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Photoreceptor Signaling Networks in Plant Responses to Shade
Open accessAbstract
The dynamic light environment of vegetation canopies is perceived by phytochromes, cryptochromes, phototropins, and UV RESISTANCE LOCUS 8 (UVR8). These receptors control avoidance responses to preclude exposure to limiting or excessive light and acclimation responses to cope with conditions that cannot be avoided. The low red/far-red ratios of shade light reduce phytochrome B activity, which allows PHYTOCHROME INTERACTING FACTORS (PIFs) to directly activate the transcription of auxin-synthesis genes, leading to shade-avoidance responses. Direct PIF interaction with DELLA proteins links gibberellin and brassinosteroid signaling to shade avoidance. Shade avoidance also requires CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1), a target of cryptochromes, phytochromes, and UVR8. Multiple regulatory loops and the input of the circadian clock create a complex network able to respond even to subtle threats of competition with neighbors while still compensating for major environmental fluctuations such as the day-night cycles.
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“Plants quantify this ratio through the phytochrome system and react with the shade avoidance syndrome that enables plants to outgrow the competitors for light (Casal, 2013; Pierik and de Wit, 2014).”
From Shaping plant architecture (2015) · cites this paper as Casal, 2013
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Self-citationA perspective on ecologically relevant plant-UV research and its practical application
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Shade Avoidance Components and Pathways in Adult Plants Revealed by Phenotypic Profiling
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Jeong, J., & Choi, G. (2013) · Molecules and Cells · doi:10.1007/s10059-013-0135-5 · Cited by 94
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“The cop1 and spa1 spa2 spa4 mutants fail to respond with enhanced stem growth to the reduced phyB activity caused by a pulse of far-red light before the night or low daytime red/far-red ratios, and to the reduced cryptochrome and phyB activity caused by shade (McNellis et al., 1994; Crocco et al., 2010; Rolauffs et al…”
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Su, J., Liu, B., Liao, J., Yang, Z., Lin, C., & Oka, Y. (2017) · Agronomy · doi:10.3390/agronomy7010025 · Cited by 93
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Wilde, A., & Mullineaux, C. W. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux045 · Cited by 93
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BackgroundCompeting neighbors: light perception and root function
Gundel, P. E., Pierik, R., Mommer, L., & Ballaré, C. L. (2014) · Oecologia · doi:10.1007/s00442-014-2983-x · Cited by 90
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Blanco‐Touriñán, N., Serrano-Mislata, A., & Alabadı́, D. (2020) · Plant and Cell Physiology · doi:10.1093/pcp/pcaa113 · Cited by 91
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BackgroundChemically Mediated Plant–Plant Interactions: Allelopathy and Allelobiosis
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“This alteration influences the synthesis and transport of auxins, triggering shade responses in plants, such as stem elongation, adjustment of leaf angle, and modulation of flowering time [100,101], and consequently, the outcomes of aboveground interactions among plants.”
BackgroundSupplemental blue and red light promote lycopene synthesis in tomato fruits
Xie, B., Jing-jing, W. E. I., ZHANG, Y.-T., Song, S., Su, W., Sun, G., Hao, Y., & Liu, H. (2019) · Journal of Integrative Agriculture · doi:10.1016/s2095-3119(18)62062-3 · Cited by 87
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Self-citationCorrelating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4
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“Modern agriculture relies on high planting densities of photosynthetic plants, but such densities cause competition among individual plants for light and trigger the shade avoidance response, reducing overall crop yield (2).”
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InfluentialSelf-citationConserved Phenylalanine Residues Are Required for Blue-Shifting of Cyanobacteriochrome Photoproducts
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“Shade signaling is mainly regulated by phyB (Franklin and 119 Whitelam, 2005; Martinez-Garcia et al., 2010; Casal, 2013).”
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“Photosynthetic organisms have developed direct and indirect mechanisms for sensing and responding to limiting or excess light (Li et al., 2009; Casal, 2013).”
BackgroundMethodInfluentialMulti-layered roles of BBX proteins in plant growth and development
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“Besides stem elongation, shade avoidance also evokes a suite of adaptive responses including reduced branching, hyponastic leaf orientation, early flowering, and accelerated senescence (Casal 2013; Pierik and de Wit 2014).”
BackgroundLED Lighting: A Grower’s Guide to Light Spectra
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“Research has shown that four Aux/IAA-ARF combinations, known as auxin signaling modules, are related to different stages of lateral root growth [137].”
