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GIGANTEA Integrates Photoperiodic and Temperature Signals to Time when Growth Occurs

2020; Elsevier BV; Volume: 13; Issue: 3 Linguagem: Inglês

10.1016/j.molp.2020.02.008

1674-2052

James Ronald, Kayla McCarthy, Seth J Davis,

Plant Stress Responses and Tolerance

Circadian clocks synchronize internal physiological responses to occur at the most optimal time of the day. In plants, hormone signaling is under the control of this clock. It has been previously shown that the circadian clock moderates the plant's sensitivity to gibberellin (GA) by regulating the expression of GA receptors. Recently, two papers by Nohales and Kay, 2019Nohales M.A. Kay S.A. GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21893-21899Crossref PubMed Scopus (28) Google Scholar and Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar revealed that post-translational regulation of DELLA proteins by the circadian clock also contributes to timing when the plant is most sensitive to GA. The daily rotation of the Earth around the sun generates predictable diurnal changes in light and temperature. Across all domains of life, networks known as circadian clocks have independently evolved. Circadian rhythms are generated either by transcriptional/translational feedback loop(s) or a post-translational mechanism (McClung, 2019McClung R.C. The plant circadian oscillator.Biology. 2019; 8: 14Crossref PubMed Scopus (74) Google Scholar). Circadian clocks regulate the sensitivity of internal responses to daily environmental fluctuations, resulting in adaptable and rhythmic oscillations in physiology. Organisms more in sync with their external environment have been shown to have enhanced fitness. In plants, the circadian clock involves morning and evening expressed genes arranged into a series of interconnected loops (McClung, 2019McClung R.C. The plant circadian oscillator.Biology. 2019; 8: 14Crossref PubMed Scopus (74) Google Scholar). The plant circadian clock plays a regulatory role in nearly all physiological responses, including hormone signaling. It has been shown that the circadian clock regulates components of auxin, jasmonate, brassinosteroids, cytokinin, GA, and abscisic acid (Singh and Mas, 2018Singh M. Mas P. A functional connection between the circadian clock and hormonal timing in Arabidopsis.Genes (Basel). 2018; 9: 567Crossref Scopus (19) Google Scholar). In addition, hormones reciprocally regulate the pace and robustness of circadian rhythms generating, a feedback mechanism that adjusts the activity of the oscillator (Hanano et al., 2006Hanano S. Domagalska M. Nagy F. Davis S. Multiple phytohormones influence distinct parameters of the plant circadian clock.Genes Cells. 2006; 11: 1381-1392Crossref PubMed Scopus (156) Google Scholar). GA has a major role throughout the lifecycle of the plant (Davière and Achard, 2016Davière J.-M. Achard P. A pivotal role of DELLAs in regulating multiple hormone signals.Mol. Plant. 2016; 9: 10-20Abstract Full Text Full Text PDF PubMed Scopus (231) Google Scholar). It was reported that the circadian clock regulates the expression of GA biosynthesis and catabolism enzymes and the expression of the GA receptor GA-INSENSITIVE DWARF1a (GID1a) and GID1b (Blázquez et al., 2002Blázquez M.A. Trénor M. Weigel D. Independent control of gibberellin biosynthesis and flowering time by the circadian clock in Arabidopsis.Plant Physiol. 2002; 130: 1770-1775Crossref PubMed Scopus (62) Google Scholar, Arana et al., 2011Arana M.V. Marín-de la Rosa N. Maloof J.N. Blázquez M.A. Alabadí D. Circadian oscillation of gibberellin signaling in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2011; 108: 9292-9297Crossref PubMed Scopus (105) Google Scholar). The diurnal regulation of GID1a/b was proposed to underpin how the clock controls when GA signaling occurs, a process termed gating. Interesting, Nohales and Kay, 2019Nohales M.A. Kay S.A. GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21893-21899Crossref PubMed Scopus (28) Google Scholar and Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar revealed that a post-translational mechanism also contributes to the gating of GA signaling. GIGANTEA (GI) is a plant-specific protein with no known functional domains. It has been previously shown to be involved in the circadian clock, flowering time, growth, and stress tolerance (Mishra and Panigrahi, 2015Mishra P. Panigrahi K.C. Gigantea – an emerging story.Front. Plant Sci. 2015; 6: 8Crossref PubMed Scopus (106) Google Scholar). GI has multiple proposed functions; the best characterized of these is as a co-chaperone with HEAT SHOCK PROTEIN90 (HSP90) to promote protein maturation and stability (Cha et al., 2017Cha J.