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Pivotal Roles of the Phytochrome-Interacting Factors in Cryptochrome Signaling

2016; Elsevier BV; Volume: 9; Issue: 4 Linguagem: Inglês

10.1016/j.molp.2016.02.007

1674-2052

Pengbo Xu, Hongli Lian, Wenxiu Wang, Feng Xu, Hong‐Quan Yang,

Greenhouse Technology and Climate Control

Light, as both energy source and informational signal, profoundly influences plant growth and development during the whole life span from seed germination to flowering. Plant senses light through multiple photoreceptors including the blue/UV-A photoreceptors cryptochromes (CRY, CRY1/2) and phototropins (PHOT, PHOT1/2), the red/far-red photoreceptors phytochromes (PHY, phyA-E), and the UV-B photoreceptor UVR8. In Arabidopsis, both CRY and PHY are involved in mediating light regulation of hypocotyl elongation, cotyledon/leaf expansion, anthocyanin accumulation, flowering, stomatal development, and light entrainment of the circadian clock. CRYs are photolyase-like flavoproteins that mediate various light responses not only in plants but in animals as well. They contain a typical N-terminal photolyase-related domain (PHR) and a distinguishing C-terminal extension domain (CCE, also known as CCT). Arabidopsis CRY1/2 C-termini (CCE1/CCE2, also known as CCT1/CCT2) are shown to mediate CRY1/2 blue light signaling. The first identified CRY1/2-interacting protein was COP1 (Wang et al., 2001Wang H. Ma L.G. Li J.M. Zhao H.Y. Deng X.W. Direct interaction of Arabidopsis cryptochromes with COP1 in light control development.Science. 2001; 294: 154-158Crossref PubMed Scopus (395) Google Scholar, Yang et al., 2001Yang H.Q. Tang R.H. Cashmore A.R. The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1.Plant Cell. 2001; 13: 2573-2587Crossref PubMed Scopus (303) Google Scholar), the master negative regulator of photomorphogenesis. CRY1/2 also interact with SPA1 (Lian et al., 2011Lian H.L. He S.B. Zhang Y.C. Zhu D.M. Zhang J.Y. Jia K.P. Sun S.X. Li L. Yang H.Q. Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism.Genes Dev. 2011; 25: 1023-1028Crossref PubMed Scopus (228) Google Scholar, Liu et al., 2011Liu B. Zuo Z. Liu H. Liu X. Lin C. Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light.Genes Dev. 2011; 25: 1029-1034Crossref PubMed Scopus (276) Google Scholar). The interactions of CRY1/2 with COP1 and SPA1 can result in attenuation of COP1 activity and stabilization of HY5/CO proteins, thus inhibiting hypocotyl elongation and promoting floral initiation (Figure 1). Another CRY2-interacting protein is CIB1, a bHLH transcription factor that promotes FT transcription to promote floral initiation (Liu et al., 2008Liu H.T. Yu X.H. Li K.W. Klejnot J. Yang H.Y. Lisiero D. Lin C.T. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis.Science. 2008; 322: 1535-1539Crossref PubMed Scopus (499) Google Scholar). Most recently, two independent studies from the Chory (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar) and Liu (Ma et al., 2016Ma D. Li X. Guo Y. Chu J. Fang S. Yan C. Noel J.P. Liu H. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light.Proc. Natl. Acad. Sci. USA. 2016; 113: 224-229Crossref PubMed Scopus (250) Google Scholar) groups revealed that the phytochrome-interacting factors (PIFs), which have been well known to specifically mediate phytochrome signaling, are also cryptochrome-interacting proteins that mediate responses to canopy shade low blue light or high temperature (Figure 1). Specifically, PIF4, PIF5, and CRY2 are found to bind to common chromatin regions of target genes (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar), and CRY1 is shown to associate with the promoters of PIF4 target genes, including auxin biosynthetic gene (YUC8) and auxin-responsive genes (IAA19, IAA29) (Ma et al., 2016Ma D. Li X. Guo Y. Chu J. Fang S. Yan C. Noel J.P. Liu H. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light.Proc. Natl. Acad. Sci. USA. 2016; 113: 224-229Crossref PubMed Scopus (250) Google Scholar). It is intriguing that, under canopy shade low blue light (LBL, 1.8315 μmol m−2 s−1 blue light under the background of red (R) and far-red (FR) light with R:FR of 7.0478) and normal temperature conditions for Arabidopsis seedling growth, CRY1/2 interact with PIF4/5 to promote hypocotyl elongation through promotion of PIF activity (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar). However, under high temperature (28°C) and high blue light (40 μmol m−2 s−1), blue-light-induced CRY1-PIF4 interaction leads to suppression of the transcriptional activity of PIF4, thus inhibits hypocotyl elongation (Ma et al., 2016Ma D. Li X. Guo Y. Chu J. Fang S. Yan C. Noel J.P. Liu H. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light.Proc. Natl. Acad. Sci. USA. 2016; 113: 224-229Crossref PubMed Scopus (250) Google Scholar). It is interesting that both CRY-PIF and PHY-PIF interactions are light-dependent. Namely, CRY1/2 interact with PIFs in a blue-light-dependent manner (Ma et al., 2016Ma D. Li X. Guo Y. Chu J. Fang S. Yan C. Noel J.P. Liu H. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light.Proc. Natl. Acad. Sci. USA. 2016; 113: 224-229Crossref PubMed Scopus (250) Google Scholar, Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar), whereas phyA/B interact with PIFs dependent on red light, which induce the formation of the active Pfr conformer of phyA/B. It is well known that red-light-triggered interaction of phytochrome B (phyB) with PIFs leads to PIFs' sequential phosphorylation, ubiquitination, and degradation via the 26S proteasome system (Leivar and Quail, 2011Leivar P. Quail P.H. PIFs: pivotal components in a cellular signaling hub.Trends Plant Sci. 2011; 16: 19-28Abstract Full Text Full Text PDF PubMed Scopus (666) Google Scholar). However, it is not known whether CRY-PIFs interactions result in these similar processes. Based on the hypocotyl elongation phenotype under LBL, it is proposed that CRY2-PIF4/5 interactions result in the promotion of PIF4/5 activity, presumably due to stabilization of CRY2 and PIF4/5 proteins (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar). Whereas under high temperature, CRY1-PIF4 interaction leads to the inhibition of PIF4 activity (Ma et al., 2016Ma D. Li X. Guo Y. Chu J. Fang S. Yan C. Noel J.P. Liu H. