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Aethionema Arabicum Genome Annotation Using Pacbio Full‐Length

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Aethionema Arabicum Genome Annotation Using Pacbio Full‐Length The Plant Journal (2021) doi: 10.1111/tpj.15161 RESOURCE Aethionema arabicum genome annotation using PacBio full-length transcripts provides a valuable resource for seed dormancy and Brassicaceae evolution research Noe Fernandez-Pozo1,* , Timo Metz1 , Jake O. Chandler2 , Lydia Gramzow3 , Zsuzsanna Merai 4 , Florian Maumus5 , Ortrun Mittelsten Scheid4 ,Gunter€ Theißen3 , M. Eric Schranz6 , Gerhard Leubner-Metzger2,7 and Stefan A. Rensing1,8,9,* 1Plant Cell Biology, Department of Biology, University of Marburg, Marburg, Germany, 2School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, UK, 3Matthias Schleiden Institute/Genetics, Friedrich Schiller University Jena, Jena, Germany, 4Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria, 5Universite Paris-Saclay, INRAE, URGI, Versailles 78026, France, 6Biosystematics Group, Wageningen University, Wageningen, The Netherlands, 7Laboratory of Growth Regulators, Centre of the Region Hana for Biotechnological and Agricultural Research, Palacky University and Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Olomouc, Czech Republic, 8BIOSS Centre for Biological Signaling Studies, University of Freiburg, Freiburg, Germany, and 9LOEWE Center for Synthetic Microbiology (SYNMIKRO), University of Marburg, Marburg, Germany Received 13 October 2020; revised 31 December 2020; accepted 8 January 2021. *For correspondence (e-mail [email protected]; [email protected]). SUMMARY Aethionema arabicum is an important model plant for Brassicaceae trait evolution, particularly of seed (development, regulation, germination, dormancy) and fruit (development, dehiscence mechanisms) charac- ters. 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 par- tially explained by loss of homeologs derived from the At-a polyploidization event and by a lower occur- rence 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-b 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). Keywords: Aethionema arabicum, genome annotation, seed germination, Brassicaceae evolution, alterna- tive splicing, transcription factors, Iso-seq. INTRODUCTION heteromorphism. It produces two types of fruits, a bigger The Brassicaceae species Aethionema arabicum has and dehiscent one that produces two to six mucilaginous become an important model system for unraveling the seeds (M+) and an indehiscent one, which only contains control and development of seed and fruit traits because it one non-mucilaginous seed (M-) (Lenser et al., 2016). This displays an unusual phenomenon, diaspore (fruit/seed) allows alternative strategies for dispersion of the seeds © 2021 The Authors. 1 The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 2 Fernandez-Pozo et al. and timing of germination depending on the environmental pipelines based on transcript and protein evidence, conditions. M+ seeds may stick to the substrate and followed by optional manual curation using a genome remain close to the mother plant, while M- seeds, inside browser to polish the results that automatic annotation an indehiscent fruit with wings, may be dispersed across cannot resolve (Yandell and Ence, 2012). Alternative meth- longer distances by wind or water currents (Arshad et al., ods are sometimes used to migrate previous gene versions 2019). Moreover, Ae. arabicum shows plasticity for the pro- to new genome versions using lift-over tools (Keilwagen portion of the two fruit types depending on environmental et al., 2016; Pracana et al., 2017). In most cases, genome responses such as temperature and nutritional or her- annotation is based on short-read assemblies recon- bivory stress (Lenser et al., 2016; Bhattacharya et al., structed using transcript assemblers (Grabherr et al., 2011; 2019a,b). Therefore, Ae. arabicum is an excellent model to Pertea et al., 2015). However, most of the multi-exon genes study seed development, regulation, germination, dor- have been observed to be alternatively spliced in plants mancy and fruit dehiscence mechanisms (Mohammadin and animals (Zhang et al., 2017; Hardwick et al., 2019), and et