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Transcriptomics of nine-cis-epoxycarotenoid dioxygenase 6 induction in imbibed seeds reveals feedback mechanisms and long non-coding RNAs

Published online by Cambridge University Press:  11 September 2017

Khadidiatou Sall ,
David Hendrix ,
Taira Sekine ,
Yoshihiko Katsuragawa ,
Ryosuke Koyari  and
Hiroyuki Nonogaki
Khadidiatou Sall
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
David Hendrix
Affiliation:
Department of Biochemistry and Biophysics and School of Electrical Engineering and Computer Science, Oregon State University, Corvallis, OR 97331, USA
Taira Sekine
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
Yoshihiko Katsuragawa
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
Ryosuke Koyari
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
Hiroyuki Nonogaki*
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
*
*Correspondence Email: hiro.nonogaki@oregonstate.edu
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Abstract

Induction of nine-cis-epoxycarotenoid dioxygenase 6 (NCED6), an abscisic acid (ABA) biosynthesis gene, alone is sufficient to suspend germination in testa-ruptured seeds, which are at the final step of germination. Molecular consequences of NCED6 induction in imbibed seeds were investigated by RNA sequencing. The analysis identified many unknown and uncharacterized genes that were up-regulated by NCED6 induction, in addition to the major regulators of ABA signalling. Interestingly, other NCEDs were up-regulated by NCED6 induction, suggesting that the major rate-limiting enzymes in the ABA biosynthesis pathway are subject to positive-feedback regulation. ZEAXANTHIN EPOXIDASE and ABSCISIC ALDEHYDE OXIDASE3, which function upstream and downstream of NCED, were also up-regulated in seeds by NCED6 induction, which suggests that the distinct layers of positive feedback loops are coordinately operating in the NCED6-induced seeds. SOMNUS (SOM), which was also up-regulated by NCED6 induction, was the major mediator of enhanced ABA signalling in NCED6-induced seeds. SOM exerted negative effects on GA biosynthesis, which also contributes to a high ABA–GA ratio and reinforces the suppressive state of germination. Besides these coding genes, long intergenic non-coding RNAs (lincRNAs) were also up-regulated upon NCED6 induction (termed N6LINCRs). Conditional expression of N6LINCR1 altered gene expression profiles in seeds. Twenty-six genes were up-regulated and 66 genes were down-regulated by the induction of N6LINCR1. These results suggest that some of N6LINCRs have a regulatory role in gene expression in seeds, which potentially contributes to the regulation of germination by ABA.

Keywords

ABAArabidopsislong non-coding RNANCEDpositive feedback
Type
Research Papers
Information
Seed Science Research , Volume 27 , Issue 4 , December 2017 , pp. 251 - 261
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Copyright
Copyright © Cambridge University Press 2017 