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light.Proc. Natl. Acad. Sci. USA. 2016; 113: 224-229Crossref PubMed Scopus (250) Google Scholar). Although both LBL and low R:FR (1.23 μE m−2 s−1 blue light under the background of R and FR light with R:FR of 0.7) lead to enhanced hypocotyl elongation, which are mediated by CRY1/2-PIF4 and phyB-PIF7, respectively, RNA-seq analyses indicate that there are few overlapping genes regulated by these light conditions (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar). These findings imply that shade avoidance response (SAR) is primarily mediated by phyB-PIF and CRY-PIF interactions under low R:FR and LBL, respectively. Given that LBL and low R:FR belong to the SAR signals, and that phyB mediates SAR, it is possible that phyB may also mediate the LBL response. Indeed, under LBL, phyB-overexpressing seedlings do not elongate in response to LBL compared with the wild type, indicating that extremely high levels of phyB suppress LBL responses (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar). Moreover, expression of PIF4/5mAPB in pif4/pif5 mutants fails to fully rescue the mutant phenotypes regardless of PIF protein abundance (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar). These observations suggest that phyB suppresses LBL responses, and that the APB domain-mediated interaction of PIF with phyB leads to enhanced PIF activity, thus promoting hypocotyl elongation in response to LBL (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar), which is in contrast to repression of PIF activity by phyB in red light (Leivar and Quail, 2011Leivar P. Quail P.H. PIFs: pivotal components in a cellular signaling hub.Trends Plant Sci. 2011; 16: 19-28Abstract Full Text Full Text PDF PubMed Scopus (666) Google Scholar). It has been shown that phyB interacts with multiple PIFs such as PIF1, PIF3, PIF4, PIF5, and PIF7, and that phyA also interacts with PIF1 and PIF3 (Leivar and Quail, 2011Leivar P. Quail P.H. PIFs: pivotal components in a cellular signaling hub.Trends Plant Sci. 2011; 16: 19-28Abstract Full Text Full Text PDF PubMed Scopus (666) Google Scholar). In addition, phyB and PIF1/3 are known to bind to the same DNA elements, and it is now shown that CRY2 and PIF4/5 bind to the similar chromatin regions (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar). CRY2 binds phyB, and phyA physically interacts with CRY1. Therefore, these highly dynamic interactions may lead to formation of varied large protein complexes consisting of CRYs, PHYs, and PIFs, which confer plants the plasticity to get adapted to the varied light conditions in nature. It is worth noting that PIFs have emerged as critical signaling integrators that link light signaling pathway to gibberellin acids (GA), brassinosteroid (BR), and auxin signaling pathways through physical interactions of PIFs with DELLA proteins, BZR1, and ARF6, which are important transcriptional regulators in GA, BR, and auxin signaling pathways, respectively (Oh et al., 2014Oh E. Zhu J.Y. Bai M.Y. Arenhart R.A. Sun Y. Wang Z.Y. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl.Elife. 2014; 3: e03031Crossref Scopus (375) Google Scholar). In future studies, more effort should be made to explore the physiological significance of these various interactions in different types of cells under different environmental conditions of light and temperature, and in the varied internal phytohormone signaling status in plants. It is interesting that the N-terminal PHR domain of CRY2 mediates the interaction with PIF5 (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar), since it has been demonstrated that the interactions of CRY1/2 with COP1 are mediated through their C termini, whereas CRY2 interacts with SPA1 and CIB1 through its N-terminal PHR domain. Given that the N-terminal domain of CRY1 (CNT1) is shown to be able to mediate blue light inhibition of hypocotyl elongation independent of its C terminus (He et al., 2015He S.B. Wang W.X. Zhang J.Y. Xu F. Lian H.L. Li L. Yang H.Q. The CNT1 domain of Arabidopsis CRY1 alone is sufficient to mediate blue light inhibition of hypocotyl elongation.Mol. Plant. 2015; 8: 822-825Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar), it has been proposed that there may be CNT1-interacting proteins. Since it is now demonstrated that CRY2 interacts with PIF5 through its N terminus (Pedmale et al., 2016Pedmale U.V. Huang S.S.C. Zander M. Cole B.J. Hetzel J. Ljung K. Reis P.A.B. Sridevi P. Nito K. Nery J.R. et al.Cryptochromes interact directly with PIFs to control plant growth in limiting blue light.Cell. 2016; 164: 233-245Abstract Full Text Full Text PDF PubMed Scopus (336) Google Scholar), it is likely that CRY1-PIF interactions are mediated by CNT1. It is tempting to speculate that there may be more CNT1-interacting proteins. Identification of these proteins will advance our understating of cryptohrome signaling network that confers plants the capacity to fine tune their growth and development under the complex external and internal signal conditions. Our work is supported by grants from the National Natural Science Foundation of China (31530085, 91217307, 90917014, 30830012, 30325007, and 90208005 to H.-Q.Y. and 31170266 to H.-L.L.).