- Email: [email protected]
Direct Regulation of Phytohormone Actions by Photoreceptors
TRPLSC 1755 No. of Pages 3
Spotlight
Direct Regulation of Phytohormone Actions by Photoreceptors Yiwen Luo1,2 and Hui Shi1,* Plants must adjust their growth and development adaptively in response to light. Four recent studies have now established novel paradigms connecting light and hormone signaling pathways, in which photoreceptors adopt three modes to directly inhibit internal hormonal responses to external stimuli. As sessile organisms, plants are equipped with the capacity to sense environmental information and adjust their growth and development accordingly. Light is one of the most important environmental factors, and exposure to light widely and profoundly regulates plant developmental processes (known as photomorphogenesis) [1]. To precisely sense the light signal, plants employ a series of photoreceptors across the spectrum of light. The red/far-red light (600– 750 nm) receptors are members of phytochrome family, which contains five members (phyA to phyE) in arabidopsis (Arabidopsis thaliana) [2]. Cryptochromes, phototropins, and the ZEITLUPE family members sense the blue light (350–500 nm) [2]. UVR8 (UV RESISTANCE LOCUS 8) is the UV-B light (275– 320 nm) receptor for UV-B responses [2]. Plants track the status of their light environment, transduce the signals to the nucleus, and ultimately direct gene expression changes to induce light responses. Without developing a nervous system, plants have evolved phytohormones which act as internal chemical messengers for multicellular communication and coordinating plant growth and
development in adaptation to various ethylene signaling pathway, is rapidly environmental conditions [3]. degraded within 30 minutes. Photoactivated phyB, EIN3, and the two F-box In the past decade the molecular interac- proteins of the EIN3 E3 ligase SCFEBF1/2 tions between light and phytohormone form a tripartite protein complex. Among pathways have been extensively investi- them, phyB interacts with EIN3 in a red gated [1]. Previous studies revealed that light-dependent manner, but physically light modulates the metabolism and sig- associates with SCFEBF1/2. With red light naling transduction of phytohormones via activation, phyB acts as the ‘molecular key transcription factors and/or regula- glue’, directly enhancing the EIN3– tors. For example, PHYTOCHROME- SCFEBF1/2 interaction and thus promoting INTERACTING FACTORs (PIFs) target EIN3 protein degradation [7]. This mechand regulate expression of the genes anism enables a primary control of the responsible for hormone biosynthesis, ethylene signaling pathway upon the initial metabolism, and signal transduction [1]. light exposure during seedling emergence Key transcription factors of light and phy- from the soil, and this sheds light on the tohormone signaling pathways, such as integrating roles of photoreceptors in PIF3 and ETHYLENE-INSENSITIVE 3 light–hormone crosstalk. (EIN3) (light and ethylene), and PIF4 and BRASSINAZOLE-RESISTANT 1 (BZR1) Subsequently, two recent studies dem(light and brassinosteroids, BRs), have onstrated that photoreceptors directly been shown to form molecular modules modulate auxin responses [8,9]. Typical and act as integrators of light and hor- auxin signaling pathway consists of F-box mone signals [4,5]. Remarkably, four protein TIR1, core repressors AUX/IAAs, recent studies have revealed that light and transcription factors AUXIN and hormone signaling pathways seem RESPONSE FACTORS (ARFs). Auxin is to be integrated at the photoreceptor perceived by receptor TIR1 that promotes level, providing a novel molecular frame- the assembly of the TIR1–AUX/IAA prowork for how plants transduce external tein complex to degrade AUX/IAA prolight information to direct internal hor- teins and initiate auxin-responsive gene monal