PIFs- and COP1-HY5-mediated temperature signaling in higher plants

Yeting Bian1, Li Chu1, Huan Lin1, Yaoyao Qi1, Fang Zheng1, Dongqing Xu1
1State Key Laboratory of Crop Genetics and Germplasm Enhancement, National Center for Soybean Improvement, College of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

Tóm tắt

AbstractPlants have to cope with the surrounding changing environmental stimuli to optimize their physiological and developmental response throughout their entire life cycle. Light and temperature are two critical environmental cues that fluctuate greatly during day-night cycles and seasonal changes. These two external signals coordinately control the plant growth and development. Distinct spectrum of light signals are perceived by a group of wavelength-specific photoreceptors in plants. PIFs and COP1-HY5 are two predominant signaling hubs that control the expression of a large number of light-responsive genes and subsequent light-mediated development in plants. In parallel, plants also transmit low or warm temperature signals to these two regulatory modules that precisely modulate the responsiveness of low or warm temperatures. The core component of circadian clock ELF3 integrates signals from light and warm temperatures to regulate physiological and developmental processes in plants. In this review, we summarize and discuss recent advances and progresses on PIFs-, COP1-HY5- and ELF3-mediated light, low or warm temperature signaling, and highlight emerging insights regarding the interactions between light and low or warm temperature signal transduction pathways in the control of plant growth.

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Tài liệu tham khảo

Bauer D, Viczián A, Kircher S, Nobis T, Nitschke R, Kunkel T et al (2004) Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16:1433–1445. https://doi.org/10.1105/tpc.021568

Blanco-Touriñán N, Legris M, Minguet EG, Costigliolo-Rojas C, Nohales MA, Iniesto E et al (2020) COP1 destabilizes DELLA proteins in Arabidopsis. Proc Natl Acad Sci U S A 117:13792–13799. https://doi.org/10.1073/pnas.1907969117

Brightbill CM, Sung S (2022) Temperature-mediated regulation of flowering time in Arabidopsis thaliana. aBIOTECH 3:78–84. https://doi.org/10.4161/psb.1.5.3452

Bu T, Lu S, Wang K, Dong L, Li S, Xie Q, Xu X, Cheng Q, Chen L, Fang C, Li H, Liu B, Weller JL, Kong F (2021) A critical role of the soybean evening complex in the control of photoperiod sensitivity and adaptation. Proc Natl Acad Sci U S A 118:e2010241118. https://doi.org/10.1073/pnas.2010241118

Casal JJ, Balasubramanian S (2019) Thermomorphogenesis. Annu Rev Plant Biol 70:321–346. https://doi.org/10.1146/annurev-arplant-050718-095919

Casal JJ, Boccalandro H (1995) Co-action between phytochrome B and HY4 in Arabidopsis thaliana. Planta 197:213–218. https://doi.org/10.1007/BF00202639

Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci U S A 108:16475–16480. https://doi.org/10.1073/pnas.1107161108

Chen D, Lyu M, Kou X, Li J, Yang Z, Gao L, Li Y, Fan LM, Shi H, Zhong S (2022) Integration of light and temperature sensing by liquid-liquid phase separation of phytochrome B. Mol Cell 12:S1097-2765(22)00493-2. https://doi.org/10.1016/j.molcel.2022.05.026

Chen M, Galvão RM, Li M, Burger B, Bugea J, Bolado J, Chory J (2010) Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141:1230–1240. https://doi.org/10.1016/j.cell.2010.05.007

Chen Q, Bai L, Wang W, Shi H, Ramón Botella J, Zhan Q, Liu K, Yang HQ, Song CP (2021) COP1 promotes ABA-induced stomatal closure by modulating the abundance of ABI/HAB and AHG3 phosphatases. New Phytol 229:2035–2049. https://doi.org/10.1111/nph.17001

Chen Z, Huang Y, Yang W, Chang G, Li P, Wei J, Yuan X, Huang J, Hu X (2019) The hydrogen sulfide signal enhances seed germination tolerance to high temperatures by retaining nuclear COP1 for HY5 degradation. Plant Sci 285:34–43. https://doi.org/10.1016/j.plantsci.2019.04.024

