INVITED REVIEWS

Deciphering the Underlying Mechanism of the Plant Circadian System and Its Regulation on Plant Growth and Development

Expand
  • 1Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
    2University of Chinese Academy of Sciences, Beijing 100049, China
    3School of Life Sciences, Guangzhou University, Guangzhou 510006, China
† These authors contributed equally to this paper

Received date: 2017-11-28

  Accepted date: 2018-02-09

  Online published: 2018-09-11

Abstract

The plant circadian system mostly includes input pathways, a core oscillator and output pathways to sense and anticipate the timing cues of the environment to optimize plant growth and fitness. As the cellular core coordinating system, the plant circadian system can sense the daily recurring light and temperature dynamics to coordinate the metabolism and multiple physiology processes, providing an adaptive advantage for plant growth and development. The core circadian oscillator regulates multiple complex downstream networks at various levels. Here, we summarize recent major research progress in deciphering the underlying mechanisms of the core oscillator and its regulatory networks. We also highlight a few fundamental questions needing to be resolved.

Cite this article

Wei Hua, Wang Yan, Liu Baohui, Wang Lei . Deciphering the Underlying Mechanism of the Plant Circadian System and Its Regulation on Plant Growth and Development[J]. Chinese Bulletin of Botany, 2018 , 53(4) : 456 -467 . DOI: 10.11983/CBB17226