responses. expression. Xu et al. found that the blue light receptor CRY1 directly interacts with Buried seedlings grow upwards in dark- AUX/IAA in a blue light-dependent manness and push against the mechanical ner [8]. Moreover, CRY1 interacts with the barrier of soil. Upon emerging from the N-terminal domain of AUX/IAA, which is soil, seedlings are exposed to light irradi- responsible for the interaction between ation and are released from mechanical TIR1 and AUX/IAA. In vitro and in vivo pressure. Previous studies showed that assays showed that CRY1 interferes with buried seedlings produce ethylene quan- the formation of the AUX/IAA–TIR1 protitatively in response to mechanical pres- tein complex, thus repressing auxinsure. It has therefore been proposed that induced AUX/IAA degradation. Taken light and ethylene signaling pathways are together, Xu et al. propose a novel antagtightly integrated with each other during onistic module, CRY1–AUX/IAA–TIR1, in seedling emergence [6]. Extensive bio- which blue light induces CRY1–AUX/IAA chemical evidence has dissected the interaction to interfere with the associamolecular actions of phyB in mediating tion and subsequent degradation of AUX/ red light-inhibited ethylene responses IAA by TIR1 [8]. Interestingly, phyA and [7]. Upon light exposure, EIN3 protein, phyB adopt similar mechanisms to prothe master transcription factor of the tect AUX/IAA in shade avoidance and red
Trends in Plant Science, Month Year, Vol. xx, No. yy
1
TRPLSC 1755 No. of Pages 3
UVB
Blue
UVR8
CRY1
Red Far-red
phyA/phyB phyA Photoreceptors
UVR8/CRY1 Nucleus CRY1 UVR8 BIM1/BES1
C
C N N
BIM1/BES1
Light spectrum
CRY1/phyA/phyB CRY1 C
C
Nucleus phyA/phyB SCFTIR1
N N
AUX/IAA ARFs
phyB Nucleus phyB
SCFEBF1/2 EIN3
AUX/IAA ARFs
BR-responsive genes
Auxin-responsive genes
SequestraƟon
Interference
Ethylene-responsive genes
Molecular glue
Figure 1. Photoreceptors Directly Connect Light and Hormone Signaling Pathways in Three Ways. (i) Sequestration: UV-B photoreceptor UVR8 and blue light receptor CRY1 associate with BIM1/BES1 to directly sequester the DNA-binding activities of BES1/BIM1 in brassinosteroid (BR) responses. (ii) Interference: blue light receptor CRY1, and red and far-red light receptors phyA and phyB, directly interact with AUX/IAA, competitively interfering with the association and degradation of AUX/IAA by their E3 ligase SCFTIR1. ARF-mediated auxin responses are then inhibited. (iii) Molecular glue: red light receptor phyB acts as a light-controlled molecular glue to promote EIN3 degradation via enhancing the interaction between EIN3 and its E3 ligase SCFEBF1/EBF2, rapidly turning off ethylene responses.
light conditions, respectively, suggesting that the photoreceptor–AUX/IAA–TIR1 module is a general machinery that allows direct regulation of the auxin signaling pathway by diverse light conditions [8,9]. In contrast to ethylene and auxin signaling, BR responses are inhibited by UV-B photoreceptor UVR8 or blue light receptor CRY1 via sequestration [10,11]. By using yeast two-hybrid screening, the transcription factors of BR signaling, BIM1 and BES1, were identified as UVR8-interacting proteins. UV-B-activated nuclear UVR8 affects neither the gene expression nor protein levels of BIM1/BES1, but it sequesters the DNA-binding activity of BIM1/ BES1 to shut down BR signaling pathway [10]. Similar to UVR8, CRY1 specifically 2
Trends in Plant Science, Month Year, Vol. xx, No. yy
interacts with the biologically active form of BES1 protein (the dephosphorylated BES1) and thus sequesters the BES1 DNA-binding activity [11]. Interestingly, the CRY1–BES1 interaction occurs in a blue light-dependent manner. However, the interactions between UVR8 and BIM1/BES1 are independent of UV-B. UV-B increases the protein abundance of UVR8 in the nucleus, resulting in increased levels of the UVR8–BES1/BIM1 protein complex [10,11].
