Plant Circadian Clock in Agricultural Production in Response to Global Warming
Received date: 2023-10-07
Accepted date: 2024-03-05
Online published: 2024-03-25
Global warming is now a major trend, in which temperature stress due to abnormal climate occurs frequently, posing a great challenge to the high-yield and stable agricultural production. The circadian clock, an endogenous, heritable timekeeping mechanism, endows plants with the ability to anticipate and respond rapidly to cyclic changes in external factors, which ensures that physiological and biochemical pathways are synchronized with the environment and greatly enhances plant’s ability to survive and reproduce. The temperature responses and temperature compensation are not only related to the key scientific issue of “synchronization” of the circadian clock with environmental signals, but also to the application of crop adaptation to temperature stress in agriculture. Temperature compensation refers to the fact that within a broad range of physiological temperatures, through transcriptional and post-transcriptional architecture, the clock can essentially maintain the circadian period length unchanged, ensuring that the timekeeping mechanism operates accurately. Light, temperature and humidity are closely coupled in the natural environment, and they act as timing factors, transmitting external cues to the core oscillators via the input pathway, which affects almost all processes of plant growth and development. In this review, we summarize the historical research of temperature response and compensation mechanism of plant circadian clocks, and describe the latest research progress, and also look forward to its application in crop genetic breeding and field management. We seek to provide new idea and solution to the problem of temperature stress adaptation in crops.
Qiguang Xie , Xiaodong Xu . Plant Circadian Clock in Agricultural Production in Response to Global Warming[J]. Chinese Bulletin of Botany, 2024 , 59(4) : 635 -650 . DOI: 10.11983/CBB23136
| [1] | Agnolucci P, Rapti C, Alexander P, De Lipsis V, Holland RA, Eigenbrod F, Ekins P (2020). Impacts of rising temperatures and farm management practices on global yields of 18 crops. Nat Food 1, 562-571. |
| [2] | Belbin FE, Hall GJ, Jackson AB, Schanschieff FE, Archibald G, Formstone C, Dodd AN (2019). Plant cir-cadian rhythms regulate the effectiveness of a glyphosate-based herbicide. Nat Commun 10, 3704. |
| [3] | Bonnot T, Nagel DH (2021). Time of the day prioritizes the pool of translating mRNAs in response to heat stress. Plant Cell 33, 2164-2182. |
| [4] | Buckley CR, Li X, Martí MC, Haydon MJ (2023). A bitter-sweet symphony: metabolic signals in the circadian sys-tem. Curr Opin Plant Biol 73, 102333. |
| [5] | 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. |
| [6] | Chen WW, Takahashi N, Hirata Y, Ronald J, Porco S, Davis SJ, Nusinow DA, Kay SA, Mas P (2020). A mobile ELF4 delivers circadian temperature information from shoots to roots. Nat Plants 6, 416-426. |
| [7] | Choudhary MK, Nomura Y, Wang L, Nakagami H, Somer-s DE (2015). Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic, and signaling pathways. Mol Cell Proteomics 14, 2243-2260. |
| [8] | Desai JS, Lawas LMF, Valente AM, Leman AR, Grinevich DO, Jagadish SVK, Doherty CJ (2021). Warm nights disrupt transcriptome rhythms in field-grown rice panicles. Proc Natl Acad Sci USA 118, e2025899118. |
| [9] | Ding YL, Li H, Zhang XY, Xie Q, Gong ZZ, Yang SH (2015). OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32,278- 289. |
