REVIEW ARTICLE https://doi.org/10.1038/s41467-019-13045-0 OPEN Molecular mechanisms underlying phytochrome- controlled morphogenesis in plants Martina Legris1, Yetkin Çaka Ince 1 & Christian Fankhauser 1* Phytochromes are bilin-binding photosensory receptors which control development over a broad range of environmental conditions and throughout the whole plant life cycle. Light- induced conformational changes enable phytochromes to interact with signaling partners, in 1234567890():,; particular transcription factors or proteins that regulate them, resulting in large-scale tran- scriptional reprograming. Phytochromes also regulate promoter usage, mRNA splicing and translation through less defined routes. In this review we summarize our current under- standing of plant phytochrome signaling, emphasizing recent work performed in Arabidopsis. We compare and contrast phytochrome responses and signaling mechanisms among land plants and highlight open questions in phytochrome research. 1 Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015 Lausanne, Switzerland. *email: [email protected] NATURE COMMUNICATIONS | (2019) 10:5219 | https://doi.org/10.1038/s41467-019-13045-0 | www.nature.com/naturecommunications 1 REVIEW ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-13045-0 hytochromes are present in bacteria, cyanobacteria, fungi, absorption maxima, but due to overlapping spectra both con- algae, and land plants, and while in all cases they can formers are always present in the light while only prolonged P 3 perceive light, their photochemical properties vary largely darkness returns all phytochrome to Pr (Fig. 1b) . Given that among phyla1,2. In this review we will focus on land plant phy- phytochrome responses depend on the proportion of Pfr con- tochromes, and in particular on Arabidopsis, for which we have a formers, signaling is influenced by a combination of light quan- better understanding of the underlying molecular mechanisms. In tity, color, and temperature3–5. land plants, phytochromes are red and far-red light receptors that Upon perception of inductive wavelengths, activated phyto- exist in two forms. They are synthesized in the inactive Pr state, chromes together with blue (phototropins, cryptochromes, and which upon light absorption converts to the active Pfr con- Zeitlupes) and UV light receptors (UVR8) control plant phy- formation. Pfr is inactivated upon far-red (FR) light absorption or siology and development6,7. Once the seed is imbibed, active through thermal relaxation, which depends on temperature, a phytochromes promote germination6. When a seedling grows in process known as dark or thermal reversion. Phytochromes act as the soil it adopts an etiolated morphology characterized by fast- dimers, resulting in three possible phytochrome species: Pr–Pr, growing hypocotyls and closed apical hook, which maximizes the Pfr–Pr, and Pfr–Pfr3 (Fig. 1a). Pr and Pfr have different chance to reach the surface. Once it reaches the light, activated phytochromes promote de-etiolation: hypocotyl growth slows a down, the apical hook opens, cotyledons expand, and chloroplasts Photoconversion develop6. This initial response to light occurs even in poor light R R PrPr PfrPr PfrPfr conditions as encountered under deep shade where blue and red FR FR light (R), which are essential for photosynthesis, are scarce6. Unfiltered sunlight has approximately equal amounts of R and FR T T Thermal reversion resulting in a ratio of R to FR (R/FR) slightly above 1 and high phytochrome activity8. However, in environments with high b Dark plant density the R/FR drops since green tissues absorb mainly R 100% Pr and blue light and transmit or reflect FR. This results in reduced Red 87% Pfr phytochrome activity triggering the shade-avoidance response in green seedlings. Stem and petiole elongation are promoted, leaves change their position and anatomy, root architecture is altered, while senescence is promoted8–10. In these conditions, plants Absorption allocate more resources to growing aerial parts11 and change their metabolism12. Increasing temperature promotes similar archi- tectural changes as shade13 and a subset of these temperature responses depend on phytochromes4,5,14. Moreover, phyto- 300 400 500 600 700 800 chromes are important to entrain the circadian clock and for the Wavelength (nm) perception of the photoperiod6,15,16. These signals in addition to fl 6,17–19 c temperature and light quality control owering time . phyA In this review we summarize the current knowledge on early 1.0 phytochrome signaling mechanisms in Arabidopsis with an phyB emphasis on de-etiolation and shade avoidance, the photo- morphogenic processes for which most information is available. 