Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities.
Arabidopsis
/ metabolism
Arabidopsis Proteins
/ metabolism
Cell Nucleus Structures
/ metabolism
Cotyledon
/ cytology
Gene Expression Regulation, Plant
Hypocotyl
/ cytology
Light
Photoreceptor Cells
/ metabolism
Phytochrome B
/ metabolism
Plant Cells
/ metabolism
Plant Epidermis
/ metabolism
Signal Transduction
Temperature
Transcription Factors
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
03 04 2020
03 04 2020
Historique:
received:
05
10
2019
accepted:
10
03
2020
entrez:
5
4
2020
pubmed:
5
4
2020
medline:
24
7
2020
Statut:
epublish
Résumé
Warm temperature is postulated to induce plant thermomorphogenesis through a signaling mechanism similar to shade, as both destabilize the active form of the photoreceptor and thermosensor phytochrome B (phyB). At the cellular level, shade antagonizes phyB signaling by triggering phyB disassembly from photobodies. Here we report temperature-dependent photobody localization of fluorescent protein-tagged phyB (phyB-FP) in the epidermal cells of Arabidopsis hypocotyl and cotyledon. Our results demonstrate that warm temperature elicits different photobody dynamics than those by shade. Increases in temperature from 12 °C to 27 °C incrementally reduce photobody number by stimulating phyB-FP disassembly from selective thermo-unstable photobodies. The thermostability of photobodies relies on phyB's photosensory module. Surprisingly, elevated temperatures inflict opposite effects on phyB's functions in the hypocotyl and cotyledon despite inducing similar photobody dynamics, indicative of tissue/organ-specific temperature signaling circuitry either downstream of photobody dynamics or independent of phyB. Our results thus provide direct cell biology evidence supporting an early temperature signaling mechanism via dynamic assembly/disassembly of individual photobodies possessing distinct thermostabilities.
Identifiants
pubmed: 32245953
doi: 10.1038/s41467-020-15526-z
pii: 10.1038/s41467-020-15526-z
pmc: PMC7125078
doi:
Substances chimiques
Arabidopsis Proteins
0
PHYB protein, Arabidopsis
0
Transcription Factors
0
Phytochrome B
136250-22-1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1660Subventions
Organisme : NIH HHS
ID : S10 OD016290
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM087388
Pays : United States
Commentaires et corrections
Type : ErratumIn
Title corrected
Références
Chinnusamy, V., Zhu, J. & Zhu, J.-K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444–451 (2007).
pubmed: 17855156
Shi, Y., Ding, Y. & Yang, S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 23, 623–637 (2018).
pubmed: 29735429
Ohama, N., Sato, H., Shinozaki, K. & Yamaguchi-Shinozaki, K. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 22, 53–65 (2017).
pubmed: 27666516
Wigge, P. A. Ambient temperature signalling in plants. Curr. Opin. Plant Biol. 16, 661–666 (2013).
pubmed: 24021869
Koini, M. A. et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413 (2009).
pubmed: 19249207
Crawford, A. J., McLachlan, D. H., Hetherington, A. M. & Franklin, K. A. High temperature exposure increases plant cooling capacity. Curr. Biol. 22, R396–R397 (2012).
pubmed: 22625853
Blázquez, M. A., Ahn, J. H. & Weigel, D. A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat. Genet. 33, 168–171 (2003).
pubmed: 12548286
Kumar, S. V. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245 (2012).
pubmed: 22437497
pmcid: 4972390
Lau, O. S. et al. Direct control of SPEECHLESS by PIF4 in the high-temperature response of stomatal development. Curr. Biol. 28, 1273–1280.e3 (2018).
pubmed: 29628371
pmcid: 5931714
Gangappa, S. N., Berriri, S. & Kumar, S. V. PIF4 coordinates thermosensory growth and immunity in Arabidopsis. Curr. Biol. 27, 243–249 (2017).
pubmed: 28041792
pmcid: 5266789
Huot, B. et al. Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. Nat. Commun. 8, 1808 (2017).
pubmed: 29180698
pmcid: 5704021
Hua, J. Modulation of plant immunity by light, circadian rhythm, and temperature. Curr. Opin. Plant Biol. 16, 406–413 (2013).
pubmed: 23856082
Quint, M. et al. Molecular and genetic control of plant thermomorphogenesis. Nat. Plants 2, 15190 (2016).
pubmed: 27250752
Casal, J. J. & Balasubramanian, S. Thermomorphogenesis. Annu. Rev. Plant Biol. 70, 321–346 (2019).
pubmed: 30786235
Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692 (2010).
pubmed: 20970368
Schlenker, W. & Roberts, M. J. Nonlinear temperature effects indicate severe damages to US crop yields under climate change. Proc. Natl Acad. Sci. USA 106, 15594–15598 (2009).
pubmed: 19717432
Bailey-Serres, J., Parker, J. E., Ainsworth, E. A., Oldroyd, G. E. D. & Schroeder, J. I. Genetic strategies for improving crop yields. Nature 575, 109–118 (2019).