| [10] | Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JCW, Lynn JR, Straume M, Smith JQ, Millar AJ (2006). FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18, 639-650. |
| [11] | Edwards KD, Lynn JR, Gyula P, Nagy F, Millar AJ (2005). Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170, 387-400. |
| [12] | Ezer D, Jung JH, Lan H, Biswas S, Gregoire L, Box MS, Charoensawan V, Cortijo S, Lai XL, St?ckle D, Zubieta C, Jaeger KE, Wigge PA (2017). The evening complex coordinates environmental and endogenous signals in Arabidopsis. Nat Plants 3, 17087. |
| [13] | Ford B, Deng WW, Clausen J, Oliver S, Boden S, Hem-ming 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. |
| [14] | Frank A, Matiolli CC, Viana AJC, Hearn TJ, Kusakina J, Belbin FE, Wells Newman D, Yochikawa A, Cano- Ramirez DL, Chembath A, Cragg-Barber K, Haydon MJ, Hotta CT, Vincentz M, Webb AAR, Dodd AN (2018). Circadian entrainment in Arabidopsis by the sugar- responsive transcription factor bZIP63. Curr Biol 28, 2597- 2606. |
| [15] | Gil KE, Kim WY, Lee HJ, Faisal M, Saquib Q, Alatar AA, Park CM (2017). ZEITLUPE contributes to a thermore-sponsive protein quality control system in Arabidopsis. Plant Cell 29, 2882-2894. |
| [16] | Gil KE, Park CM (2019). Thermal adaptation and plasticity of the plant circadian clock. New Phytol 221, 1215-1229. |
| [17] | Goodspeed D, Liu JD, Chehab EW, Sheng ZJ, Francisco M, Kliebenstein DJ, Braam J (2013). Postharvest circa-dian entrainment enhances crop pest resistance and phy-tochemical cycling. Curr Biol 23, 1235-1241. |
| [18] | Gould PD, Locke JCW, Larue C, Southern MM, Davis SJ, Hanano S, Moyle R, Milich R, Putterill J, Millar AJ, Hall A (2006). The molecular basis of temperature compensa-tion in the Arabidopsis circadian clock. Plant Cell 18, 1177-1187. |
| [19] | Gould PD, Ugarte N, Domijan M, Costa M, Foreman J, Macgregor D, Rose K, Griffiths J, Millar AJ, Finkens-t?dt B, Penfield S, Rand DA, Halliday KJ, Hall AJW (2013). Network balance via CRY signaling controls the Arabidopsis circadian clock over ambient temperatures. Mol Syst Biol 9, 650. |
| [20] | Greenham K, McClung CR (2015). Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16, 598-610. |
| [21] | Gutiérrez RA, Stokes TL, Thum K, Xu XD, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008). Systems approach identifies an organic nitrogen-responsive gene network that is regula-ted by the master clock control gene CCA1. Proc Natl Acad Sci USA 105, 4939-4944. |
| [22] | Hansen LL, Imrie L, Le Bihan T, van den Burg HA, van Ooijen G (2017a). Sumoylation of the plant clock transcription factor CCA1 suppresses DNA binding. J Biol Rhythms 32, 570-582. |
| [23] | Hansen LL, van den Burg HA, van Ooijen G (2017b). Sumoylation contributes to timekeeping and temperature compensation of the plant circadian clock. J Biol Rhythms 32, 560-569. |
| [24] | Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AAR (2013). Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502, 689-692. |
| [25] | Haydon MJ, Román á, Arshad W (2015). Nutrient homeo-stasis within the plant circadian network. Front Plant Sci 6, 299. |
| [26] | Hong S, Song HR, Lutz K, Kerstetter RA, Michael TP, McClung CR (2010). Type II protein arginine methyltrans-ferase 5 (PRMT5) is required for circadian period deter-mination in Arabidopsis thaliana. Proc Natl Acad Sci USA 107, 21211-21216. |
| [27] | Hsu PY, Devisetty UK, Harmer SL (2013). Accurate time-keeping is controlled by a cycling activator in Arabidopsis. eLife 2, e00473. |
| [28] | Huang H, Alvarez S, Bindbeutel R, Shen ZX, Naldrett MJ, Evans BS, Briggs SP, Hicks LM, Kay SA, Nusinow DA (2016). Identification of evening complex associated pro-teins in Arabidopsis by affinity purification and mass spectrometry. Mol Cell Proteomics 15, 201-217. |
