Abstract
Photoperiod is the most important environmental cue for the regulation of flowering time, a highly important agronomic trait for crop productivity. To help elucidate the photoperiodic control of flowering in Brassicaceae, we performed microarray experiments using species-specific oligo-arrays with the long day (LD) plant Arabidopsis thaliana and the photoperiod-independent plant rapid cycling Brassica rapa (RCBr). Enrichment analysis of the gene ontologies of differentially expressed genes (DEGs) did not uncover clear differences in gene expression between photoperiod-dependent and -independent plants. Most genes that were up-regulated under LD conditions in Arabidopsis were also up-regulated in RCBr. In addition, most genes associated with light signaling and the circadian clock showed similar expression patterns between Arabidopsis and RCBr, implying that most components known to be key regulators in the photoperiodic flowering pathway are not responsible for the photoperiod independence of RCBr. Nonetheless, we identified one clock-associated gene, PSEUDO-RESPONSE REGULATOR9 (PRR9), as a candidate gene explaining the photoperiod independence of RCBr. The mechanism underlying the role of PRR9 in photoperiodic control and genomic polymorphisms should be further explored using different B. rapa species.
Similar content being viewed by others
References
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25:25–29
Bagheri H, El-Soda M, van Oorschot I, Hanhart C, Bonnema G, Jansen-van den Bosch T, Mank R, Keurentjes JJ, Meng L, Wu J, Koornneef M, Aarts MG (2012) Genetic analysis of morphological traits in a new, versatile, rapid-cycling Brassica rapa recombinant inbred line population. Front Plant Sci 3:183
Blée E, Boachon B, Burcklen M, Le Guédard M, Hanano A, Heintz D, Ehlting J, Herrfurth C, Feussner I, Bessoule JJ (2014) The reductase activity of the Arabidopsis caleosin RESPONSIVE TO DESSICATION 20 mediates gibberellin-dependent flowering time, abscisic acid sensitivity, and tolerance to oxidative stress. Plant Physiol 166:109–124
Dong X, Feng H, Xu M, Lee J, Kim YK, Lim YP, Piao Z, Park YD, Ma H, Hur Y (2013) Comprehensive analysis of genic male sterility-related genes in Brassica rapa using a newly developed Br300K oligomeric chip. PLoS ONE 8(9):e72178
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucl Acids Res 38:W64–W70
Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, De Bodt S, Vanden Bossche R, De Milde L, Yoshizumi T, Matsui M, Inzé D (2013) Ethylene Response Factor6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiol 162:319–332
Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722
Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249
Jiang B, Yue Y, Gao T, Ma L, Sun S, Wu C, Hou W, Lam HM, Han T (2013) GmFT2a polymorphism and maturity diversity in soybeans. PLoS ONE 8(10):e77474
Kakizaki T, Kato T, Fukino N, Ishida M, Hatakeyama K, Matsumoto S (2011) Identification of quantitative trait loci controlling late bolting in Chinese cabbage (Brassica rapa L.) parental like Nou 6 gou. Breed Sci 61:151–159
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M et al (2008) KEGG for linking genomes to life and the environment. Nucl Acids Res 36:D480–D484
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105
Kuno N, Møller SG, Shinomura T, Xu XM, Chua NH, Furuya M (2003) The novel MYB protein EARLY-PHYTOCHROME-RESPONSIVE1 is a component of a slave circadian oscillator in Arabidopsis. Plant cell 15:2476–2488
Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathway in Arabidopsis. Genes Dev 14:2366–2376
Lin K, Zhang N, Severing EI, Nijveen H, Cheng F, Visser RG, Wang X, de Ridder D, Bonnema G (2014) Beyond genomic variation–comparison and functional annotation of three Brassica rapa genomes: a turnip, a rapid cycling and a Chinese cabbage. BMC Genomics 15:250
Lou P, Zhao J, Kim JS, Shen S, Carpio DPD, Song X, Jin M, Vreugdenhil D, Wang X, Koornneef M, Bonnema G (2007) Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. J Exp Bot 58:4005–4016
Lou P, Xie Q, Xu X, Edwards CE, Brock MT, Weinig C, McClung CR (2011) Genetic architecture of the circadian clock and flowering time in Brassica rapa. Theor Appl Genet 123:397–409
Marrocco K, Zhou Y, Dieterle M, Funk M, Genschik P, Krenz M, Stolpe T, Kretsch T (2006) Functional analysis of EID1, an F-box protein involved in phytochrome A-dependent light signal transduction. Plant J 45:423–438
Mizuno T, Kitayama M, Takayama C, Yamashino T (2015) Insight into a physiological role for the EC night-time repressor in the Arabidopsis circadian clock. Plant Cell Physiol 56:1738–1747