Cheng MC, Kathare PK, Paik I, Huq E (2021) Phytochrome signaling networks. Annu Rev Plant Biol 72:217–244. https://doi.org/10.1146/annurev-arplant-080620-024221

Chory J, Peto C, Feinbaum R, Pratt L, Ausubel F (1989) Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58:991–999. https://doi.org/10.1016/0092-8674(89)90950-1

Chung BYW, Balcerowicz M, Di Antonio M, Jaeger KE, Geng F, Franaszek K, Marriott P, Brierley I, Firth AE, Wigge PA (2020) An RNA thermoswitch regulates daytime growth in Arabidopsis. Nat Plants 6:522–532. https://doi.org/10.1038/s41477-020-0633-3

de Wit M, Galvão VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:513–537. https://doi.org/10.1146/annurev-arplant-043015-112252

Delker C, Sonntag L, James GV, Janitza P, Ibañez C, Ziermann H, Peterson T, Denk K, Mull S, Ziegler J, Davis SJ, Schneeberger K, Quint M (2014) The DET1-COP1-HY5 pathway constitutes a multipurpose signaling module regulating plant photomorphogenesis and thermomorphogenesis. Cell Rep 9:1983–1989. https://doi.org/10.1016/j.celrep.2014.11.043

Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71:791–801. https://doi.org/10.1016/0092-8674(92)90555-q

Ding L, Wang S, Song Z, Jiang Y, Han J, Lu S, Li L, Liu J (2018) Two B-Box domain proteins, BBX18 and BBX23, interact with ELF3 and regulate thermomorphogenesis in Arabidopsis. Cell Rep 25:1718–1728. https://doi.org/10.1016/j.celrep.2018.10.060

Ding Y, Shi Y, Yang S (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222:1690–1704. https://doi.org/10.1111/nph.15696

Ding Y, Shi Y, Yang S (2020) Molecular regulation of plant responses to environmental temperatures. Mol Plant 13:544–564. https://doi.org/10.1016/j.molp.2020.02.004

Ding Y, Yang S (2022) Surviving and thriving: how plants perceive and respond to temperature stress. Dev Cell 57:947–958. https://doi.org/10.1016/j.devcel.2022.03.010

Dong J, Ni W, Yu R, Deng XW, Chen H, Wei N (2017) Light-dependent degradation of PIF3 by SCFEBF1/2 promotes a photomorphogenic response in Arabidopsis. Curr Biol 27:2420–2430. https://doi.org/10.1016/j.cub.2017.06.062

Dong X, Yan Y, Jiang B, Shi Y, Jia Y, Cheng J, Shi Y, Kang J, Li H, Zhang D, Qi L, Han R, Zhang S, Zhou Y, Wang X, Terzaghi W, Gu H, Kang D, Yang S, Li J (2020) The cold response regulator CBF1 promotes Arabidopsis hypocotyl growth at ambient temperatures. EMBO J 39:e103630. https://doi.org/10.15252/embj.2019103630

Enderle B, Sheerin DJ, Paik I, Kathare PK, Schwenk P, Klose C, Ulbrich MH, Huq E, Hiltbrunner A (2017) PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nat Commun 8:2221. https://doi.org/10.1038/s41467-017-02311-8

Ernesto Bianchetti R, Silvestre Lira B, Santos Monteiro S, Demarco D, Purgatto E, Rothan C, Rossi M, Freschi L (2018) Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato. J Exp Bot 69:3573–3586. https://doi.org/10.1093/jxb/ery145

Fairchild CD, Schumaker MA, Quail PH (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome a signal transduction. Genes Dev 14:2377–2391. https://doi.org/10.1101/gad.828000

Fernández-Milmanda GL, Crocco CD, Reichelt M, Mazza CA, Köllner TG, Zhang T, Cargnel MD, Lichy MZ, Fiorucci AS, Fankhauser C, Koo AJ, Austin AT, Gershenzon J, Ballaré CL (2020) A light-dependent molecular link between competition cues and defence responses in plants. Nat Plants 6:223–230. https://doi.org/10.1038/s41477-020-0604-8