| [29] | Jones MA, Morohashi K, Grotewold E, Harmer SL (2019). Arabidopsis JMJD5/JMJ30 acts independently of LUX ARRHYTHMO within the plant circadian clock to enable temperature compensation. Front Plant Sci 10, 57. |
| [30] | Jung JH, Barbosa AD, Hutin S, Kumita JR, Gao MJ, Derwort D, Silva CS, Lai XL, Pierre E, Geng F, Kim SB, Baek S, Zubieta C, Jaeger KE, Wigge PA (2020). A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 585, 256-260. |
| [31] | Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao MJ, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JCW, Sch?fer E, Jaeger KE, Wigge PA (2016). Phytochromes function as thermosen-sors in Arabidopsis. Science 354, 886-889. |
| [32] | Kidokoro S, Konoura I, Soma F, Suzuki T, Miyakawa T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2023). Clock-regulated coactivators selectively control gene expression in response to different temperature stress conditions in Arabidopsis. Proc Natl Acad Sci USA 120, e2216183120. |
| [33] | Kim SC, Nusinow DA, Sorkin ML, Pruneda-Paz J, Wang XM (2019). Interaction and regulation between lipid me-diator phosphatidic acid and circadian clock regulators. Plant Cell 31, 399-416. |
| [34] | Kim TS, Kim WY, Fujiwara S, Kim J, Cha JY, Park JH, Lee SY, Somers DE (2011). HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE. Proc Natl Acad Sci USA 108, 16843-16848. |
| [35] | 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. |
| [36] | Kon N, Wang HT, Kato YS, Uemoto K, Kawamoto N, Kawasaki K, Enoki R, Kurosawa G, Nakane T, Sugiya-ma Y, Tagashira H, Endo M, Iwasaki H, Iwamoto T, Kume K, Fukada Y (2021). Na+/Ca2+ exchanger mediates cold Ca2+ signaling conserved for temperature-compensated circadian rhythms. Sci Adv 7, eabe8132. |
| [37] | Kong YM, Han L, Liu X, Wang HF, Wen LZ, Yu XL, Xu XD, Kong FJ, Fu CX, Mysore KS, Wen JQ, Zhou C (2020). The nodulation and nyctinastic leaf movement is orchest-rated by clock gene LHY in Medicago truncatula. J Integr Plant Biol 62, 1880-1895. |
| [38] | Legris M, Klose C, Burgie ES, Rojas CCR, Neme M, Hilt-brunner A, Wigge PA, Sch?fer E, Vierstra RD, Casal JJ (2016). Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897-900. |
| [39] | Li BJ, Gao ZH, Liu XY, Sun DY, Tang WQ (2019). Trans-criptional profiling reveals a time-of-day-specific role of REVEILLE 4/8 in regulating the first wave of heat shock- induced gene expression in Arabidopsis. Plant Cell 31, 2353-2369. |
| [40] | Li W, Tian YY, Li JY, Yuan L, Zhang LL, Wang ZY, Xu XD, Davis SJ, Liu JX (2023). A competition-attenuation mechanism modulates thermoresponsive growth at warm temperatures in plants. New Phytol 237, 177-191. |
| [41] | Li Y, Wang LB, Yuan L, Song Y, Sun JQ, Jia Q, Xie QG, Xu XD (2020). Molecular investigation of organ-autonomous expression of Arabidopsis circadian oscillators. Plant Cell Environ 43, 1501-1512. |
| [42] | Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001). ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13, 1293-1304. |
| [43] | 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. |
| [44] | Ma Y, Dai XY, Xu YY, Luo W, Zheng XM, Zeng DL, Pan YJ, Lin XL, Liu HH, Zhang DJ, Xiao J, Guo XY, Xu SJ, Niu YD, Jin JB, Zhang H, Xu X, Li LG, Wang W, Qian Q, Ge S, Chong K (2015). COLD1 confers chilling tolerance in rice. Cell 160, 1209-1221. |
| [45] | Marshall CM, Tartaglio V, Duarte M, Harmon FG (2016). The Arabidopsis sickle mutant exhibits altered circadian clock responses to cool temperatures and temperature- dependent alternative splicing. Plant Cell 28, 2560-2575. |