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References

Alonso-Blanco, C., Bentsink, L., Hanhart, C.J., Blankestijn-de Vries, H. and Koornneef, M. (2003) Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana . Genetics 164, 711–729.Google Scholar
Barrero, J.M., Cavanagh, C., Verbyla, K.L., Tibbits, J.F.G., Verbyla, A.P., Huang, B.E., Rosewarne, G.M., Stephen, S., Wang, P., Whan, A., Rigault, P., Hayden, M.J. and Gubler, F. (2015) Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biology 16, 1–18.CrossRefGoogle Scholar
Bentsink, L., Jowett, J., Hanhart, C.J. and Koornneef, M. (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis . Proceedings of the National Academy of Sciences USA 103, 17042–17047.Google Scholar
Bentsink, L., Hanson, J., Hanhart, C.J., Blankestijn-de Vries, H., Coltrane, C., Keizer, P., El-Lithy, M., Alonso-Blanco, C., de Andres, M.T., Reymond, M., van Eeuwijk, F., Smeekens, S. and Koornneef, M. (2010) Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways. Proceedings of the National Academy of Sciences USA 107, 4264–4269.Google Scholar
Bewley, J.D., Bradford, K.J., Hilhorst, H.W.M. and Nonogaki, H. (2013) Seeds: Physiology of Development, Germination and Dormancy. New York, Springer.Google Scholar
Bhaskara, G.B., Nguyen, T.T. and Verslues, P.E. (2012) Unique drought resistance functions of the Highly ABA-Induced clade A protein phosphatase 2Cs. Plant Physiology 160, 379–395.Google Scholar
Bouyer, D., Roudier, F., Heese, M., Andersen, E.D., Gey, D., Nowack, M.K., Goodrich, J., Renou, J.P., Grini, P.E., Colot, V. and Schnittger, A. (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genetics 7, e1002014.Google Scholar
Buske, F.A., Bauer, D.C., Mattick, J.S. and Bailey, T.L. (2012) Triplexator: detecting nucleic acid triple helices in genomic and transcriptomic data. Genome Research 22, 1372–1381.Google Scholar
Cho, J.N., Ryu, J.Y., Jeong, Y.M., Park, J., Song, J.J., Amasino, R.M., Noh, B. and Noh, Y.S. (2012) Control of seed germination by light-induced histone arginine demethylation activity. Developmental Cell 22, 736–748.CrossRefGoogle ScholarPubMed
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana . The Plant Journal 16, 735–743.CrossRefGoogle Scholar
Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R. and Abrams, S.R. (2010) Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651–679.CrossRefGoogle ScholarPubMed
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. Proceedings of the National Academy of Sciences USA 113, E7846–7855.Google Scholar
Galupa, R. and Heard, E. (2015) X-chromosome inactivation: new insights into cis and trans regulation. Current Opinion in Genetics and Development 31, 57–66.CrossRefGoogle ScholarPubMed
Glazko, G.V., Zybailov, B.L. and Rogozin, I.B. (2012) Computational prediction of polycomb-associated long non-coding RNAs. PLoS One 7, e44878.Google Scholar
Gubler, F., Millar, A.A. and Jacobsen, J.V. (2005) Dormancy release, ABA and pre-harvest sprouting. Current Opinion in Plant Biology 8, 183–187.Google Scholar
Hansen, T.B., Jensen, T.I., Clausen, B.H., Bramsen, J.B., Finsen, B., Damgaard, C.K. and Kjems, J. (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495, 384–388.CrossRefGoogle ScholarPubMed
Jin, J., Liu, J., Wang, H., Wong, L. and Chua, N.H. (2013) PLncDB: plant long non-coding RNA database. Bioinformatics 29, 1068–1071.Google Scholar
Kim, D., Langmead, B. and Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12, 357–360.Google Scholar
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. and Salzberg, S.L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14, R36.Google Scholar
Kim, D.H., Yamaguchi, S., Lim, S., Oh, E., Park, J., Hanada, A., Kamiya, Y. and Choi, G. (2008) SOMNUS, a CCCH-Type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20, 1260–1277.Google Scholar
Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y. and Nambara, E. (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. The EMBO Journal 23, 1647–1656.Google Scholar
Langmead, B. and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357–359.Google Scholar
Lim, S., Park, J., Lee, N., Jeong, J., Toh, S., Watanabe, A., Kim, J., Kang, H., Kim, D.H., Kawakami, N. and Choi, G. (2013) ABA-INSENSITIVE3, ABA-INSENSITIVE5, and DELLAs interact to activate the expression of SOMNUS and other high-temperature-inducible genes in imbibed seeds in Arabidopsis . Plant Cell 25, 4863–4878.Google Scholar
Liu, J., Wang, H. and Chua, N.H. (2015) Long noncoding RNA transcriptome of plants. Plant Biotechnology Journal 13, 319–328.Google Scholar
Liu, Y., Koornneef, M. and Soppe, W.J. (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19, 433–444.Google Scholar
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. Proceedings of the National Academy of Sciences USA 108, 17225–17229.Google Scholar
