One, 13, e0191910. PubMed PMC
Wang, Y. , Zhou, L. , Yu, X. , Stover, E. , Luo, F. and Duan, Y. (2016) Transcriptome profiling of Huanglongbing (HLB) tolerant and susceptible citrus plants reveals the role of basal resistance in HLB tolerance. Front Plant Sci. 7, 933. PubMed PMC
Wilhelmsson, P.K.I. , Chandler, J.O. , Fernandez‐Pozo, N. et al . (2019) Usability of reference‐free transcriptome assemblies for detection of differential expression: a case study on Aethionema arabicum dimorphic seeds. BMC Genom. 20, 95. PubMed PMC
Wilhelmsson, P.K.I. , Muhlich, C. , Ullrich, K.K. and Rensing, S.A. (2017) Comprehensive genome‐wide classification reveals that many plant‐specific transcription factors evolved in streptophyte algae. Genome Biol. Evol. 9, 3384–3397. PubMed PMC
Wilkinson, M. , Lenton, J. and Holdsworth, M. (2005) Transcripts of Vp‐1 homoeologues are alternatively spliced within the Triticeae tribe. Euphytica, 143, 243–246.
Wu, T.D. and Watanabe, C.K. (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics, 21, 1859–1875. PubMed
Xu, J. , Wang, X.Y. and Guo, W.Z. (2015) The cytochrome P450 superfamily: key players in plant development and defense. J. Integr. Agr. 14, 1673–1686.
Yandell, M. and Ence, D. (2012) A beginner's guide to eukaryotic genome annotation. Nat. Rev. Genet. 13, 329–342. PubMed
Zhang, Q. , Zhang, X. , Wang, S. , Tan, C. , Zhou, G. and Li, C. (2016) Involvement of alternative splicing in barley seed germination. PLoS One, 11, e0152824. PubMed PMC
Zhang, R. , Calixto, C.P.G. , Marquez, Y. et al . (2017) A high quality Arabidopsis transcriptome for accurate transcript‐level analysis of alternative splicing. Nucleic Acids Res. 45, 5061–5073. PubMed PMC
Zhou, C. , Lin, Q. , Lan, J. et al . (2020) WRKY transcription factor OsWRKY29 represses seed dormancy in rice by weakening abscisic acid response. Front. Plant Sci. 11, 691. PubMed PMC
Aethionema arabicum dimorphic seed trait resetting during transition to seedlings