Fiorucci AS, Galvão VC, Ince YÇ, Boccaccini A, Goyal A, Allenbach Petrolati L, Trevisan M, Fankhauser C (2020) PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to elevated temperature in Arabidopsis seedlings. New Phytol 226:50–58. https://doi.org/10.1111/nph.16316

Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1413. https://doi.org/10.1038/ng.2007.3

Fujii Y, Tanaka H, Konno N, Ogasawara Y, Hamashima N, Tamura S, Hasegawa S, Hayasaki Y, Okajima K, Kodama Y (2017) Phototropin perceives temperature based on the lifetime of its photoactivated state. Proc Natl Acad Sci U S A 114:9206–9211. https://doi.org/10.1073/pnas.1704462114

Gaillochet C, Burko Y, Platre MP, Zhang L, Simura J, Willige BC, Kumar SV, Ljung K, Chory J, Busch W (2020) HY5 and phytochrome activity modulate shoot-to-root coordination during thermomorphogenesis in Arabidopsis. Development 147:dev192625. https://doi.org/10.1242/dev.192625

Galvão RM, Li M, Kothadia SM, Haskel JD, Decker PV, Van Buskirk EK, Chen M (2012) Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis. Genes Dev 26:1851–1863. https://doi.org/10.1101/gad.193219.112

Gangappa SN, Kumar SV (2017) DET1 and HY5 control PIF4-mediated thermosensory elongation growth through distinct mechanisms. Cell Rep 18:344–351. https://doi.org/10.1016/j.celrep.2016.12.046

Ge S, He L, Jin L, Xia X, Li L, Ahammed GJ, Qi Z, Yu J, Zhou Y (2022) Light-dependent activation of HY5 promotes mycorrhizal symbiosis in tomato by systemically regulating strigolactone biosynthesis. New Phytol 233:1900–1914. https://doi.org/10.1111/nph.17883

Guo X, Liu D, Chong K (2018) Cold signaling in plants: insights into mechanisms and regulation. J Integr Plant Biol 60:745–756. https://doi.org/10.1111/jipb.12706

Han D, Yu Z, Lai J, Yang C (2022) Post-translational modification: a strategic response to high temperature in plants. aBIOTECH 3:49–64. https://doi.org/10.1007/s42994-021-00067-w

Han X, Huang X, Deng XW (2020) The photomorphogenic central repressor COP1: conservation and functional diversification during evolution. Plant Commun 1:100044. https://doi.org/10.1016/j.xplc.2020.100044

Han X, Yu H, Yuan R, Yang Y, An F, Qin G (2019) Arabidopsis transcription factor TCP5 controls plant thermomorphogenesis by positively regulating PIF4 activity. iScience 15:611–622. https://doi.org/10.1016/j.isci.2019.04.005

Hayes S, Sharma A, Fraser DP, Trevisan M, Cragg-Barber CK, Tavridou E, Fankhauser C, Jenkins GI, Franklin KA (2017) UV-B rerceived by the UVR8 photoreceptor inhibits plant thermomorphogenesis. Curr Biol 27:120–127. https://doi.org/10.1016/j.cub.2016.11.004

Hoecker U (2017) The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Curr Opin Plant Biol 37:63–69. https://doi.org/10.1016/j.pbi.2017.03.015

Huai J, Zhang X, Li J, Ma T, Zha P, Jing Y, Lin R (2018) SEUSS and PIF4 coordinately eegulate light and temperature signaling pathways to control plant growth. Mol Plant 11:928–942. https://doi.org/10.1016/j.molp.2020.11.014

Huang D, Yuan Y, Tang Z, Huang Y, Kang C, Deng X, Xu Q (2019) Retrotransposon promoter of Ruby1 controls both light- and cold-induced accumulation of anthocyanins in blood orange. Plant Cell Environ 42:3092–3104. https://doi.org/10.1111/pce.13609

Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21:2441–2450. https://doi.org/10.1093/emboj/21.10.2441

Hwang G, Park J, Kim S, Park J, Seo D, Oh E (2021) Overexpression of BBX18 promotes thermomorphogenesis through the PRR5-PIF4 pathway. Front Plant Sci 12:782352. https://doi.org/10.3389/fpls.2021.782352