| [46] | Mizuno T, Nakamichi N (2005). Pseudo-response regula-tors (PRRs) or True oscillator components (TOCs). Plant Cell Physiol 46, 677-685. |
| [47] | Mody T, Bonnot T, Nagel DH (2020). Interaction between the circadian clock and regulators of heat stress responses in plants. Genes (Basel) 11, 156. |
| [48] | Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Levi H, Moran N, Kaldenhoff R (2002). Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14, 727- 739. |
| [49] | Mwimba M, Karapetyan S, Liu LJ, Marqués J, McGinnis EM, Buchler NE, Dong XN (2018). Daily humidity oscil-lation regulates the circadian clock to influence plant physiology. Nat Commun 9, 4290. |
| [50] | 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. |
| [51] | 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. |
| [52] | Park YJ, Kim JY, Lee JH, Lee BD, Paek NC, Park CM (2020). GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis. Mol Plant 13, 459-470. |
| [53] | Patnaik A, Alavilli H, Rath J, Panigrahi KCS, Panigrahy M (2022). Variations in circadian clock organization & func-tion: a journey from ancient to recent. Planta 256, 91. |
| [54] | Portolés S, Más P (2010). The functional interplay between protein kinase CK2 and CCA1 transcriptional activity is essential for clock temperature compensation in Arabi-dopsis. PLoS Genet 6, e1001201. |
| [55] | Prado K, Cotelle V, Li GW, Bellati J, Tang N, Tournaire-Roux C, Martinière A, Santoni V, Maurel C (2019). Oscillating aquaporin phosphorylation and 14-3-3 proteins mediate the circadian regulation of leaf hydraulics. Plant Cell 31, 417-429. |
| [56] | Rawat R, Takahashi N, Hsu PY, Jones MA, Schwartz J, Salemi MR, Phinney BS, Harmer SL (2011). REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genet 7, e1001350. |
| [57] | Rikin A, Dillwith JW, Bergman DK (1993). Correlation between the circadian rhythm of resistance to extreme temperatures and changes in fatty acid composition in cot- ton seedlings. Plant Physiol 101, 31-36. |
| [58] | Salomé PA, Weigel D, McClung CR (2010). The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. Plant Cell 22, 3650-3661. |
| [59] | Sanchez SE, Kay SA (2016). The plant circadian clock: from a simple timekeeper to a complex developmental manager. Cold Spring Harb Perspect Biol 8, a027748. |
| [60] | Sanchez SE, Rugnone ML, Kay SA (2020). Light percep-tion: a matter of time. Mol Plant 13, 363-385. |
| [61] | Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998). The late elongated hypo-cotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219- 1229. |
| [62] | Schlaen RG, Mancini E, Sanchez SE, Perez-Santángelo S, Rugnone ML, Simpson CG, Brown JWS, Zhang X, Chernomoretz A, Yanovsky MJ (2015). The spliceosome assembly factor GEMIN2 attenuates the effects of temperature on alternative splicing and circadian rhythms. Proc Natl Acad Sci USA 112, 9382-9387. |
| [63] | Seo PJ, Park MJ, Lim MH, Kim SG, Lee M, Baldwin IT, Park CM (2012). A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24, 2427-2442. |
| [64] | Simon NML, Graham CA, Comben NE, Hetherington AM, Dodd AN (2020). The circadian clock influences the long- term water use efficiency of Arabidopsis. Plant Physiol 183, 317-330. |
| [65] | Somers DE, Webb AAR, Pearson M, Kay SA (1998). The short-period mutant, toc1-1, alters circadian clock regula-tion of multiple outputs throughout development in Arabidopsis thaliana. Development 125, 485-494. |
| [66] | Steed G, Ramirez DC, Hannah MA, Webb AAR (2021). Chronoculture, harnessing the circadian clock to improve crop yield and sustainability. Science 372, eabc9141. |