References

1 徐江民, 姜洪真, 林晗, 黄苗苗, 符巧丽, 曾大力, 饶玉春 (2016). 水稻ES1参与生物钟基因表达调控以及逆境胁迫响应. 植物学报 51, 743-756.
2 Adams S, Manfield I, Stockley P, Carré IA (2015). Revised morning loops of the Arabidopsis circadian clock based on analyses of direct regulatory interactions.PLoS One 10, e0143943.
3 Alabadı? D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001). Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880-883.
4 Atamian HS, Harmer SL (2016). Circadian regulation of hormone signaling and plant physiology.Plant Mol Biol 91, 691-702.
5 Bhardwaj V, Meier S, Petersen LN, Ingle RA, Roden LC (2011). Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLoS One 6, e26968.
6 Boden SA, Weiss D, Ross JJ, Davies NW, Trevaskis B, Chandler PM, Swain SM (2014). EARLY FLOWERING 3 regulates flowering in spring barley by mediating gibberellin production and FLOWERING LOCUS T expression. Plant Cell 26, 1557-1569.
7 Cha JY, Kim J, Kim TS, Zeng QN, Wang L, Lee SY, Kim WY, Somers DE (2017). GIGANTEA is a co-chaperone which facilitates maturation of ZEITLUPE in the Arabidopsis circadian clock.Nat Commun 8, 3.
8 Chew YH, Halliday KJ (2011). A stress-free walk from Arabidopsis to crops.Curr Opin Biotechnol 22, 281-286.
9 Chow BY, Sanchez SE, Breton G, Pruneda-Paz JL, Krogan NT, Kay SA (2014). Transcriptional regulation of LUX by CBF1 mediates cold input to the circadian clock in Ara- bidopsis. Curr Biol 24, 1518-1524.
10 Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development.Genome Biol 9, R130.
11 Ford B, Deng WW, Clausen J, Oliver S, Boden S, Hemming M, Trevaskis B (2016). Barley (Hordeum vulgare) circadian clock genes can respond rapidly to temperature in an EARLY FLOWERING 3-dependent manner. J Exp Bot 67, 5517-5528.
12 Fowler SG, Cook D, Thomashow MF (2005). Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137, 961-968.
13 Gao H, Jin MN, Zheng XM, Chen J, Yuan DY, Xin YY, Wang MQ, Huang DY, Zhang Z, Zhou KN, Sheng PK, Ma J, Ma WW, Deng HF, Jiang L, Liu SJ, Wang HY, Wu CY, Yuan LP, Wan JM (2014). Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci USA 111, 16337-16342.
14 Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012). Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor.Proc Natl Acad Sci USA 109, 3167-3172.
15 Greenham K, McClung CR (2015). Integrating circadian dynamics with physiological processes in plants.Nat Rev Genet 16, 598-610.
16 Grundy J, Stoker C, Carré IA (2015). Circadian regulation of abiotic stress tolerance in plants.Front Plant Sci 6, 648.
17 Harmer SL (2009). The circadian system in higher plants.Annu Rev Plant Biol 60, 357-377.
18 Hayama R, Sarid-Krebs L, Richter R, Fernández V, Jang S, Coupland G (2017). PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length.EMBO J 36, 904-918.
19 Huang W, Peréz-García P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012). Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator.Science 336, 75-79.
20 Izawa T, Mihara M, Suzuki Y, Gupta M, Itoh H, Nagano AJ, Motoyama R, Sawada Y, Yano M, Hirai MY, Makino A, Nagamura Y (2011). Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23, 1741-1755.
21 Kamioka M, Takao S, Suzuki T, Taki K, Higashiyama T, Kinoshita T, Nakamichi N (2016). Direct repression of evening genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis circadian clock. Plant Cell 28, 696-711.
22 Keily J, MacGregor DR, Smith RW, Millar AJ, Halliday KJ, Penfield S (2013). Model selection reveals control of cold signaling by evening-phased components of the plant circadian clock.Plant J 76, 247-257.
23 Kim WY, Ali Z, Park HJ, Park SJ, Cha JY, Perez- Hormaeche J, Quintero FJ, Shin G, Kim MR, Qiang Z, Ning L, Park HC, Lee SY, Bressan RA, Pardo JM, Bohnert HJ, Yun DJ (2013). Release of SOS2 kinase from sequestration with GIGANTEA determines salt tole- rance in Arabidopsis.Nat Commun 4, 1352.
24 Ko DK, Rohozinski D, Song QX, Taylor SH, Juenger TE, Harmon FG, Chen ZJ (2016). Temporal shift of circa- dian-mediated gene expression and carbon fixation contributes to biomass heterosis in maize hybrids.PLoS Genet 12, e1006197.
25 Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999). A pair of related genes with antagonistic roles in mediating flowering signals.Science 286, 1960-1962.