Ikeda M, Mitsuda N, Ishizuka T, Satoh M, Ohme-Takagi M (2021) The CIB1 transcription factor regulates light- and heat-inducible cell elongation via a two-step HLH/bHLH system. J Exp Bot 72:1795–1808. https://doi.org/10.1093/jxb/eraa567

Jiang B, Shi Y, Peng Y, Jia Y, Yan Y, Dong X, Li H, Dong J, Li J, Gong Z, Thomashow MF, Yang S (2020) Cold-induced CBF-PIF3 interaction enhances freezing tolerance by stabilizing the phyB thermosensor in Arabidopsis. Mol Plant 13:894–906. https://doi.org/10.1016/j.molp.2020.04.006

Jiang B, Shi Y, Zhang X, Xin X, Qi L, Guo H, Li J, Yang S (2017) PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proc Natl Acad Sci U S A 114:E6695–E6702. https://doi.org/10.1073/pnas.1706226114

Jin H, Lin J, Zhu Z (2020) PIF4 and HOOKLESS1 impinge on common transcriptome and isoform regulation in thermomorphogenesis. Plant Commun 1:100034. https://doi.org/10.1016/j.xplc.2020.100034

Jing Y, Lin R (2020) Transcriptional regulatory network of the light signaling pathways. New Phytol 227:683–697. https://doi.org/10.1111/nph.16602

Jung JH, Barbosa AD, Hutin S, Kumita JR, Gao M, Derwort D, Silva CS, Lai X, 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. https://doi.org/10.1038/s41586-020-2644-7

Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JC, Schäfer E, Jaeger KE, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354:886–889. https://doi.org/10.1126/science.aaf6005

Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141. https://doi.org/10.1126/science.291.5511.2138

Kahle N, Sheerin DJ, Fischbach P, Koch LA, Schwenk P, Lambert D, Rodriguez R, Kerner K, Hoecker U, Zurbriggen MD, Hiltbrunner A (2020) COLD REGULATED 27 and 28 are targets of CONSTITUTIVELY PHOTOMORPHOGENIC 1 and negatively affect phytochrome B signalling. Plant J 104:1038–1053. https://doi.org/10.1111/tpj.14979

Kang X, Ni M (2006) Arabidopsis SHORT HYPOCOTYL UNDER BLUE1 contains SPX and EXS domains and acts in cryptochrome signaling. Plant Cell 18:921–934. https://doi.org/10.1105/tpc.105.037879

Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16:3033–3044. https://doi.org/10.1105/tpc.104.025643

Kim C, Kim SJ, Jeong J, Park E, Oh E, Park YI, Lim PO, Choi G (2020) High ambient temperature accelerates leaf senescence via PHYTOCHROME-INTERACTING FACTOR 4 and 5 in Arabidopsis. Mol Cells 43:645–661. https://doi.org/10.14348/molcells.2020.0117

Kim HJ, Kim YK, Park JY, Kim J (2002) Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J 29:693–704. https://doi.org/10.1046/j.1365-313x.2002.01249.x

Kim S, Hwang G, Lee S, Zhu J, Paik I, Nguyen TT, Kim J, Oh E (2017) High ambient temperature represses anthocyanin biosynthesis through degradation of HY5. Front Plant Sci 8:1787. https://doi.org/10.3389/fpls.2017.01787

Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413. https://doi.org/10.1016/j.cub.2009.01.046

Lau OS, Song Z, Zhou Z, Davies KA, Chang J, Yang X, Wang S, Lucyshyn D, Tay IHZ, Wigge PA, Bergmann DC (2018) Direct control of SPEECHLESS by PIF4 in the high-temperature response of stomatal development. Curr Biol 28:1273–1280. https://doi.org/10.1016/j.cub.2018.02.054

Lee CM, Thomashow MF (2012) Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci U S A 109:15054–15059. https://doi.org/10.1073/pnas.1211295109

Lee JH, Park YJ, Kim JY, Park CM (2022) Phytochrome B conveys low ambient temperature cues to the ethylene-mediated leaf senescence in Arabidopsis. Plant Cell Physiol 63:326–339. https://doi.org/10.1093/pcp/pcab178

Lee S, Paik I, Huq E (2020) SPAs promote thermomorphogenesis by regulating the phyB-PIF4 module in Arabidopsis. Development 47:dev189233. https://doi.org/10.1242/dev.189233