Concluding Remarks and Perspectives The reports highlighted here together illustrate that photoreceptors directly integrate light and hormone signaling pathways. For the ethylene signaling pathway, the red
light photoreceptor phyB promotes the interaction between EIN3 and its E3 ligase SCFEBF1/2 in a light-dependent way, stimulating rapid degradation of EIN3 proteins [7]. For the auxin signaling pathway, photoactivated CRY1, phyA, and phyB interact with AUX/IAA, interfere the AUX/IAA– TIR1 interactions, and thus inhibit auxininduced AUX/IAA protein degradation [8,9]. For the BR signaling pathway, the photoreceptors CRY1 and UVR8 directly interact with BIM1/BES1, sequestering their DNA-binding activity and repressing downstream responses [10,11]. These reports not only propose exciting modes of action of photoreceptors but have also established the early integration events of light and hormone signaling pathways (Figure 1).
TRPLSC 1755 No. of Pages 3
Being sessile, plants adopt a highly developed strategy to optimize their growth and development according to the changing environment. As mentioned above, research in the past few years has revealed the multiple-level integration of light and hormone signaling pathways. First, light regulates the expression of genes involved in hormone biosynthesis or responses. Second, transcription factor modules integrate light and hormone signaling pathways via transcription cascades or protein–protein interactions. The photoreceptor-integrated mechanisms reported here reveal more direct signal transduction from external factors to modify internal responses. It will be necessary to elucidate further the relationships between these multiple levels of integration and reveal their biological significance in the diverse and dynamic light environment. For example, red light irradiation rapidly represses the expression of several AUX/IAA genes, probably through direct regulation targeted by PIF proteins [12]. Therefore, light stabilizes AUX/IAA protein accumulation via interaction with photoreceptors, but
decreases the expression of AUX/IAA genes, likely depending on PIFs. The opposing effects of light on AUX/IAA protein stability and gene transcription might constitute a negative feedback circuit to fine-tune auxin responses upon light. In addition, whether lightregulated hormone responses are tissue- or organ-specific needs to be explored. Dissecting their regulation specifically in cotyledons, hypocotyls, and roots would greatly improve our understanding of photomorphogenesis. Acknowledgments We thank Dr Shangwei Zhong for comments. This work was supported by the National Science Foundation of China (grant 31770208 to H.S.). 1
College of Life Sciences, Capital Normal University, Beijing 100048, China
2
State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China *Correspondence: [email protected] (H. Shi). https://doi.org/10.1016/j.tplants.2018.11.002
2. Galvao, V.C. and Fankhauser, C. (2015) Sensing the light environment in plants: photoreceptors and early signaling steps. Curr. Opin. Neurobiol. 34, 46–53 3. Chaiwanon, J. et al. (2016) Information integration and communication in plant growth regulation. Cell 164, 1257–1268 4. Liu, X. et al. (2017) EIN3 and PIF3 form an interdependent module that represses chloroplast development in buried seedlings. Plant Cell 29, 3051–3067 5. Oh, E. et al. (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802–809 6. Zhong, S. et al. (2014) Ethylene-orchestrated circuitry coordinates a seedling's response to soil cover and etiolated growth. Proc. Natl. Acad. Sci. U. S. A. 111, 3913– 3920 7. Shi, H. et al. (2016) The red light receptor phytochrome B directly enhances substrate–E3 ligase interactions to attenuate ethylene responses. Dev. Cell 39, 597–610 8. Xu, F. et al. (2018) Photoactivated CRY1 and phyB interact directly with AUX/IAA proteins to inhibit auxin signaling in Arabidopsis. Mol. Plant 11, 523–541 9. Yang, C. et al. (2018) Phytochrome A negatively regulates the shade avoidance response by increasing auxin/indole acidic acid protein stability. Dev. Cell 44, 29–41 10. Liang, T. et al. (2018) UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Dev. Cell 44, 512–523 11. Wang, W. et al. (2018) Photoexcited CRYPTOCHROME1 interacts with dephosphorylated BES1 to regulate brassinosteroid signaling and photomorphogenesis in Arabidopsis. Plant Cell 30, 1989–2005 12. Leivar, P. et al. (2012) Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24, 1398–1419