pubmed: 31695205
pmcid: 7024682
Legris, M. et al. Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900 (2016).
pubmed: 27789798
Jung, J.-H. et al. Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889 (2016).
pubmed: 27789797
Rockwell, N. C., Su, Y. S. & Lagarias, J. C. Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57, 837–858 (2006).
pubmed: 16669784
pmcid: 2664748
Burgie, E. S. & Vierstra, R. D. Phytochromes: an atomic perspective on photoactivation and signaling. Plant Cell 26, 4568–4583 (2014).
pubmed: 25480369
pmcid: 4311201
Rockwell, N. C. & Lagarias, J. C. Phytochrome evolution in 3D: deletion, duplication, and diversification. New Phytol. 225, 2283–2300 (2020).
pubmed: 31595505
Franklin, K. A. & Whitelam, G. C. Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat. Genet. 39, 1410–1413 (2007).
pubmed: 17965713
Ballaré, C. L. & Pierik, R. The shade-avoidance syndrome: multiple signals and ecological consequences. Plant Cell Environ. 40, 2530–2543 (2017).
pubmed: 28102548
Legris, M., Ince, Y. Ç. & Fankhauser, C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 10, 5219 (2019).
pubmed: 31745087
pmcid: 6864062
Nagy, F. & Schafer, E. Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants. Annu. Rev. Plant Biol. 53, 329–355 (2002).
pubmed: 12221979
Klose, C., Nagy, F. & Schafer, E. Thermal reversion of plant phytochromes, Mol. Plant 13, 386–397 (2020).
pubmed: 31812690
Chen, M. & Chory, J. Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21, 664–671 (2011).
pubmed: 21852137
pmcid: 3205231
Neff, M. M. & Van Volkenburgh, E. Light-stimulated cotyledon expansion in Arabidopsis seedlings (The role of phytochrome B.). Plant Physiol. 104, 1027–1032 (1994).
pubmed: 12232145
pmcid: 160701
Reed, J. W., Nagpal, P., Poole, D. S., Furuya, M. & Chory, J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147–157 (1993).
pubmed: 8453299
pmcid: 160258
Gray, W. M., Ostin, A., Sandberg, G., Romano, C. P. & Estelle, M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7197–7202 (1998).
pubmed: 9618562
Paik, I., Kathare, P. K., Kim, J.-I. & Huq, E. Expanding roles of PIFs in signal integration from multiple processes. Mol. Plant 10, 1035–1046 (2017).
pubmed: 28711729
pmcid: 5551451
Procko, C., Crenshaw, C. M., Ljung, K., Noel, J. P. & Chory, J. Cotyledon-generated auxin is required for shade-induced hypocotyl growth in Brassica rapa. Plant Physiol. 165, 1285–1301 (2014).
pubmed: 24891610
pmcid: 4081337
Fankhauser, C. & Chen, M. Transposing phytochrome into the nucleus. Trends Plant Sci. 13, 596–601 (2008).
pubmed: 18824397
Van Buskirk, E. K., Decker, P. V. & Chen, M. Photobodies in light signaling. Plant Physiol. 158, 52–60 (2012).
pubmed: 21951469
Yamaguchi, R., Nakamura, M., Mochizuki, N., Kay, S. A. & Nagatani, A. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J. Cell Biol. 145, 437–445 (1999).
pubmed: 10225946
pmcid: 2185089
Kircher, S. et al. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 11, 1445–1456 (1999).
pubmed: 10449579
pmcid: 144301
Bauer, D. et al. 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 (2004).
pubmed: 15155879
pmcid: 490037
Van Buskirk, E. K., Reddy, A. K., Nagatani, A. & Chen, M. Photobody localization of phytochrome B is tightly correlated with prolonged and light-dependent inhibition of hypocotyl elongation in the dark. Plant Physiol. 165, 595–607 (2014).
pubmed: 24769533
pmcid: 4044834
Chen, M., Schwab, R. & Chory, J. Characterization of the requirements for localization of phytochrome B to nuclear bodies. Proc. Natl Acad. Sci. USA 100, 14493–14498 (2003).
pubmed: 14612575
Rausenberger, J. et al. An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS ONE 5, e10721 (2010).
pubmed: 20502669
pmcid: 2873432
Kircher, S. et al. Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14, 1541–1555 (2002).
pubmed: 12119373
pmcid: 150705
Klose, C. et al. Systematic analysis of how phytochrome B dimerization determines its specificity. Nat. Plants 1, 15090 (2015).
pubmed: 27250256
Chen, M. et al. Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141, 1230–1240 (2010).
pubmed: 20603003
pmcid: 2935685
Trupkin, S. A., Legris, M., Buchovsky, A. S., Rivero, M. B. T. & Casal, J. J. Phytochrome B nuclear bodies respond to the low red to far-red ratio and to the reduced irradiance of canopy shade in Arabidopsis. Plant Physiol. 165, 1698–1708 (2014).