Lee S, Wang W, Huq E (2021b) Spatial regulation of thermomorphogenesis by HY5 and PIF4 in Arabidopsis. Nat Commun 12:3656. https://doi.org/10.1038/s41467-021-24018-7

Lee S, Zhu L, Huq E (2021a) An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis. PLoS Genet 17:e1009595. https://doi.org/10.1371/journal.pgen.1009595

Legris M, Klose C, Burgie ES, Rojas CC, Neme M, Hiltbrunner A, Wigge PA, Schäfer E, Vierstra RD, Casal JJ (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354:897–900. https://doi.org/10.1126/science.aaf5656

Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194. https://doi.org/10.1016/s0092-8674(00)81095-8

Leivar P, Monte E, Oka Y, Liu T, Carle C, Castillon A, Huq E, Quail PH (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18:1815–1823. https://doi.org/10.1016/j.cub.2008.10.058

Li N, Bo C, Zhang Y, Wang L (2021b) PHYTOCHROME INTERACTING FACTORS PIF4 and PIF5 promote heat stress induced leaf senescence in Arabidopsis. J Exp Bot 72:4577–4589. https://doi.org/10.1093/jxb/erab158

Li N, Zhang Y, He Y, Wang Y, Wang L (2020b) Pseudo response regulators regulate photoperiodic hypocotyl growth by repressing PIF4/5 transcription. Plant Physiol 183:686–699. https://doi.org/10.1104/pp.19.01599

Li X, Liang T, Liu H (2022) How plants coordinate their development in response to light and temperature signals. Plant Cell 34:955–966. https://doi.org/10.1093/plcell/koab302

Li X, Liu C, Zhao Z, Ma D, Zhang J, Yang Y, Liu Y, Liu H (2020a) COR27 and COR28 are novel regulators of the COP1-HY5 regulatory hub and Photomorphogenesis in Arabidopsis. Plant Cell 32:3139–3154. https://doi.org/10.1105/tpc.20.00195

Li X, Ma D, Lu S, Hu X, Huang R, Liang T, Xu T, Tobin EM, Liu H (2016) Blue light- and low temperature-regulated COR27 and COR28 play roles in the Arabidopsis circadian clock. Plant Cell 28:2755–2769. https://doi.org/10.1105/tpc.16.00354

Li Y, Shi Y, Li M, Fu D, Wu S, Li J, Gong Z, Liu H, Yang S (2021a) The CRY2–COP1–HY5–BBX7/8 module regulates blue light-dependent cold acclimation in Arabidopsis. Plant Cell 33:3555–3573. https://doi.org/10.1093/plcell/koab215

Liang T, Yang Y, Liu H (2019) Signal transduction mediated by the plant UV-B photoreceptor UVR8. New Phytol 221:1247–1252. https://doi.org/10.1111/nph.15469

Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci U S A 95:2686–2690. https://doi.org/10.1073/pnas.95.5.2686

Liscum E, Briggs WR (1995) Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell 7:473–485. https://doi.org/10.1105/tpc.7.4.473

Liu J, Shi Y, Yang S (2018) Insights into the regulation of C-repeat binding factors in plant cold signaling. J Integr Plant Biol 60:780–795. https://doi.org/10.1111/jipb.12657

Ma D, Li X, Guo Y, Chu J, Fang S, Yan C, Noel JP, Liu H (2016) Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc Natl Acad Sci U S A 113:224–229. https://doi.org/10.1073/pnas.1511437113

Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160:1209–1221. https://doi.org/10.1016/j.cell.2015.01.046

Mao Z, He S, Xu F, Wei X, Jiang L, Liu Y, Wang W, Li T, Xu P, Du S, Li L, Lian H, Guo T, Yang HQ (2020) Photoexcited CRY1 and phyB interact directly with ARF6 and ARF8 to regulate their DNA-binding activity and auxin-induced hypocotyl elongation in Arabidopsis. New Phytol 225:848–865. https://doi.org/10.1111/nph.16194

Murcia G, Enderle B, Hiltbrunner A, Casal JJ (2021) Phytochrome B and PCH1 protein dynamics store night temperature information. Plant J 105:22–33. https://doi.org/10.1111/tpj.15034

