TEAseq-based identification of 35,696 <i>Dissociation</i> insertional mutations facilitates functional genomic studies in maize

Mingjie Lyu; Huafeng Liu; Joram Kiriga Waititu; Ying Sun; Huan Wang; Junjie Fu; Yanhui Chen; Jun Liu; Lixia Ku; Xiliu Cheng

doi:10.1016/j.jgg.2021.07.010

Volume 48 Issue 11

Nov. 2021

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Article Navigation > Journal of Genetics and Genomics > 2021 > 48(11): 961-971

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TEAseq-based identification of 35,696 Dissociation insertional mutations facilitates functional genomic studies in maize

doi: 10.1016/j.jgg.2021.07.010

a Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China;
b College of Agronomy, Collaborative Innovation Center of Henan Grain Crops and National Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, Henan 450002, China;
c Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China

Funds:

We thank Ms. Lina Zhang from the Core Facility Platform, Institute of Crop Sciences, Chinese Academy of Agriculture Sciences (CAAS), for managing the high-throughput genomic DNA extraction appliances. This work was supported by grants from the Ministry of Science and Technology of China (2016YFD0101000 and 2016YFD0101001) and the Natural Science Foundation of China (31901595).

Received Date: 2021-04-20
Accepted Date: 2021-07-17
Rev Recd Date: 2021-07-11
Publish Date: 2021-11-20

Abstract

Abstract

In plants, transposable element (TE)-triggered mutants are important resources for functional genomic studies. However, conventional approaches for genome-wide identification of TE insertion sites are costly and laborious. This study developed a novel, rapid, and high-throughput TE insertion site identification workflow based on next-generation sequencing and named it Transposable Element Amplicon Sequencing (TEAseq). Using TEAseq, we systemically profiled the Dissociation (Ds) insertion sites in 1606 independent Ds insertional mutants in advanced backcross generation using K17 as background. The Ac-containing individuals were excluded for getting rid of the potential somatic insertions. We characterized 35,696 germinal Ds insertions tagging 10,323 genes, representing approximately 23.3% of the total genes in the maize genome. The insertion sites were presented in chromosomal hotspots around the ancestral Ds loci, and insertions occurred preferentially in gene body regions. Furthermore, we mapped a loss-of-function AGL2 gene using bulked segregant RNA-sequencing assay and proved that AGL2 is essential for seed development. We additionally established an open-access database named MEILAM for easy access to Ds insertional mutations. Overall, our results have provided an efficient workflow for TE insertion identification and rich sequence-indexed mutant resources for maize functional genomic studies.
- Maize,
- Zea mays,
- Insertion identification,
- Ds transposon,
- Mutant library,
- Next-generation sequencing,
- Functional genomics

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References(46)

References

Andrews, S., 2010. FastQC:a quality control tool for high throughput sequence data. Babraham Bioinformatics. Babraham Institute, Cambridge, United Kingdom.

Carpentier, M.-C., Manfroi, E., Wei, F.-J., Wu, H.-P., Lasserre, E., Llauro, C., Debladis, E., Akakpo, R., Hsing, Y.-I., Panaud, O., 2019. Retrotranspositional landscape of Asian rice revealed by 3000 genomes. Nat. Commun. 10, 1-12.

Cermak, T., Doyle, E.L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J.A., Somia, N.V., Bogdanove, A.J., Voytas, D.F., 2011. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82.

Cheng, W.-H., Taliercio, E.W., Chourey, P.S., 1999. Sugars modulate an unusual mode of control of the cell-wall invertase gene (Incw1) through its 30' untranslated region in a cell suspension culture of maize. Proc. Natl. Acad. Sci. U. S. A. 96, 10512-10517.

Chin, H.G., Choe, M.S., Lee, S.H., Park, S.H., Park, S.H., Koo, J.C., Kim, N.Y., Lee, J.J., Oh, B.G., Yi, G.H., 1999. Molecular analysis of rice plants harboring an Ac/Ds transposable element-mediated gene trapping system. Plant J. 19, 615-623.

Cowperthwaite, M., Park, W., Xu, Z., Yan, X., Maurais, S.C., Dooner, H.K., 2002. Use of the transposon Ac as a gene-searching engine in the maize genome. Plant Cell 14, 713-726.