al., 2017; Lenser et al., 2018; Arshad et al., 2019; Merai often short reads cannot cover the full length of tran- et al., 2019; Bhattacharya et al., 2019b). Additionally, multi- scripts, which makes it hard to reconstruct the correct com- ple resources and studies are available for two ecotypes of bination of exons of alternative isoforms in silico Ae. arabicum, from Turkey (TUR) or Cyprus (CYP) (Moham- (Hardwick et al., 2019). Alternative splicing (AS) produces madin et al., 2018; Merai et al., 2019; Nguyen et al., 2019), multiple transcripts that may yield different proteins from adapted to different environmental conditions (Bhat- the same gene. Additionally, AS can lead to different tacharya et al., 2019b) and differently reacting to stresses untranslated regions (UTRs), which might be important for and environmental stimuli, such as in response to light post-transcriptional regulation and may affect mRNA trans- during germination (Merai et al., 2019). port, stability, translation efficiency and subcellular local- Aethionema arabicum is a member of the tribe Aethio- ization (Grillo et al., 2010; Kelemen et al., 2013). nema, sister group to all other ‘crown group’ Brassicaceae Interestingly, it has been observed that AS might play an species. The crown group includes many plants of agricul- important role in seed germination (Zhang et al., 2016; tural interest such as cabbage (Brassica oleracea), rape- Narsai et al., 2017), involving key genes such as DELAY OF seed (Brassica napus) and mustard (Brassica rapa), as well GERMINATION 1 (DOG1), which affects seed dormancy as the model plant Arabidopsis thaliana (Nikolov et al., (Nakabayashi et al., 2015). 2019). Brassicaceae species, including Ae. arabicum, went Recently, version 3 (V3) of the Ae. arabicum genome of through five ancient polyploidization events in their evolu- the TUR ecotype was assembled and organized in 11 link- tionary history: near the origin of seed plants (At-f), in age groups (based on a linkage map derived from crossing flowering plants (At-e), in eudicots (ancient hexaploidy, At- the TUR ecotype with the CYP ecotype) and 2872 unor- c) and in part of the Brassicales including the sister group dered scaffolds (Nguyen et al., 2019), with 65.5% of the of Brassicaceae (Cleomaceae) (At-b), and importantly, all genome sequence covered by the linkage groups. This Brassicaceae species including Ae. arabicum share the At-a genome version did not predict gene models de novo, but whole genome duplication (WGD) (Schranz et al., 2012; lifted over the gene models from v2.5, which were lifted Cheng et al., 2013; Walden et al., 2020). Due to its phyloge- before from v1.0. This process caused formatting inconsis- netically important position and shared WGD history, Ae. tencies and gene structure annotation errors such as incor- arabicum greatly facilitates evolutionary, comparative rect stop codons, incomplete genes, missing features and genomic and gene family phylogenetic analyses to under- frameshifts, which were carried over from annotation v1.0 stand genome and trait evolution of crucifers (Schranz through v2.5 to v3.0. Here, we present the gene model et al., 2012; Nguyen et al., 2019; Walden et al., 2020). Addi- annotation v3.1 for Ae. arabicum, based on the genome tionally, Brassicaceae produce glucosinolates, secondary assembly V3 and predicting the gene model structure de metabolites involved in plant defense against biotic and novo, using MAKER (Campbell et al., 2014). In total, 294 abiotic stresses (Del Carmen Martinez-Ballesta et al., 2013; Illumina RNA-seq samples from multiple tissues and Pac- Bhattacharya et al., 2019a), which is another interesting Bio full-length transcript sequences of seeds and leaves of trait also present in Ae. arabicum (Mohammadin et al., the ecotypes TUR and CYP were used, capturing full-length 2017; Mohammadin et al., 2018; Bhattacharya et al., isoform sequences and UTRs that were used to improve 2019a). the genome annotation of this model plant. Genome annotation can be addressed using different strategies, with increasing accuracy depending on the time RESULTS AND DISCUSSION and effort invested and the quality of the evidence support- Annotation workflow overview
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