Murcia G, Nieto C, Sellaro R, Prat S, Casal JJ (2022) Hysteresis in PHYTOCHROME INTERACTING FACTOR 4 and EARLY-FLOWERING 3 dynamics dominates warm daytime memory in Arabidopsis. Plant Cell 34:2188–2204. https://doi.org/10.1093/plcell/koac078

Nusinow D, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay S (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402. https://doi.org/10.1038/nature10182

Oh E, Zhu JY, Wang ZY (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14:802–809. https://doi.org/10.1038/ncb2545

Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466. https://doi.org/10.1038/35013076

Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995. https://doi.org/10.1101/gad.11.22.2983

Paik I, Huq E (2019) Plant photoreceptors: multi-functional sensory proteins and their signaling networks. Semin Cell Dev Biol 92:114–121. https://doi.org/10.1016/j.semcdb.2019.03.007

Paik I, Kathare PK, Kim JI, Huq E (2017) Expanding roles of PIFs in signal integration from multiple processes. Mol Plant 10:1035–1046. https://doi.org/10.1016/j.molp.2017.07.002

Pan C, Yang D, Zhao X, Liu Y, Li M, Ye L, Ali M, Yu F, Lamin-Samu AT, Fei Z, Lu G (2021) PIF4 negatively modulates cold tolerance in tomato anthers via temperature-dependent regulation of tapetal cell death. Plant Cell 33:2320–2339. https://doi.org/10.1093/plcell/koab120

Park YJ, Kim JY, Park CM (2022) SMAX1 potentiates phytochrome B-mediated hypocotyl thermomorphogenesis. Plant Cell. https://doi.org/10.1093/plcell/koac124

Park YJ, Lee HJ, Ha JH, Kim JY, Park CM (2017) COP1 conveys warm temperature information to hypocotyl thermomorphogenesis. New Phytol 215:269–280. https://doi.org/10.1111/nph.14581

Perea-Resa C, Rodríguez-Milla MA, Iniesto E, Rubio V, Salinas J (2017) Prefoldins negatively regulate cold acclimation in Arabidopsis thaliana by promoting nuclear proteasome-mediated HY5 degradation. Mol Plant 10:791–804. https://doi.org/10.1016/j.molp.2017.03.012

Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiol 76:1025–1038. https://doi.org/10.1104/pp.17.01384

Podolec R, Demarsy E, Ulm R (2021) Perception and signaling of ultraviolet-B radiation in plants. Annu Rev Plant Biol 72:793–822. https://doi.org/10.1146/annurev-arplant-050718-095946

Podolec R, Ulm R (2018) Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr Opin Plant Biol 45:18–25

Qi L, Shi Y, Terzaghi W, Yang S, Li J (2022) Integration of light and temperature signaling pathways in plants. J Integr Plant Biol 64:393–411. https://doi.org/10.1111/jipb.13216

Qiu Y, Li M, Kim RJ, Moore CM, Chen M (2019) Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA. Nat Commun 10:140. https://doi.org/10.1038/s41467-018-08059-z

Qiu Y, Li M, Pasoreck EK, Long L, Shi Y, Galvão RM et al (2015) HEMERA couples the proteolysis and transcriptional activity of PHYTOCHROME INTERACTING FACTORs in Arabidopsis photomorphogenesis. Plant Cell 27:1409–1427. https://doi.org/10.1105/tpc.114.136093

Qiu Y, Pasoreck EK, Yoo CY, He J, Wang H, Bajracharya A et al (2021) RCB initiates Arabidopsis thermomorphogenesis by stabilizing the thermoregulator PIF4 in the daytime. Nat Commun 12:2042. https://doi.org/10.1038/s41467-021-22313-x

Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E et al (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106. https://doi.org/10.1126/science.1200660

Ronald J, Su C, Wang L, Davis SJ (2022) Cellular localization of Arabidopsis EARLY FLOWERING3 is responsive to light quality. Plant Physiol 22:kiac072. https://doi.org/10.1093/plphys/kiac072