26 Kolmos E, Chow BY, Pruneda-Paz JL, Kay SA (2014). HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock. Proc Natl Acad Sci USA 111, 16172-16177.
27 Koo BH, Yoo SC, Park JW, Kwon CT, Lee BD, An G, Zhang ZY, Li JJ, Li ZC, Paek NC (2013). Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant 6, 1877-1888.
28 Korneli C, Danisman S, Staiger D (2014). Differential control of pre-invasive and post-invasive antibacterial defense by the Arabidopsis circadian clock.Plant Cell Physiol 55, 1613-1622.
29 Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress.Plant Physiol 130, 2129-2141.
30 Lee YS, Yi J, An G (2016). OsPhyA modulates rice flowering time mainly through OsGI under short days and Ghd7 under long days in the absence of phytochrome B. Plant Mol Biol 91, 413-427.
31 Li F, Zhang XM, Hu RB, Wu FQ, Ma JH, Meng Y, Fu YF (2013). Identification and molecular characterization of FKF1 and GI homologous genes in soybean. PLoS One 8, e79036.
32 Li S, Yue WH, Wang M, Qiu WM, Zhou L, Shou HX (2016a). Mutation of OsGIGANTEA leads to enhanced tolerance to polyethylene glycol-generated osmotic stress in rice. Front Plant Sci 7, 465.
33 Li X, Ma DB, Lu SX, Hu XY, Huang RF, Liang T, Xu TD, Tobin EM, Liu HT (2016b). Blue light- and low temperature-regulated COR27 and COR28 play roles in the Ara- bidopsis circadian clock.Plant Cell 28, 2755-2769.
34 Liu C, Song GY, Zhou YH, Qu XF, Guo ZB, Liu ZW, Jiang DM, Yang DC (2015). OsPRR37 and Ghd7 are the major genes for general combining ability of DTH, PH and SPP in rice. Sci Rep 5, 12803.
35 Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.Plant Cell 10, 1391-1406.
36 Liu T, Carlsson J, Takeuchi T, Newton L, Farré EM (2013). Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7.Plant J 76, 101-114.
37 Lu SJ, Zhao XH, Hu YL, Liu SL, Nan HY, Li XM, Fang C, Cao D, Shi XY, Kong LP, Su T, Zhang FG, Li SC, Wang Z, Yuan XH, Cober ER, Weller JL, Liu BH, Hou XL, Tian ZX, Kong FJ (2017). Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet 49, 773-779.
38 Matsubara K, Ogiso-Tanaka E, Hori K, Ebana K, Ando T, Yano M (2012). Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol 53, 709-716.
39 Millar AJ, Carre IA, Strayer CA, Chua NH, Kay SA (1995). Circadian clock mutants in Arabidopsis identified by luci- ferase imaging.Science 267, 1161-1163.
40 Nagel DH, Pruneda-Paz JL, Kay SA (2014). FBH1 affects warm temperature responses in the Arabidopsis circadian clock.Proc Natl Acad Sci USA 111, 14595-14600.
41 Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010). PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock.Plant Cell 22, 594-605.
42 Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T (2012). Transcriptional repressor PRR5 directly regulates clock-output pathways.Proc Natl Acad Sci USA 109, 17123-17128.
43 Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009). Transcript profiling of an Arabidopsis PSEUDO RES- PONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50, 447-462.
44 Nieto C, López-Salmerón V, Davière JM, Prat S (2015). ELF3-PIF4 interaction regulates plant growth independently of the evening complex.Curr Biol 25, 187-193.
45 Ning YS, Shi XT, Wan RY, Fan JB, Park CH, Zhang CY, Zhang T, Ouyang XH, Li SG, Wang GL (2015). OsELF3- 2, an ortholog of Arabidopsis ELF3, interacts with the E3 ligase APIP6 and negatively regulates immunity against Magnaporthe oryzae in rice. Mol Plant 8, 1679-1682.
46 Nohales MA, Kay SA (2016). Molecular mechanisms at the core of the plant circadian oscillator.Nat Struct Mol Biol 23, 1061-1069.
47 Nolte C, Staiger D (2015). RNA around the clock-regulation at the RNA level in biological timing.Front Plant Sci 6, 311.
48 Nomoto Y, Kubozono S, Yamashino T, Nakamichi N, Mizuno T (2012). Circadian clock- and PIF4-controlled plant growth: a coincidence mechanism directly integrates a hormone signaling network into the photoperiodic control of plant architectures inArabidopsis thaliana. Plant Cell Physiol 53, 1950-1964.
49 Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007). Rhythmic growth explained by coincidence between internal and external cues.Nature 448, 358-361.
50 Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011). The ELF4-ELF3- LUX complex links the circadian clock to diurnal control of hypocotyl growth.Nature 475, 398-402.