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“The affected gene codes for ELONGATED HYPOCOTYL5 (HY5), which is a basic domain/leucine zipper (bZIP) transcription factor that works downstream of several families of light receptors (Koornneef et al. 1980; Oyama et al. 1997; Ang et al. 1998; Chattopadhyay et al. 1998; Li et al. 2010; Casal 2013).”
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BackgroundInfluentialShedding (far-red) light on phytochrome mechanisms and responses in land plants
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“This view has, however, been challenged by a growing body of evidence supporting the idea that signalling networks rather than resource allocation coordinate this balance to optimize fitness (Casal, 2013; Kliebenstein, 2016; de Vries et al., 2017; Guo et al., 2018).”
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“phyB is the main photoreceptor with two different activation states (36).”
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Light-mediated self-organization of sunflower stands increases oil yield in the field
Pereira, M. L., Sadras, V. O., Batista, W. B., Casal, J. J., & Hall, A. J. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618990114 · Cited by 73
“For instance, mutual shading in dense stands reduces the activity of photosensory receptors such as phytochromes and cryptochromes (14, 15).”
BackgroundSelf-citationCOP1 regulates plant growth and development in response to light at the post-translational level
Kim, J. Y., Song, J. T., & Seo, H. S. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx312 · Cited by 72
Blum, A. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert289 · Cited by 71
“These signals as sensed and modulated by the phytochrome complex are crucial in regulating plant response to crowding in terms of plant morphology and function (e.g. Smith, 2000; Sawers et al., 2005; Carvalho et al., 2011; Casal 2013a, b).”
BackgroundMeng, Y., Shuai, H., Luo, X., Chen, F., Zhou, W., Yang, W., & Shu, K. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2016.02021 · Cited by 72
Translational regulation in chloroplasts for development and homeostasis
Sun, Y., & Zerges, W. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.008 · Cited by 70
Differential Sensitivity of Fruit Pigmentation to Ultraviolet Light between Two Peach Cultivars
Zhao, Y., Dong, W., Wang, K., Zhang, B., Allan, A. C., Lin‐Wang, K., Chen, K., & Xu, C. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01552 · Cited by 69
“Light photoreceptors include four groups: PHYs, CRY, PHOTs, and UVR8 (Rizzini et al., 2011; Casal, 2013).”
BackgroundMultiple Pathways in the Control of the Shade Avoidance Response
Sessa, G., Carabelli, M., Possenti, M., Morelli, G., & Ruberti, I. (2018) · Plants · doi:10.3390/plants7040102 · Cited by 68
“phyB–E are all relatively stable in the Pfr form [5,10,12].”
BackgroundInfluentialPhytochromes and Other (Photo)Receptors of Information in Plants
Voitsekhovskaja, O. V. (2019) · Russian Journal of Plant Physiology · doi:10.1134/s1021443719030154 · Cited by 67
“Furthermore, DELLA and PIFs directly bind BZR1, the regulator of brassinosteroid-responsive genes [13].”
BackgroundInfluentialThe Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation
Simon, N. M. L., Kusakina, J., Fernández-López, Á., Chembath, A., Belbin, F. E., & Dodd, A. N. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.01395 · Cited by 67
“Examples of signals that adjust hypocotyl elongation include phytochrome-mediated signals concerning the ratio of red to far red light (Casal, 2013), blue light (Liscum and Hangarter, 1991), UV-B light (Kim et al., 1998; Hayes et al., 2014), temperature (Koini et al., 2009; Wigge, 2013; Mizuno et…”
BackgroundFunctional Characterization of the Maize Phytochrome-Interacting Factors PIF4 and PIF5
Shi, Q., Zhang, H., Song, X., Jiang, Y., Liang, R., & Li, G. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2017.02273 · Cited by 67
“Shade avoidance is mainly triggered by the reduced ratio of R:FR, which is sensed by the phytochrome family of photoreceptors (Franklin et al., 2003; Casal, 2013).”
Canopy Light Quality Modulates Stress Responses in Plants
Courbier, S., & Pierik, R. (2019) · iScience · doi:10.1016/j.isci.2019.11.035 · Cited by 67
“Plants employ a suite of developmental adjustments to increase their competitive ability, known as the ‘‘shade avoidance syndrome (SAS)’’ (Ballaré and Pierik, 2017; Casal, 2013).”