-Y. Kim J. Kim T.-S. Zeng Q. Wang L. Lee S.Y. Kim W.-Y. Somers D.E. GIGANTEA is a co-chaperone which facilitates maturation of ZEITLUPE in the Arabidopsis circadian clock.Nat. Commun. 2017; 8: 3Crossref PubMed Scopus (79) Google Scholar). Nohales and Kay, 2019Nohales M.A. Kay S.A. GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21893-21899Crossref PubMed Scopus (28) Google Scholar found that GI could interact with the DELLA proteins REPRESSOR OF GA1-3 (RGA), GIBBERELLIC ACID INSENSITIVE (GAI) and RGA-LIKE PROTEIN3 (RGL3). DELLA proteins are transcriptional regulators that repress the expression of GA responsive genes (Figure 1C ). DELLA proteins interact directly with GA receptors through their DELLA domain, leading to their degradation via the 26S-proteasome pathway (Davière and Achard, 2016Davière J.-M. Achard P. A pivotal role of DELLAs in regulating multiple hormone signals.Mol. Plant. 2016; 9: 10-20Abstract Full Text Full Text PDF PubMed Scopus (231) Google Scholar). Circadian regulation of GID1a/b causes diurnal accumulation of RGA protein, with RGA levels peaking in the mid-afternoon before declining in the evening. Nohales and Kay, 2019Nohales M.A. Kay S.A. GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21893-21899Crossref PubMed Scopus (28) Google Scholar found that the oscillations in RGA were dependent on GI. In the absence of gi, RGA levels remained low and did not oscillate, while the overexpression of GI increased DELLA stability across the night. The binding of GID1a to RGA was disrupted by the presence of GI (Figure 1C), but GI did not bind to the DELLA domain of RGA. Therefore, it is unlikely that GI directly competes with the GID1a-DELLA interaction and instead stabilizes DELLA via a separate, unknown mechanism. As with RGA, GI has diurnal changes in protein accumulation (Figures 1A and 1B). In the evening, GI is degraded by the circadian protein EARLY FLOWERING3 (ELF3) and the E3 ligase CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) (Yu et al., 2008Yu J.W. Rubio V. Lee N.Y. Bai S. Lee S.Y. Kim S.S. Liu L. Zhang Y. Irigoyen M.L. Sullivan J.A. et al.COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability.Mol. Cell. 2008; 32: 617-630Abstract Full Text Full Text PDF PubMed Scopus (278) Google Scholar). The degradation of GI coincides with maximal expression of GID1a/b. Thus, the circadian clock can precisely time when GA signaling occurs through transcriptional and post-translational mechanisms that converge on the stability of DELLA proteins. Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar found the same GI–DELLA interaction is required for gating growth in response to increased temperature. Such warmth initiates a range of physiological changes, including elongated hypocotyls, leaf span, and leaf angle. Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar found the gi-2 mutant had an enhanced thermomorphogenic growth at 28°C compared with wild-type plants. This response was not found to be caused by genes downstream of GI in flowering time, circadian, or stress signaling pathways. The transcription factor PHYTOCHROME INTERACTING FACTOR4 (PIF4) is a central hub for the thermomorphogenic growth (Quint et al., 2016Quint M. Delker C. Franklin K.A. Wigge P.A. Halliday K.J. van Zanten M. Molecular and genetic control of plant thermomorphogenesis.Nat. Plants. 2016; 2: 15190Crossref PubMed Scopus (304) Google Scholar). The gi-2 mutant had increased expression of PIF4 targets, and introducing the pif4-101 mutant into the gi-2 background suppressed the gi-2 thermomorphogenic phenotype (Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar). However, the gi-2 mutant did not have dramatically increased PIF4 transcription. Therefore, it was proposed that GI regulates PIF4 through a post-translational mechanism. A previous study showed that GA promotes thermomorphogenesis by inhibiting DELLA-mediated sequestration and degradation of PIF4 (Quint et al., 2016Quint M. Delker C. Franklin K.A. Wigge P.A. Halliday K.J. van Zanten M. Molecular and genetic control of plant thermomorphogenesis.Nat. Plants. 