Doebley, J., Stec, A., Gustus, C., 1995. Teosinte branched1 and the origin of maize:evidence for epistasis and the evolution of dominance. Genetics 141, 333-346.

Doebley, J., Stec, A., Hubbard, L., 1997. The evolution of apical dominance in maize. Nature 386, 485-488.

Du, C., Hoffman, A., He, L., Caronna, J., Dooner, H.K., 2011. The complete Ac/Ds transposon family of maize. BMC Genom. 12, 1-12.

Fujimoto, S., Matsunaga, S., Murata, M., 2016. Mapping of T-DNA and Ac/Ds by TAIL-PCR to analyze chromosomal rearrangements. In:Murata, M. (Ed.), Chromosome and Genomic Engineering in Plants. Springer, NewYork, pp. 207-216.

Ito, T., Motohashi, R., Kuromori, T., Noutoshi, Y., Seki, M., Kamiya, A., Mizukado, S., Sakurai, T., Shinozaki, K., 2005. A resource of 5,814 dissociation transposontagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant Cell Physiol. 46, 1149-1153.

Kim, D., Langmead, B., Salzberg, S.L., 2015. HISAT:a fast spliced aligner with low memory requirements. Nat. Methods 12, 357-360.

Kolesnik, T., Szeverenyi, I., Bachmann, D., Kumar, C.S., Jiang, S., Ramamoorthy, R., Cai, M., Ma, Z.G., Sundaresan, V., Ramachandran, S., 2004. Establishing an efficient Ac/Ds tagging system in rice, large-scale analysis of Ds flanking sequences. Plant J. 37, 301-314.

Kunze, R., Weil, C.F., 2002. The hAT and CACTA superfamilies of plant transposons. In:Mobile DNA II. American Society for Microbiology (ASM), pp. 565-610.

Kuromori, T., Hirayama, T., Kiyosue, Y., Takabe, H., Mizukado, S., Sakurai, T., Akiyama, K., Kamiya, A., Ito, T., Shinozaki, K., 2004. A collection of 11800 singlecopy Ds transposon insertion lines in Arabidopsis. Plant J. 37, 897-905.

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

Levin, H.L., Moran, J.V., 2011. Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615-627.

Li, G.T., Jain, R., Chern, M., Pham, N.T., Martin, J.A., Wei, T., Schackwitz, W.S., Lipzen, A.M., Duong, P.Q., Jones, K.C., et al., 2017. The sequences of 1504 mutants in the model rice variety kitaake facilitate rapid functional genomic studies. Plant Cell 29, 1218-1231.

Li, X., Song, Y., Century, K., Straight, S., Ronald, P., Dong, X., Lassner, M., Zhang, Y., 2001. A fast neutron deletion mutagenesis-based reverse genetics system for plants. Plant J. 27, 235-242.

Liang, L., Zhou, L., Tang, Y., Li, N., Song, T., Shao, W., Zhang, Z., Cai, P., Feng, F., Ma, Y., et al., 2019. A sequence-indexed Mutator insertional library for maize functional genomics study. Plant Physiol. 181, 1404-1414.

Liao, G.-C., Rehm, E.J., Rubin, G.M., 2000. Insertion site preferences of the P transposable element in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 97, 3347-3351.

Liu, S., Yeh, C.-T., Ji, T., Ying, K., Wu, H., Tang, H.M., Fu, Y., Nettleton, D., Schnable, P.S., 2009. Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet. 5, e1000733.

Loveless, A., 1958. Increased rate of plaque-type and host-range mutation following treatment of bacteriophage in vitro with ethyl methane sulphonate. Nature 181, 1212-1213.

Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M., 2013. RNA-guided human genome engineering via Cas9. Science 339, 823-826.

Mansfeld, B.N., Grumet, R., 2018. QTLseqr:an R package for bulk segregant analysis with next-generation sequencing. Plant Genome 11, 180006.

Marcon, C., Altrogge, L., Win, Y.N., Stoecker, T., Gardiner, J.M., Portwood, J.L., II, Opitz, N., Kortz, A., Baldauf, J.A., Hunter, C.T., et al., 2020. BonnMu:a sequenceindexed resource of transposon-induced maize mutations for functional genomics studies. Plant Physiol. 184, 620-631.