| [67] | Sun QB, Wang SL, Xu G, Kang XJ, Zhang M, Ni M (2019). SHB1 and CCA1 interaction desensitizes light responses and enhances thermomorphogenesis. Nat Commun 10, 3110. |
| [68] | Takase T, Ishikawa H, Murakami H, Kikuchi J, Sato-Nara K, Suzuki H (2011). The circadian clock modulates water dynamics and aquaporin expression in Arabidopsis roots. Plant Cell Physiol 52, 373-383. |
| [69] | Verslues PE, Bailey-Serres J, Brodersen C, Buckley TN, Conti L, Christmann A, Dinneny JR, Grill E, Hayes S, Heckman RW, Hsu PK, Juenger TE, Mas P, Munnik T, Nelissen H, Sack L, Schroeder JI, Testerink C, Tyer-man SD, Umezawa T, Wigge PA (2023). Burning ques-tions for a warming and changing world: 15 unknowns in plant abiotic stress. Plant Cell 35, 67-108. |
| [70] | Wang F, Han TW, Song QX, Ye WX, Song XG, Chu JF, Li JY, Chen ZJ (2020a). The rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell 32, 3124-3138. |
| [71] | Wang XH, Zhao C, Müller C, Wang CZ, Ciais P, Janssens I, Pe?uelas J, Asseng S, Li T, Elliott J, Huang Y, Li L, Piao S (2020b). Emergent constraint on crop yield res-ponse to warmer temperature from field experiments. Nat Sustain 3, 908-916. |
| [72] | 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 compo-nent of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24, 3278-3295. |
| [73] | Wang ZY, Tobin EM (1998). Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene dis-rupts circadian rhythms and suppresses its own expres-sion. Cell 93, 1207-1217. |
| [74] | Wei H, Wang Y, Liu BH, Wang L (2018). Deciphering the underlying mechanism of the plant circadian system and its regulation on plant growth and development. Chin Bull Bot 53, 456-467. (in Chinese) |
| 魏华, 王岩, 刘宝辉, 王雷 (2018). 植物生物钟及其调控生长发育的研究进展. 植物学报 53, 456-467. | |
| [75] | 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. |
| [76] | Xie QG, Wang P, Liu X, Yuan L, Wang LB, Zhang CG, Li Y, Xing HY, Zhi LY, Yue ZL, Zhao CS, McClung CR, Xu XD (2014). LNK1 and LNK2 are transcriptional coactive-tors in the Arabidopsis circadian oscillator. Plant Cell 26, 2843-2857. |
| [77] | Xu XD, Hotta CT, Dodd AN, Love J, Sharrock R, Lee YW, Xie QG, Johnson CH, Webb AAR (2007). Distinct light and clock modulation of cytosolic free Ca2+ oscillations and rhythmic CHLOROPHYLL A/B BINDING PROTEIN2 promoter activity in Arabidopsis. Plant Cell 19, 3474-3490. |
| [78] | Xu XD, Yuan L, Xie QG (2022a). The circadian clock ticks in plant stress responses. Stress Biol 2, 15. |
| [79] | Xu XD, Yuan L, Yang X, Zhang X, Wang L, Xie QG (2022b). Circadian clock in plants: linking timing to fitness. J Integr Plant Biol 64, 792-811. |
| [80] | Yanovsky MJ, Izaguirre M, Wagmaister JA, Gatz C, Jackson SD, Thomas B, Casal JJ (2000). Phytochrome A resets the circadian clock and delays tuber formation under long days in potato. Plant J 23, 223-232. |
| [81] | Yuan L, Hu Y, Li SL, Xie QG, Xu XD (2021). PRR9 and PRR7 negatively regulate the expression of EC compo-nents under warm temperature in roots. Plant Signal Be-hav 16, 1855384. |
| [82] | Zhang HT, Kumimoto RW, Anver S, Harmer SL (2023). XAP5 CIRCADIAN TIMEKEEPER regulates RNA splicing and the circadian clock by genetically separable pathway-s. Plant Physiol 192, 2492-2506. |
| [83] | Zhang LL, Li W, Tian YY, Davis SJ, Liu JX (2021a). The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis. J Integr Plant Biol 63,1097-1103. |
| [84] | Zhang LL, Luo AN, Davis SJ, Liu JX (2021b). Timing to grow: roles of clock in thermomorphogenesis. Trends Plant Sci 26, 1248-1257. |
| [85] | Zhou M, Wang W, Karapetyan S, Mwimba M, Marqués J, Buchler NE, Dong XN (2015). Redox rhythm reinforces the circadian clock to gate immune response. Nature 523, 472-476. |
/
| 〈 |
|
〉 |
Home