BackgroundInfluentialYoosefzadeh-Najafabadi, M., Torabi, S., Torkamaneh, D., Tulpan, D., Rajcan, I., & Eskandari, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105538 · Cited by 75
“In addition, PHYB is inactivated after imbibition shade signals, which repress PHYA-dependent signaling in the embryo that results in the maturity of seeds by preventing germination (Casal 2013; De Wit et al. 2016).”
BackgroundMeng, Y., Chen, F., Shuai, H., Luo, X., Ding, J., Tang, S., Xu, S., Liu, J., Liu, W., Du, J., et al. (2016) · Scientific Reports · doi:10.1038/srep22073 · Cited by 66
Developmental mechanisms underlying variable, invariant and plastic phenotypes
Abley, K., Locke, J. C. W., & Leyser, O. (2016) · Annals of Botany · doi:10.1093/aob/mcw016 · Cited by 67
Transcriptome Analysis of Shade-Induced Inhibition on Leaf Size in Relay Intercropped Soybean
Gong, W., Qi, P., Du, J., Sun, X., Wu, X., Song, C. Y., Liu, W., Wu, Y., Yu, X., Yong, T., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098465 · Cited by 65
“Many critical genes involved in IAA regulation under shade have identified on model plant [12].”
BackgroundPossart, A., Xu, T., Paik, I., Hanke, S. T., Keim, S., Hermann, H.-M., Wolf, L., Hiß, M., Becker, C., Huq, E., et al. (2017) · The Plant Cell · doi:10.1105/tpc.16.00388 · Cited by 65
“Moreover, At-PIF4, At-PIF5, and At-PIF7 have been reported to promote the shade avoidance syndrome in deetiolated seedlings, and At-PIF3 andAt-PIF4 regulate flowering time (Leivar andQuail, 2011;Casal, 2013; Leivar andMonte, 2014).”
BackgroundAnnunziata, M. G., Apelt, F., Carillo, P., Krause, U., Feil, R., Koehl, K., Lunn, J. E., & Stitt, M. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/ery276 · Cited by 64
The Red Edge: Bilin-Binding Photoreceptors as Optogenetic Tools and Fluorescence Reporters
Tang, K., Beyer, H. M., Zurbriggen, M. D., & Gärtner, W. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00194 · Cited by 64
Shading of the mother plant during seed development promotes subsequent seed germination in soybean
Chen, F., Zhou, W., Yin, H., Luo, X., Chen, W., Liu, X., Wang, X., Meng, Y., Feng, L., Qin, Y., et al. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz553 · Cited by 63
Rusaczonek, A., Czarnocka, W., Kacprzak, S., Witoń, D., Ślesak, I., Szechyńska‐Hebda, M., Gawroński, P., & Karpiński, S. M. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv375 · Cited by 61
The decision to germinate is regulated by divergent molecular networks in spores and seeds
Vesty, E. F., Saidi, Y., Moody, L. A., Holloway, D., Whitbread, A. L., Needs, S. H., Choudhary, A., Burns, B., McLeod, D., Bradshaw, S. J., et al. (2016) · New Phytologist · doi:10.1111/nph.14018 · Cited by 63
“…via effects on hormone metabolism (and subsequent hormone levels), via transcriptional changes in signalling genes (reviewed in Piskurewicz et al. , 2009), and via interactions between transcription factors from different pathways (e.g. Richter et al. , 2010; Casal, 2013; Tang et al. , 2013).”
The hormonal, metabolic, and environmental regulation of plant shoot branching
Liu, Y., Chen, S., Pal, S., Yu, J., Zhou, Y., Tran, L. P., & Xia, X. (2024) · New Crops · doi:10.1016/j.ncrops.2024.100028 · Cited by 65
Fu, B., Ji, X., Zhao, M., He, F., Wang, X., Yiding, W., Liu, P., & Niu, L. (2016) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2016.07.016 · Cited by 62
Platero, J. S., Leivar, P., & Monte, E. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/ert465 · Cited by 61
Das, D., Onge, K. R. S., Voesenek, L. A. C. J., Pierik, R., & Sasidharan, R. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00725 · Cited by 61
“With energy reserves being invested in escape traits, plants often have lower plant biomass and crop yield (Casal, 2013).”