References 1. de Wit, M. et al. (2016) Light-mediated hormonal regulation of plant growth and development. Annu. Rev. Plant Biol. 67, 513–537
Trends in Plant Science, Month Year, Vol. xx, No. yy
3
Spotlight
Direct Regulation of Phytohormone Actions by Photoreceptors Yiwen Luo1,2 and Hui Shi1,* Plants must adjust their growth and development adaptively in response to light. Four recent studies have now established novel paradigms connecting light and hormone signaling pathways, in which photoreceptors adopt three modes to directly inhibit internal hormonal responses to external stimuli. As sessile organisms, plants are equipped with the capacity to sense environmental information and adjust their growth and development accordingly. Light is one of the most important environmental factors, and exposure to light widely and profoundly regulates plant developmental processes (known as photomorphogenesis) [1]. To precisely sense the light signal, plants employ a series of photoreceptors across the spectrum of light. The red/far-red light (600– 750 nm) receptors are members of phytochrome family, which contains five members (phyA to phyE) in arabidopsis (Arabidopsis thaliana) [2]. Cryptochromes, phototropins, and the ZEITLUPE family members sense the blue light (350–500 nm) [2]. UVR8 (UV RESISTANCE LOCUS 8) is the UV-B light (275– 320 nm) receptor for UV-B responses [2]. Plants track the status of their light environment, transduce the signals to the nucleus, and ultimately direct gene expression changes to induce light responses. Without developing a nervous system, plants have evolved phytohormones which act as internal chemical messengers for multicellular communication and coordinating plant growth and
development in adaptation to various ethylene signaling pathway, is rapidly environmental conditions [3]. degraded within 30 minutes. Photoactivated phyB, EIN3, and the two F-box In the past decade the molecular interac- proteins of the EIN3 E3 ligase SCFEBF1/2 tions between light and phytohormone form a tripartite protein complex. Among pathways have been extensively investi- them, phyB interacts with EIN3 in a red gated [1]. Previous studies revealed that light-dependent manner, but physically light modulates the metabolism and sig- associates with SCFEBF1/2. With red light naling transduction of phytohormones via activation, phyB acts as the ‘molecular key transcription factors and/or regula- glue’, directly enhancing the EIN3– tors. For example, PHYTOCHROME- SCFEBF1/2 interaction and thus promoting INTERACTING FACTORs (PIFs) target EIN3 protein degradation [7]. This mechand regulate expression of the genes anism enables a primary control of the responsible for hormone biosynthesis, ethylene signaling pathway upon the initial metabolism, and signal transduction [1]. light exposure during seedling emergence Key transcription factors of light and phy- from the soil, and this sheds light on the tohormone signaling pathways, such as integrating roles of photoreceptors in PIF3 and ETHYLENE-INSENSITIVE 3 light–hormone crosstalk. (EIN3) (light and ethylene), and PIF4 and BRASSINAZOLE-RESISTANT 1 (BZR1) Subsequently, two recent studies dem(light and brassinosteroids, BRs), have onstrated that photoreceptors directly been shown to form molecular modules modulate auxin responses [8,9]. Typical and act as integrators of light and hor- auxin signaling pathway consists of F-box mone signals [4,5]. Remarkably, four protein TIR1, core repressors AUX/IAAs, recent studies have revealed that light and transcription factors AUXIN and hormone signaling pathways seem RESPONSE FACTORS (ARFs). Auxin is to be integrated at the photoreceptor perceived by receptor TIR1 that promotes level, providing