McCarty, D.R., Latshaw, S., Wu, S., Suzuki, M., Hunter, C.T., Avigne, W.T., Koch, K.E., 2013. Mu-seq:sequence-based mapping and identification of transposon induced mutations. PLoS One 8, e77172.

McCarty, D.R., Mark Settles, A., Suzuki, M., Tan, B.C., Latshaw, S., Porch, T., Robin, K., Baier, J., Avigne, W., Lai, J., et al., 2005. Steady-state transposon mutagenesis in inbred maize. Plant J. 44, 52-61.

McClintock, B., 1951. Chromosome organization and genic expression. Cold Spring Harbor Symp. Quant. Biol. 16, 13-47.

McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., 2010. The Genome Analysis Toolkit:a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.

Miyao, A., Iwasaki, Y., Kitano, H., Itoh, J.-I., Maekawa, M., Murata, K., Yatou, O., Nagato, Y., Hirochika, H., 2007. A large-scale collection of phenotypic data describing an insertional mutant population to facilitate functional analysis of rice genes. Plant Mol. Biol. 63, 625-635.

Pertea, M., Pertea, G.M., Antonescu, C.M., Chang, T.-C., Mendell, J.T., Salzberg, S.L., 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290-295.

Piffanelli, P., Droc, G., Mieulet, D., Lanau, N., Bès, M., Bourgeois, E., Rouvière, C., Gavory, F., Cruaud, C., Ghesquière, A., 2007. Large-scale characterization of Tos17 insertion sites in a rice T-DNA mutant library. Plant Mol. Biol. 65, 587-601.

Sabot, F., 2014. Tos17 rice element:incomplete but effective. Mobile DNA 5, 1-4.

Schmidt, R.J., Veit, B., Mandel, M.A., Mena, M., Hake, S., Yanofsky, M.F., 1993. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5, 729-737.

Stanford, W.L., Cohn, J.B., Cordes, S.P., 2001. Gene-trap mutagenesis:past, present and beyond. Nat. Rev. Genet. 2, 756-768.

Tang, G.-Q., Lüscher, M., Sturm, A., 1999. Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11, 177-189.

Uren, A.G., Mikkers, H., Kool, J., Van Der Weyden, L., Lund, A.H., Wilson, C.H., Rance, R., Jonkers, J., Van Lohuizen, M., Berns, A., 2009. A high-throughput splinkerette-PCR method for the isolation and sequencing of retroviral insertion sites. Nat. Protoc. 4, 789-798.

Vollbrecht, E., Duvick, J., Schares, J.P., Ahern, K.R., Deewatthanawong, P., Xu, L., Conrad, L.J., Kikuchi, K., Kubinec, T.A., Hall, B.D., 2010. Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell 22, 1667-1685.

Wang, D., Peterson, T., 2013. Isolation of sequences flanking Ac insertion sites by Ac casting. In:Peterson, T. (Ed.), Plant Transposable Elements. Springer, New York, pp. 117-122.

Wang, Q., Dooner, H.K., 2006. Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc. Natl. Acad. Sci. U. S. A. 103, 17644-17649.

Williams-Carrier, R., Stiffler, N., Belcher, S., Kroeger, T., Stern, D.B., Monde, R.A., Coalter, R., Barkan, A., 2010. Use of Illumina sequencing to identify transposon insertions underlying mutant phenotypes in high-copy Mutator lines of maize. Plant J. 63, 167-177.

Xiong, W., He, L., Li, Y., Dooner, H.K., Du, C., 2013. InsertionMapper:a pipeline tool for the identification of targeted sequences from multidimensional high throughput sequencing data. BMC Genom. 14, 1-7.

Yadav, N., Postle, K., Saiki, R., Thomashow, M., Chilton, M.-D., 1980. T-DNA of a crown gall teratoma is covalently joined to host plant DNA. Nature 287, 458-461.

Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A., Meyerowitz, E.M., 1990. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35-39.

Zhang, J., Yu, C., Pulletikurti, V., Lamb, J., Danilova, T., Weber, D.F., Birchler, J., Peterson, T., 2009. Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize. Genes Dev. 23, 755-765.

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