2016; 2: 15190Crossref PubMed Scopus (304) Google Scholar). As demonstrated by Nohales and Kay, 2019Nohales M.A. Kay S.A. GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21893-21899Crossref PubMed Scopus (28) Google Scholar and Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar GI could interact and stabilize DELLA proteins (Figure 1C). The stabilization of DELLA by GI was not dependent on HSP90, indicating that GI stabilizes DELLA independently of its known chaperone function. Whether GI uses a shared mechanism to stabilize DELLA at ambient and increased temperatures remains to be demonstrated. In the absence of GI stabilizing DELLA, PIF4 protein levels became increased in the night (Figures 1A and 1D), triggering a stronger thermomorphogenic response. The expression and activity of PIF4 is controlled by the circadian clock to precisely time when thermomorphogenesis occurs (Quint et al., 2016Quint M. Delker C. Franklin K.A. Wigge P.A. Halliday K.J. van Zanten M. Molecular and genetic control of plant thermomorphogenesis.Nat. Plants. 2016; 2: 15190Crossref PubMed Scopus (304) Google Scholar). It has been previously shown that under short-day (SD) photoperiods, thermomorphogenesis occurs before dawn (ZT16–24) (Figure 1A), whereas under long days (LD), thermomorphogenesis is shifted to the early morning and midday (ZT4–12) (Figure 1B). The work of Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar revealed that GI confers photoperiodic information and alters the timing of thermomorphogenesis. Increased temperatures during LD nights promoted the stability of GI (Figure 1C), leading to prolonged DELLA activity (Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar). The prolongment of DELLA activity subsequently reduced the activity and stability of PIF4, shifting the thermomorphogenic response from the night into the morning. In the absence of gi, thermomorphogenesis under LD was no longer precisely timed and occurred in both the morning and evening. Under SD, GI protein is relatively unstable at night under short days compared with long days, leading to the pronounced thermomorphogenic growth at night-time under short days (Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar). Therefore, GI integrates photoperiodic and temperature signals to time the initiation of growth by regulating the stability of DELLA. Extensive studies have shown that GI and DELLA are molecular hubs in Arabidopsis, integrating external and internal cues to control an array of processes. The work of Nohales and Kay, 2019Nohales M.A. Kay S.A. GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis.Proc. Natl. Acad. Sci. U S A. 2019; 116: 21893-21899Crossref PubMed Scopus (28) Google Scholar and Park et al., 2020Park Y.-J. Kim J.Y. Lee J.-H. Lee B.-D. Paek N.-C. Park C.-M. GIGANTEA shapes the photoperiodic rhythms of thermomorphogenic growth in Arabidopsis.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.01.003Scopus (26) Google Scholar further revealed that these two molecular hubs are interconnected, with GI stabilizing DELLA proteins. The integration of temporal and thermal sensitivity into GI provides a mechanism to precisely gate growth under ambient and increased temperatures. In both studies, hypocotyl development in Arabidopsis seedlings was used as the output to measure and understand the importance of the GI–DELLA interaction. However, GA has a critical role in many other processes throughout the lifecycle of Arabidopsis as well as in other plants. For example, the induction of flowering time in barley is dependent on GA signaling, with improper accumulation of GA leading to early flowering under non-inductive photoperiods (Boden et al., 2014Boden S.A. Weiss D. Ross J.J. Davies N.W. Trevaskis B. Chandler P.M. Swain S.M. EARLY FLOWERING3 regulates flowering in spring barley by mediating gibberellin production and FLOWERING LOCUS T expression.Plant Cell. 2014; 26: 1557-1569Crossref PubMed Scopus (89) Google Scholar). It is possible that photoperiodic information transmitted through GI to DELLA could contribute to the timing of flowering to occur only under favorable conditions. No conflict of interest declared.