a novel molecular frame- the assembly of the TIR1–AUX/IAA prowork for how plants transduce external tein complex to degrade AUX/IAA prolight information to direct internal hor- teins and initiate auxin-responsive gene monal responses. expression. Xu et al. found that the blue light receptor CRY1 directly interacts with Buried seedlings grow upwards in dark- AUX/IAA in a blue light-dependent manness and push against the mechanical ner [8]. Moreover, CRY1 interacts with the barrier of soil. Upon emerging from the N-terminal domain of AUX/IAA, which is soil, seedlings are exposed to light irradi- responsible for the interaction between ation and are released from mechanical TIR1 and AUX/IAA. In vitro and in vivo pressure. Previous studies showed that assays showed that CRY1 interferes with buried seedlings produce ethylene quan- the formation of the AUX/IAA–TIR1 protitatively in response to mechanical pres- tein complex, thus repressing auxinsure. It has therefore been proposed that induced AUX/IAA degradation. Taken light and ethylene signaling pathways are together, Xu et al. propose a novel antagtightly integrated with each other during onistic module, CRY1–AUX/IAA–TIR1, in seedling emergence [6]. Extensive bio- which blue light induces CRY1–AUX/IAA chemical evidence has dissected the interaction to interfere with the associamolecular actions of phyB in mediating tion and subsequent degradation of AUX/ red light-inhibited ethylene responses IAA by TIR1 [8]. Interestingly, phyA and [7]. Upon light exposure, EIN3 protein, phyB adopt similar mechanisms to prothe master transcription factor of the tect AUX/IAA in shade avoidance and red
Trends in Plant Science, Month Year, Vol. xx, No. yy
1
TRPLSC 1755 No. of Pages 3
UVB
Blue
UVR8
CRY1
Red Far-red
phyA/phyB phyA Photoreceptors
UVR8/CRY1 Nucleus CRY1 UVR8 BIM1/BES1
C
C N N
BIM1/BES1
Light spectrum
CRY1/phyA/phyB CRY1 C
C
Nucleus phyA/phyB SCFTIR1
N N
AUX/IAA ARFs
phyB Nucleus phyB
SCFEBF1/2 EIN3
AUX/IAA ARFs
BR-responsive genes
Auxin-responsive genes
SequestraƟon
Interference
Ethylene-responsive genes
Molecular glue
Figure 1. Photoreceptors Directly Connect Light and Hormone Signaling Pathways in Three Ways. (i) Sequestration: UV-B photoreceptor UVR8 and blue light receptor CRY1 associate with BIM1/BES1 to directly sequester the DNA-binding activities of BES1/BIM1 in brassinosteroid (BR) responses. (ii) Interference: blue light receptor CRY1, and red and far-red light receptors phyA and phyB, directly interact with AUX/IAA, competitively interfering with the association and degradation of AUX/IAA by their E3 ligase SCFTIR1. ARF-mediated auxin responses are then inhibited. (iii) Molecular glue: red light receptor phyB acts as a light-controlled molecular glue to promote EIN3 degradation via enhancing the interaction between EIN3 and its E3 ligase SCFEBF1/EBF2, rapidly turning off ethylene responses.
light conditions, respectively, suggesting that the photoreceptor–AUX/IAA–TIR1 module is a general machinery that allows direct regulation of the auxin signaling pathway by diverse light conditions [8,9]. In contrast to ethylene and auxin signaling, BR responses are inhibited by UV-B photoreceptor UVR8 or blue light receptor CRY1 via sequestration [10,11]. By using yeast two-hybrid screening, the transcription factors of BR signaling, BIM1 and BES1, were identified as UVR8-interacting proteins. UV-B-activated nuclear UVR8 affects neither the gene expression nor protein levels of BIM1/BES1, but it sequesters the DNA-binding activity of BIM1/ BES1 to shut down BR signaling pathway [10]. Similar to UVR8, CRY1 specifically 2
Trends in Plant Science, Month Year, Vol. xx, No. yy
interacts with the biologically active form of BES1 protein (the dephosphorylated BES1) and thus sequesters the BES1 DNA-binding activity [11]. Interestingly, the CRY1–BES1 interaction occurs in a blue light-dependent manner. However, the interactions between UVR8 and BIM1/BES1 are independent of UV-B. UV-B increases the protein abundance of UVR8 in the nucleus, resulting in increased levels of the UVR8–BES1/BIM1 protein complex [10,11].