Silva, T. D., Batista, D. S., Fortini, E. A., de Castro, K. M., Felipe, S. H. S., Fernandes, A. M., Sousa, R. M. D. J., Chagas, K., da Silva, J. V. S., Correia, L. N. F., et al. (2019) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2019.111761 · Cited by 62
González, C. V., Fanzone, M., Cortés, L. E., Bottini, R., Lijavetzky, D., Ballaré, C. L., & Boccalandro, H. E. (2014) · Phytochemistry · doi:10.1016/j.phytochem.2014.11.018 · Cited by 60
Chen, S., Lory, N. C., Stauber, J., & Hoecker, U. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005516 · Cited by 60
“To sense the light, plants have evolved several classes of photoreceptors [1,2].”
BackgroundLight signaling and the phytohormonal regulation of shoot growth
Kurepin, L. V., & Pharis, R. P. (2014) · Plant Science · doi:10.1016/j.plantsci.2014.10.006 · Cited by 59
Soyk, S., Šimková, K., Zürcher, E., Luginbuehl, L. H., Brand, L. H., Vaughan, C. K., Wanke, D., & Zeeman, S. C. (2014) · The Plant Cell · doi:10.1105/tpc.114.123703 · Cited by 59
“These responses are believed to help the plant compete for light to enable photosynthesis (Casal, 2013).”
BackgroundKegge, W., Ninkovic, V., Glinwood, R., Welschen, R. A. M., Voesenek, L. A. C. J., & Pierik, R. (2015) · Annals of Botany · doi:10.1093/aob/mcv036 · Cited by 59
Adjustment of the PIF7‐HFR1 transcriptional module activity controls plant shade adaptation
Paulišić, S., Qin, W., Verasztó, H. A., Then, C., Alary, B., Nogué, F., Tsiantis, M., Hothorn, M., & Martínez‐García, J. F. (2020) · The EMBO Journal · doi:10.15252/embj.2019104273 · Cited by 59
“Shade avoiders usually promote elongation of organs to outgrow the neighbors and avoid light shortages, reduce the levels of photosynthetic pigments to cope to light shortage, and accelerate flowering to ensure species survival (Casal, 2013).”
Zhao, Y., Min, T., Chen, M., Wang, H., Zhu, C., Jin, R., Allan, A. C., Lin‐Wang, K., & Xu, C. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2020.603178 · Cited by 58
“Higher plants have evolved extremely advanced systems to sense changes in ambient light conditions (Casal, 2013), by being equipped with specialized sensory photoreceptors for specific wavelengths of light, including red/far-red light receptor phytochromes (PHYA to PHYE) (Oh and Montgomery, 2017),…”
BackgroundBantis, F. (2021) · Plants · doi:10.3390/plants10102182 · Cited by 58
“cal shade-avoidance responses triggered by phytochrome photoreceptors under certain red/far-red ratios [20].”
Background
Metadata
- Authors
- Casal, J. J.
- Affiliations
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Corresponding author
- Casal, Jorge J.
- ORCID
- Casal, Jorge J.
- Venue
- Annual Review of Plant Biology
- Publisher
- Annual Reviews
- Published
- 2013-04-29
- Volume
- 64
- Issue
- 1
- Pages
- 403-427
- ISSN
- 1543-5008 (ISSN-L)
- 1545-2123
- OpenAlex
- W2107201571
- Cited by
- 865
- References
- 144
- Citations by year
- 2026: 81 · 2025: 66 · 2024: 72 · 2023: 61 · 2022: 79 · 2021: 91 · 2020: 67 · 2019: 60 · 2018: 62 · 2017: 60 · 2016: 58 · 2015: 44 · 2014: 51 · 2013: 13
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- cc-by-nc-nd
- Locations
- Annual Review of Plant Biology (publishedVersion)
- PubMed (publishedVersion)
- CONICET Digital (CONICET) (submittedVersion, cc-by-nc-nd)
- Funders
- Consejo Nacional de Investigaciones Científicas y Técnicas
- Universidad de Buenos Aires (CONICET)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- shade avoidance, photoreceptors, phytochrome, cryptochrome, phototropin, UVR8, phytochrome-interacting factors, DELLA proteins, gibberellin signaling, brassinosteroid signaling, auxin biosynthesis, COP1, circadian clock, red:far-red ratio, plant light signaling, canopy light environment
- MeSH terms
- Gibberellins, Light, Phytochrome, Plant Growth Regulators, Plants, Signal Transduction, Ecosystem, Photoreceptors, Plant
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