pubmed: 24948827
pmcid: 4119049
Qiu, Y. et al. Mechanism of early light signaling by the carboxy-terminal output module of Arabidopsis phytochrome B. Nat. Commun. 8, 1905 (2017).
pubmed: 29199270
pmcid: 5712524
Yoo, C. et al. Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat. Commun. 10, 2629 (2019).
pubmed: 31201355
pmcid: 6570650
Yang, E. J. et al. NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches. Nat. Commun. 10, 2630 (2019).
pubmed: 31201314
pmcid: 6570768
Kaiserli, E. et al. Integration of light and photoperiodic signaling in transcriptional nuclear foci. Dev. Cell 35, 311–321 (2015).
pubmed: 26555051
pmcid: 4654455
Huang, H. et al. PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis. Proc. Natl Acad. Sci. USA 116, 8603–8608 (2019).
pubmed: 30948632
Huang, H. et al. PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis. Elife 5, e13292 (2016).
pubmed: 26839287
pmcid: 4755757
Enderle, B. et al. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nat. Commun. 8, 2221 (2017).
pubmed: 29263319
pmcid: 5738371
Su, Y.-S. & Lagarias, J. C. Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell 19, 2124–2139 (2007).
pubmed: 17660358
pmcid: 1955707
Matsushita, T., Mochizuki, N. & Nagatani, A. Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424, 571–574 (2003).
pubmed: 12891362
Chen, M., Tao, Y., Lim, J., Shaw, A. & Chory, J. Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals. Curr. Biol. 15, 637–642 (2005).
pubmed: 15823535
Qiu, Y., Li, M., Kim, R. J.-A., Moore, C. M. & Chen, M. Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA. Nat. Commun. 10, 140 (2019).
pubmed: 30635559
pmcid: 6329817
Blum, D. E., Neff, M. M. & Van Volkenburgh, E. Light-stimulated cotyledon expansion in the blu3 and hy4 mutants of Arabidopsis thaliana. Plant Physiol. 105, 1433–1436 (1994).
pubmed: 7972499
pmcid: 159477
Yoo, C. Y., Williams, D. & Chen, M. Quantitative analysis of photobodies. Methods Mol. Biol. 2026, 135–141 (2019).
pubmed: 31317408
Grima, R. et al. Insight into nuclear body formation of phytochromes through stochastic modelling and experiment. Phys. Biol. 15, 056003 (2018).
pubmed: 29714708
Sharrock, R. A. & Clack, T. Heterodimerization of type II phytochromes in Arabidopsis. Proc. Natl Acad. Sci. USA 101, 11500–11505 (2004).
pubmed: 15273290
Liu, P. & Sharrock, R. A. Directed dimerization: an in vivo expression system for functional studies of type II phytochromes. Plant J. 75, 915–926 (2013).
pubmed: 23738620
Fischer, A. J. & Lagarias, J. C. Harnessing phytochrome’s glowing potential. Proc. Natl Acad. Sci. USA 101, 17334–17339 (2004).
pubmed: 15548612
Fischer, A. J. et al. Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes. Biochemistry 44, 15203–15215 (2005).
pubmed: 16285723
pmcid: 1343512
Hu, W., Su, Y. S. & Lagarias, J. C. A light-independent allele of phytochrome B faithfully recapitulates photomorphogenic transcriptional networks. Mol. Plant 2, 166–182 (2009).
pubmed: 19529817
Galvao, R. M. et al. Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis. Genes Dev. 26, 1851–1863 (2012).
pubmed: 22895253
pmcid: 3426763
Feng, C. M., Qiu, Y., Van Buskirk, E. K., Yang, E. J. & Chen, M. Light-regulated gene repositioning in Arabidopsis. Nat. Commun. 5, 3027 (2014).
pubmed: 24390011
pmcid: 4136543
Ni, W. et al. A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science 344, 1160–1164 (2014).
pubmed: 24904166
pmcid: 4414656
Sun, N. et al. Arabidopsis SAURs are critical for differential light regulation of the development of various organs. Proc. Natl Acad. Sci. USA 113, 6071–6076 (2016).
pubmed: 27118848
Johansson, H. et al. Arabidopsis cell expansion is controlled by a photothermal switch. Nat. Commun. 5, 4848 (2014).
pubmed: 25258215
pmcid: 4200516
Medzihradszky, M. et al. Phosphorylation of phytochrome B inhibits light-induced signaling via accelerated dark reversion in Arabidopsis. Plant Cell 25, 535–544 (2013).
pubmed: 23378619
pmcid: 3608776
Nito, K., Wong, C. C. L., Yates, J. R. 3rd & Chory, J. Tyrosine phosphorylation regulates the activity of phytochrome photoreceptors. Cell Rep. 3, 1970–1979 (2013).
pubmed: 23746445
pmcid: 4023694
Viczián, A. et al. Differential phosphorylation of the N-terminal extension regulates phytochrome B signaling. New Phytol. 42, 606–617 (2019).
Sweere, U. et al. Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294, 1108–1111 (2001).
pubmed: 11691995