Concluding Remarks and Perspectives The reports highlighted here together illustrate that photoreceptors directly integrate light and hormone signaling pathways. For the ethylene signaling pathway, the red
light photoreceptor phyB promotes the interaction between EIN3 and its E3 ligase SCFEBF1/2 in a light-dependent way, stimulating rapid degradation of EIN3 proteins [7]. For the auxin signaling pathway, photoactivated CRY1, phyA, and phyB interact with AUX/IAA, interfere the AUX/IAA– TIR1 interactions, and thus inhibit auxininduced AUX/IAA protein degradation [8,9]. For the BR signaling pathway, the photoreceptors CRY1 and UVR8 directly interact with BIM1/BES1, sequestering their DNA-binding activity and repressing downstream responses [10,11]. These reports not only propose exciting modes of action of photoreceptors but have also established the early integration events of light and hormone signaling pathways (Figure 1).
TRPLSC 1755 No. of Pages 3
Being sessile, plants adopt a highly developed strategy to optimize their growth and development according to the changing environment. As mentioned above, research in the past few years has revealed the multiple-level integration of light and hormone signaling pathways. First, light regulates the expression of genes involved in hormone biosynthesis or responses. Second, transcription factor modules integrate light and hormone signaling pathways via transcription cascades or protein–protein interactions. The photoreceptor-integrated mechanisms reported here reveal more direct signal transduction from external factors to modify internal responses. It will be necessary to elucidate further the relationships between these multiple levels of integration and reveal their biological significance in the diverse and dynamic light environment. For example, red light irradiation rapidly represses the expression of several AUX/IAA genes, probably through direct regulation targeted by PIF proteins [12]. Therefore, light stabilizes AUX/IAA protein accumulation via interaction with photoreceptors, but
decreases the expression of AUX/IAA genes, likely depending on PIFs. The opposing effects of light on AUX/IAA protein stability and gene transcription might constitute a negative feedback circuit to fine-tune auxin responses upon light. In addition, whether lightregulated hormone responses are tissue- or organ-specific needs to be explored. Dissecting their regulation specifically in cotyledons, hypocotyls, and roots would greatly improve our understanding of photomorphogenesis. Acknowledgments We thank Dr Shangwei Zhong for comments. This work was supported by the National Science Foundation of China (grant 31770208 to H.S.). 1
College of Life Sciences, Capital Normal University, Beijing 100048, China
2
State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China *Correspondence: [email protected] (H. Shi). https://doi.org/10.1016/j.tplants.2018.11.002
2. Galvao, V.C. and Fankhauser, C. (2015) Sensing the light environment in plants: photoreceptors and early signaling steps. Curr. Opin. Neurobiol. 34, 46–53 3. Chaiwanon, J. et al. (2016) Information integration and communication in plant growth regulation. Cell 164, 1257–1268 4. Liu, X. et al. (2017) EIN3 and PIF3 form an interdependent module that represses chloroplast development in buried seedlings. Plant Cell 29, 3051–3067 5. Oh, E. et al. (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802–809 6. Zhong, S. et al. (2014) Ethylene-orchestrated circuitry coordinates a seedling's response to soil cover and etiolated growth. Proc. Natl. Acad. Sci. U. S. A. 111, 3913– 3920 7. Shi, H. et al. (2016) The red light receptor phytochrome B directly enhances substrate–E3 ligase interactions to attenuate ethylene responses. Dev. Cell 39, 597–610 8. Xu, F. et al. (2018) Photoactivated CRY1 and phyB interact directly with AUX/IAA proteins to inhibit auxin signaling in Arabidopsis. Mol. Plant 11, 523–541 9. Yang, C. et al. (2018) Phytochrome A negatively regulates the shade avoidance response by increasing auxin/indole acidic acid protein stability. Dev. Cell 44, 29–41 10. Liang, T. et al. (2018) UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Dev. Cell 44, 512–523 11. Wang, W. et al. (2018) Photoexcited CRYPTOCHROME1 interacts with dephosphorylated BES1 to regulate brassinosteroid signaling and photomorphogenesis in Arabidopsis. Plant Cell 30, 1989–2005 12. Leivar, P. et al. (2012) Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24, 1398–1419
References 1. de Wit, M. et al. (2016) Light-mediated hormonal regulation of plant growth and development. Annu. Rev. Plant Biol. 67, 513–537
Trends in Plant Science, Month Year, Vol. xx, No. yy
3