Matsui, A., Ishida, J., Morosawa, T., Mochizuki, Y., Kaminuma, E., Endo, T.A., Okamoto, M., Nambara, E., Nakajima, M., Kawashima, M., Satou, M., Kim, J.M., Kobayashi, N., Toyoda, T., Shinozaki, K. and Seki, M. (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant and Cell Physiology 49, 1135–1149.Google Scholar
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 Genetics 11, e1005737.Google Scholar
Nakabayashi, K., Bartsch, M., Xiang, Y., Miatton, E., Pellengahr, S., Yano, R., Seo, M. and Soppe, W.J. (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. Plant Cell 24, 2826–2838.Google Scholar
Nakamura, S., Abe, F., Kawahigashi, H., Nakazono, K., Tagiri, A., Matsumoto, T., Utsugi, S., Ogawa, T., Handa, H., Ishida, H., Mori, M., Kawaura, K., Ogihara, Y. and Miura, H. (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23, 3215–3229.Google Scholar
Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., Maruyama, K., Yoshida, T., Ishiyama, K., Kobayashi, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant and Cell Physiology 50, 1345–1363.Google Scholar
Nee, G., Xiang, Y. and Soppe, W.J. (2016) The release of dormancy, a wake-up call for seeds to germinate. Current Opinion in Plant Biology 35, 8–14.Google Scholar
Nonogaki, H. (2014) Seed dormancy and germination – emerging mechanisms and new hypotheses. Frontiers in Plant Science 5, 233.Google Scholar
Nonogaki, M. and Nonogaki, H. (2017) Prevention of preharvest sprouting through hormone engineering and germination recovery by chemical biology. Frontiers in Plant Science 8, 90.Google Scholar
Nonogaki, M., Sall, K., Nambara, E. and Nonogaki, H. (2014) Amplification of ABA biosynthesis and signaling through a positive feedback mechanism in seeds. The Plant Journal 78, 527–539.Google Scholar
Okamoto, M., Tatematsu, K., Matsui, A., Morosawa, T., Ishida, J., Tanaka, M., Endo, T.A., Mochizuki, Y., Toyoda, T., Kamiya, Y., Shinozaki, K., Nambara, E. and Seki, M. (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. The Plant Journal 62, 39–51.Google Scholar
Park, J., Lee, N., Kim, W., Lim, S. and Choi, G. (2011) ABI3 and PIL5 collaboratively activate the expression of SOMNUS by directly binding to its promoter in imbibed Arabidopsis seeds. Plant Cell 23, 1404–1415.Google Scholar
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. Nature Biotechnology 33, 290–295.Google Scholar
Qin, F., Kodaira, K.S., Maruyama, K., Mizoi, J., Tran, L.S., Fujita, Y., Morimoto, K., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2011) SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiology 157, 1900–1913.Google Scholar
Richter, R., Behringer, C., Muller, I.K. and Schwechheimer, C. (2010) The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes and Development 24, 2093–2104.Google Scholar
Rizza, A., Boccaccini, A., Lopez-Vidriero, I., Costantino, P. and Vittorioso, P. (2011) Inactivation of the ELIP1 and ELIP2 genes affects Arabidopsis seed germination. New Phytologist 190, 896–905.Google Scholar
Simon, J.A. and Kingston, R.E. (2009) Mechanisms of Polycomb gene silencing: knowns and unknowns. Nature Review Molecular Cell Biology 10, 697–708.Google Scholar
Sugimoto, K., Takeuchi, Y., Ebana, K., Miyao, A., Hirochika, H., Hara, N., Ishiyama, K., Kobayashi, M., Ban, Y., Hattori, T. and Yano, M. (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proceedings of the National Academy of Sciences USA 107, 5792–5797.Google Scholar
Trapnell, C., Hendrickson, D.G., Sauvageau, M., Goff, L., Rinn, J.L. and Pachter, L. (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nature Biotechnology 31, 46–53.Google Scholar
Turner, M., Galloway, A. and Vigorito, E. (2014) Noncoding RNA and its associated proteins as regulatory elements of the immune system. Nature Immunology 15, 484–491.CrossRefGoogle ScholarPubMed
Visscher, A.M., Paul, A.L., Kirst, M., Guy, C.L., Schuerger, A.C. and Ferl, R.J. (2010) Growth performance and root transcriptome remodeling of Arabidopsis in response to Mars-like levels of magnesium sulfate. PLoS One 5, e12348.Google Scholar
Wang, Z., Cao, H., Sun, Y., Li, X., Chen, F., Carles, A., Li, Y., Ding, M., Zhang, C., Deng, X., Soppe, W.J. and Liu, Y.X. (2013) Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid-ethylene antagonism mediated by histone deacetylation. Plant Cell 25, 149–166.Google Scholar
Xi, W., Liu, C., Hou, X. and Yu, H. (2010) MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis . Plant Cell 22, 1733–1748.Google Scholar
Xiong, L., Lee, H., Ishitani, M. and Zhu, J.K. (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis . Journal of Biological Chemistry 277, 8588–8596.CrossRefGoogle ScholarPubMed
Yoo, S.Y., Kardailsky, I., Lee, J.S., Weigel, D. and Ahn, J.H. (2004) Acceleration of flowering by overexpression of MFT (MOTHER OF FT AND TFL1). Molecules and Cells 17, 95–101.Google Scholar
Zhao, J., Ohsumi, T.K., Kung, J.T., Ogawa, Y., Grau, D.J., Sarma, K., Song, J.J., Kingston, R.E., Borowsky, M. and Lee, J.T. (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Molecular Cell 40, 939–953.Google Scholar
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