Rosado D, Trench B, Bianchetti R, Zuccarelli R, Rodrigues Alves FR, Purgatto E, Segal Floh EI, Silveira Nogueira FT, Freschi L, Rossi M (2019) Downregulation of PHYTOCHROME-INTERACTING FACTOR 4 influences plant development and fruit production. Plant Physiol 18:1360–1370. https://doi.org/10.1104/pp.19.00833

Saitoh A, Takase T, Abe H, Watahiki M, Hirakawa Y, Kiyosue T (2021) ZEITLUPE enhances expression of PIF4 and YUC8 in the upper aerial parts of Arabidopsis seedlings to positively regulate hypocotyl elongation. Plant Cell Rep 40:479–489. https://doi.org/10.1007/s00299-020-02643-8

Sato E, Nakamichi N, Yamashino T, Mizuno T (2002) Aberrant expression of the Arabidopsis circadian-regulated APRR5 gene belonging to the APRR1/TOC1 quintet results in early flowering and hypersensitiveness to light in early photomorphogenesis. Plant Cell Physiol 43:1374–1385. https://doi.org/10.1093/pcp/pcf166

Sellaro R, Smith RW, Legris M, Fleck C, Casal JJ (2019) Phytochrome B dynamics departs from photoequilibrium in the field. Plant Cell Environ 42:606–617. https://doi.org/10.1111/pce.13445

Shen H, Moon J, Huq E (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J 44:1023–1035. https://doi.org/10.1111/j.1365-313X.2005.02606.x

Shi J, Zhu Z (2021) Seedling morphogenesis: when ethylene meets high ambient temperature. aBIOTECH 3:40–48. https://doi.org/10.1007/s42994-021-00063-0

Shi Y, Ding Y, Yang S (2018) Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 23:623–637. https://doi.org/10.1016/j.tplants.2018.04.002

Somers DE, Kim WY, Geng R (2004) The F-box protein ZEITLUPE confers dosage-dependent control on the circadian clock, photomorphogenesis, and flowering time. Plant Cell 16:769–782. https://doi.org/10.1105/tpc.016808

Song Z, Bian Y, Liu J, Sun Y, Xu D (2020) B-box proteins: pivotal players in light-mediated development in plants. J Integr Plant Biol 62:1293–1309. https://doi.org/10.1111/jipb.12935

Sun J, Qi L, Li Y, Chu J, Li C (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating arabidopsis hypocotyl growth. PLoS Genet 8:e1002594. https://doi.org/10.1371/journal.pgen.1002594

Sun J, Qi L, Li Y, Zhai Q, Li C (2013) PIF4 and PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis. Plant Cell 25:2102–2114. https://doi.org/10.1105/tpc.113.112417

Sun Q, Wang S, Xu G, Kang X, Zhang M, Ni M (2019) SHB1 and CCA1 interaction desensitizes light responses and enhances thermomorphogenesis. Nat Commun 10:3110. https://doi.org/10.1038/s41467-019-11071-6

van der Woude LC, Perrella G, Snoek BL, van Hoogdalem M, Novák O, van Verk MC, van Kooten HN, Zorn LE, Tonckens R, Dongus JA, Praat M, Stouten EA, MCG P, Vellutini E, Patitaki E, Shapulatov U, Kohlen W, Balasubramanian S, Ljung K, van der Krol AR, Smeekens S, Kaiserli E, van Zanten M (2019) HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion. Proc Natl Acad Sci U S A 116:25343–25354. https://doi.org/10.1073/pnas.1911694116

von Arnim AG, Deng XW (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79:1035–1045. https://doi.org/10.1016/0092-8674(94)90034-5

Wagner D, Tepperman JM, Quail PH (1991) Overexpression of phytochrome B induces a short hypocotyl phenotype in transgenic Arabidopsis. Plant Cell 3:1275–1288. https://doi.org/10.1105/tpc.3.12.1275

Wang F, Chen X, Dong S, Jiang X, Wang L, Yu J, Zhou Y (2020) Crosstalk of PIF4 and DELLA modulates CBF transcript and hormone homeostasis in cold response in tomato. Plant Biotechnol J 18:1041–1055. https://doi.org/10.1111/pbi.13272

Wang P, Cui X, Zhao C, Shi L, Zhang G, Sun F et al (2017) COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response. J Integr Plant Biol 59:78–85. https://doi.org/10.1111/jipb.12512