0.6 Other phytochrome-controlled developmental processes are dis- cussed in the context of long-distance signaling. Comparisons between Arabidopsis and other species for which molecular or 0.2 genetic data are available is presented in a separate chapter. Due Rel. photon effectiveness Rel. to space constraints we could not systematically refer to the older primary literature but we suggest more focused review articles 660 680 700 720 740 where historical perspectives can be found. Wavelength (nm) Fig. 1 Control of phytochrome activity. a Factors controlling phytochrome activity. Phytochromes exist in two conformations, Pr and Pfr, the latter The phytochrome family in Arabidopsis being the active form. They exist as dimers so three species can be found. Most land plants possess several phytochromes, and in most Each monomer can be activated by red light (R) and inactivated by far-red angiosperms three groups can be identified: phytochrome A light (FR) or by thermal reversion, a process that depends on temperature (phyA), phyB, and phyC2,20. Arabidopsis has one member in the (T). At least in the case of phyB, Pfr in heterodimers reverts much faster phyA and phyC groups while the phyB class is composed of than that in homodimers, allowing phyB to perceive temperature both phyB, phyD, and phyE6,14,21,22 (Table 1). Each phytochrome has during the day and during the night. b Plant phytochrome absorption different roles and their relative contributions vary depending on spectra of the Pr and Pfr conformations. In dark-adapted seedlings the environmental conditions and developmental stage of the phytochromes are in the Pr form. Upon a saturating R pulse, due to plant (Table 1)14,21–25. Angiosperm phytochromes are further overlapping absorption spectra of Pr and Pfr, only 87% of Pfr is achieved. classified into two categories according to their capacity to trigger c Action spectra for phyA and phyB in the control of hypocotyl elongation. responses to specific light signals. Type I, represented by phyA in Data from Klose et al.3. Fluence rate response curves are measured at Arabidopsis, are light labile and allow germination and de- different wavelengths and fluence rate that leads to 40% inhibition etiolation when light is scarce (Very Low Fluence Response or compared with dark control is determined. In order to specifically VLFR) or when the R/FR is very low (FR-High Irradiance determine action spectra for phyA and phyB, for phyB the curve was Response, FR-HIR)6. Such conditions are encountered under a performed with phyB-GFP/phyAphyB seedlings, and for phyA using phyB-5 thin layer of soil and in deep shade. Type II phytochromes seedlings. Values are relative to the response obtained at the most efficient (phyB–phyE in Arabidopsis) are light stable but require a sub- wavelength in each case stantial fraction of Pfr to promote signaling. Therefore, they are 2 NATURE COMMUNICATIONS | (2019) 10:5219 | https://doi.org/10.1038/s41467-019-13045-0 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-13045-0 REVIEW ARTICLE Table 1 Functional diversification of the phytochrome family in Arabidopsis Phytochrome phyA phyB phyC phyD phyE Type (light IIIIIIIII responses) Class (phylogeny) A B C B B Level in etiolated 85 10 2 1,5 1,5 seedlings26 Level in the light26 540151525 Germination14,25 WLc. WLc Can't promote on its own WLc Poor inducer on its own but VLFR, HIR LFR but can interact Major role in RLc, but can interact synergistically synergistically with other can't respond to Rp with other phytochromes phytochromes Synergy with phyA in FR De-etiolation VLFR, HIR LFR LFR LFR LFR Not sufficient Not always sufficient Not always sufficient Shade avoidance Negative Dominant No function on its own Small effect, in Small effect, in regulation combination with phyB22 combination with phyB21 Flowering Weak Strong repressor. Repressor in SD23 Weak repressor Strong repressor repressor. Together with phyC Together with phyB Temperature dependent Antagonizes necessary for flowering necessary for photoperiodic phyD and phyE in response to flowering Can confer photoperiod photoperiod sensitivity on its own Dimers30 a Homodimers Both Heterodimers Both Bothb Nuclear Mediated by Independent of FHY1 Dependent on dimerization Independent of FHY1 and Independent of FHY1 and internalization57 FHY1 and FHL and FHL. Possibly with phyB (or phyD) FHL. Not light regulated FHL mediated by PIFs in the absence of phyB WL white light, R red light, FR far red light, c continuous, p pulse, SD short days aSanchez Lamas et al.14 could detect all possible dimers with the exception of phyC/phyC using BiFC bAlthough they were not detected in Co-IP30, they were found in native western blots24, and phyE alone can repress flowering