Musgrave ME (2000) Realizing the potential of rapid-cycling Brassica as a model system for use in plant biology research. J Plant Growth Regul 19:314–325
Nakamichi N, Kita M, Niimura K, Ito S, Yamashino T, Mizoguch T, Mizuno T (2007) Arabidopsis clock-associated pseudoresponse regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol 48:822–832
Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285:1579–1582
Rugnone ML, Soverna AF, Sanchez SE, Schlaen RG, Hernando CE, Seymour DK, Mancini E, Chernomoretz A, Weigel D, Más P, Yanovsky MJ (2013) LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proc Natl Acad Sci 110:12120–12125
Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195
Seki M, Chono M, Matsunaka H, Fujita M, Oda S, Kubo K, Kiribuchi-Otobe C, Kojima H, Nishida H, Kato K (2011) Distribution of photoperiod-insensitive alleles Ppd-B1a and Ppd-D1a and their effect on heading time in Japanese wheat cultivars. Breed Sci 61:405–412
Seki M, Chono M, Nishimura T, Sato M, Yoshimura Y, Matsunaka H, Fujita M, Oda S, Kubo K, Kiribuchi-Otobe C, Kojima H, Nishida H, Kato K (2013) Distribution of photoperiod-insensitive allele Ppd-A1a and its effect on heading time in Japanese wheat cultivars. Breed Sci 63:309–316
Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453
Song YH, Ito S, Imaizumi T (2013) Flowering time regulation: photoperiod- and temperature sensing in leaves. Trends Plant Sci 18:575–583
Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464
Song H, Dong X, Yi H, Nou IS, Hur Y (2016) Differential expression of flowering genes between rapid- and slow-cycling Brassica rapa. Plant Breed Biotechnol 4:145–157
Sun H, Guo Z, Gao L, Zhao G, Zhang W, Zhou R, Wu Y, Wang H, An H, Jia J (2014) DNA methylation pattern of Photoperiod-B1 is associated with photoperiod insensitivity in wheat (Triticum aestivum). New Phytol 204:682–692
Tsubokura Y, Watanabe S, Xia Z, Kanamori H, Yamagata H, Kaga A, Katayose Y, Abe J, Ishimoto M, Harada K (2014) Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann Bot 113:429–441
Turner AS, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034
Vallee RB, McKenney RJ, Ori-McKenney KM (2012) Multiple modes of cytoplasmic dynein regulation. Nat Cell Biol 14:224–230
Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006
Weis AE (2015) Inheritance of rapid cycling in Brassica rapa fast plants: dominance that increases with photoperiod. Int J Plant Sci 176:859–868
Williams PH, Hill GM (1986) Rapid-cycling populations of brassica. Science 232:1385–1389
Xing H, Wang P, Cui X, Zhang C, Wang L, Liu X, Yuan L, Li Y, Xie Q, Xu X (2015) LNK1 and LNK2 recruitment to the evening element require morning expressed circadian related MYB-like transcription factors. Plant Signal Behav 10(3):e1010888
Xu M, Xu Z, Liu B, Kong F, Tsubokura Y, Watanabe S, Xia Z, Harada K, Kanazawa A, Yamada T, Abe J (2013) Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biol 13:91
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2484
Zhang F, Yao J, Ke J, Zhang L, Lam VQ, Xin XF, Zhou XE, Chen J, Brunzelle J, Griffin PR, Zhou M, Xu HE, Melcher K, He SY (2015) Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 525(7568):269–273
Zheng ZL, Yang Z, Jang JC, Metzger JD (2006) Phytochromes A1 and B1 have distinct functions in the photoperiodic control of flowering in the obligate long-day plant Nicotiana sylvestris. Plant Cell Environ 29:1673–1685
Acknowledgements
This work was supported by Research Fund of Chungnam National University (CNU), Daejeon, Korea, to Yoonkang Hur (2015-1115-01) and by research grants from Golden Seed Project (Center for Horticultural Seed Development, 213003-04-4-SB230), Ministry of Agriculture, Food and Rural Affairs (MAFRA), Ministry of Oceans and Fisheries (MOF), and Rural Development Administration (RDA).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Hayoung Song, Hankuil Yi, Ching-Tack Han, Ill-Sup Nou and Yoonkang Hur declares no conflict of interest.
Studies with human or animal research
This article does not contain any studies with human subjects or animals performed by any of the authors.
Additional information
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Song, H., Yi, H., Do, C. et al. Genome-wide analysis of gene expression to distinguish photoperiod-dependent and -independent flowering in Brassicaceae. Genes Genom 39, 207–223 (2017). https://doi.org/10.1007/s13258-016-0487-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-016-0487-2