Wang Q, Zuo Z, Wang X, Liu Q, Gu L, Oka Y, Lin C (2018) Beyond the photocycle-how cryptochromes regulate photoresponses in plants? Curr Opin Plant Biol 45:120–126. https://doi.org/10.1016/j.pbi.2018.05.014

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. https://doi.org/10.1016/s0092-8674(00)81464-6

Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM (2015) A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27:1925–1944. https://doi.org/10.1105/tpc.15.00146

Xiao Y, Chu L, Zhang Y, Bian Y, Xiao J, Xu D (2022) HY5: a pivotal regulator of light-dependent development in higher plants. Front Plant Sci 12:800989. https://doi.org/10.3389/fpls.2021.800989

Xu D (2020) COP1 and BBXs-HY5-mediated light signal transduction in plants. New Phytol 228:1748–1753. https://doi.org/10.1111/nph.16296

Xue M, Zhang H, Zhao F, Zhao T, Li H, Jiang D (2021) The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis. Mol. Plant 14:1799–1813. https://doi.org/10.1016/j.molp.2021.07.001

Yang G, Zhang C, Dong H, Liu X, Guo H, Tong B, Fang F, Zhao Y, Yu Y, Liu Y, Lin L, Yin R (2022) Activation and negative feedback regulation of SlHY5 transcription by the SlBBX20/21-SlHY5 transcription factor module in UV-B signaling. Plant Cell 34:2038–2055. https://doi.org/10.1093/plcell/koac064

Zhang J, Li X, Lin H, Chong K (2019) Crop improvement through temperature resilience. Annu Rev Plant Biol 70:753–780. https://doi.org/10.1146/annurev-arplant-050718-100016

Zhang L, Jiang X, Liu Q, Ahammed GJ, Lin R, Wang L, Shao S, Yu J, Zhou Y (2020) The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway. Plant Cell Environ 43:2712–2726. https://doi.org/10.1111/pce.13868

Zhang L, Li W, Tian Y, Davis S, Liu J (2021b) The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis. J Integr Plant Biol 63:1097–1103. https://doi.org/10.1111/jipb.13107

Zhang L, Shao Y, Ding L, Wang M, Davis S, Liu J (2021a) XBAT31 regulates thermoresponsive hypocotyl growth through mediating degradation of the thermosensor ELF3 in Arabidopsis. Sci Adv 7:eabf4427. https://doi.org/10.1126/sciadv.abf4427

Zhou P, Song M, Yang Q, Su L, Hou P, Guo L, Zheng X, Xi Y, Meng F, Xiao Y, Yang L, Yang J (2014) Both PHYTOCHROME RAPIDLY REGULATED1 (PAR1) and PAR2 promote seedling photomorphogenesis in multiple light signaling pathways. Plant Physiol 164:841–852. https://doi.org/10.1104/pp.113.227231

Zhou Y, Xun Q, Zhang D, Lv M, Ou Y, Li J (2019) TCP transcription factors associate with PHYTOCHROME INTERACTING FACTOR 4 and CRYPTOCHROME 1 to regulate thermomorphogenesis in Arabidopsis thaliana. iScience 15:600–610. https://doi.org/10.1016/j.isci.2019.04.002

Zhou Y, Zhang D, An J, Yin H, Fang S, Chu J, Zhao Y, Li J (2018) TCP transcription factors regulate shade avoidance via directly mediating the expression of both PHYTOCHROME INTERACTING FACTORs and auxin biosynthetic genes. Plant Physiol 176:1850–1861. https://doi.org/10.1104/pp.17.01566

Zhu J, Oh E, Wang T, Wang Z (2016) TOC1-PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis. Nat Commun 7:13692. https://doi.org/10.1038/ncomms13692

Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324. https://doi.org/10.1016/j.cell.2016.08.029

Zhu W, Zhou H, Lin F, Zhao X, Jiang Y, Xu D et al (2020) COLD-REGULATED GENE27 integrates signals from light and the circadian clock to promote hypocotyl growth in Arabidopsis. Plant Cell 32:3155–3169. https://doi.org/10.1105/tpc.20.00192