51 Romanowski A, Yanovsky MJ (2015). Circadian rhythms and post-transcriptional regulation in higher plants.Front Plant Sci 6, 437.
52 Sakuraba Y, Han SH, Yang HJ, Piao WL, Paek NC (2016). Mutation of Rice Early Flowering 3.1 (OsELF3.1) delays leaf senescence in rice. Plant Mol Biol 92, 223-234.
53 Sakuraba Y, Jeong J, Kang MY, Kim J, Paek NC, Choi G (2014). Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis.Nat Commun 5, 4636.
54 Seo PJ, Mas P (2014). Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis.Plant Cell 26, 79-87.
55 Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ (2012). TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis.Plant Cell 24, 2470-2482.
56 Song SS, Huang H, Gao H, Wang JJ, Wu DW, Liu XL, Yang SH, Zhai QZ, Li CY, Qi TC, Xie DX (2014). Interaction between MYC2 and ETHYLENE INSENSITIVE3 mo- dulates antagonism between jasmonate and ethylene signaling in Arabidopsis.Plant Cell 26, 263-279.
57 Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015). Photoperiodic flowering: time measurement mech- anisms in leaves.Annu Rev Plant Biol 66, 441-464.
58 Soy J, Leivar P, González-Schain N, Martín G, Diaz C, Sentandreu M, Al-Sady B, Quail PH, Monte E (2016). Molecular convergence of clock and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target promoters.Proc Natl Acad Sci USA 113, 4870-4875.
59 Tripathi P, Carvallo M, Hamilton EE, Preuss S, Kay SA (2017). Arabidopsis B-BOX32 interacts with CONSTANS- LIKE3 to regulate flowering.Proc Natl Acad Sci USA 114, 172-177.
60 Wang GY, Zhang C, Battle S, Lu H (2014). The phosphate transporter PHT4;1 is a salicylic acid regulator likely controlled by the circadian clock protein CCA1.Front Plant Sci 5, 701.
61 Wang L, Fujiwara S, Somers DE (2010). PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock.EMBO J 29, 1903-1915.
62 Wang L, Kim J, Somers DE (2013). Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription.Proc Natl Acad Sci USA 110, 761-766.
63 Wang P, Cui X, Zhao CS, Shi LY, Zhang GW, Sun FL, Cao XF, Yuan L, Xie QG, Xu XD (2017). COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response. J Integr Plant Biol 59, 78-85.
64 Wang W, Barnaby JY, Tada Y, Li Hr, Tör M, Caldelari D, Lee DU, Fu XD, Dong XN (2011a). Timing of plant immune responses by a central circadian regulator.Nature 470, 110-114.
65 Wang XT, Wu LJ, Zhang SF, Wu LC, Ku LX, Wei XM, Xie LL, Chen YH (2011b). Robust expression and association of ZmCCA1 with circadian rhythms in maize. Plant Cell Rep 30, 1261-1272.
66 Wang XX, Wu FM, Xie QG, Wang HM, Wang Y, Yue YL, Gahura O, Ma SS, Liu L, Cao Y, Jiao YL, Puta F, McClung CR, Xu XD, Ma LG (2012). SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis.Plant Cell 24, 3278-3295.
67 Wang ZY, Tobin EM (1998). Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207-1217.
68 Wu JF, Tsai HL, Joanito I, Wu YC, Chang CW, Li YH, Wang Y, Hong JC, Chu JW, Hsu CP, Wu SH (2016). LWD-TCP complex activates the morning gene CCA1 in Arabidopsis. Nat Commun 7, 13181.
69 Yang Y, Peng Q, Chen GX, Li XH, Wu CY (2013). OsELF3 is involved in circadian clock regulation for promoting flow- ering under long-day conditions in rice.Mol Plant 6, 202-215.
70 Yue YL, Liu NX, Jiang BJ, Li M, Wang HJ, Jiang Z, Pan HT, Xia QJ, Ma QB, Han TF, Nian H (2017). A single nucleotide deletion in J encoding GmELF3 confers long juvenility and is associated with adaption of tropic soybean. Mol Plant 10, 656-658.
71 Zhang C, Xie QG, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR, McDowell JM, Kong DD, Kwak JM, Lu H (2013). Crosstalk between the circadian clock and innate immunity in Arabidopsis.PLoS Pathog 9, e1003370.
72 Zhang YY, Wang Y, Wei H, Li N, Tian WW, Chong K, Wang L (2018). Circadian evening complex represses jasmo- nate-induced leaf senescence in Arabidopsis.Mol Plant 11, 326-337.
73 Zhao JM, Huang X, Ouyang XH, Chen WL, Du AP, Zhu L, Wang SG, Deng XW, Li SG (2012). OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS One 7, e43705.
74 Zheng XY, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW, Kay SA, Dong XN (2015). Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid.Proc Natl Acad Sci USA 112, 9166-9173.
75 Zhu JY, Oh E, Wang TN, Wang ZY (2016). TOC1-PIF4 interaction mediates the circadian gating of thermores- ponsive growth in Arabidopsis.Nat Commun 7, 13692.
Outlines

/