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We thank Ester Botterweg and Mª Rosa Rodríguez (CRAG) for their technical support; Victor González and Martí Bernardo (Bioinformatics Core unit, CRAG) for help in statistical analyses; Peter Quail (PGEC, Albany, CA, USA) for providing the anti-phyA antibody; Fernando Valladares (National Museum of Natural History, Madrid, Spain) for discussions about the shade habit of A. thaliana and C. hirsuta; and to Charlotte Gommers (CRAG) for comments on the manuscript. MJM-C, SP and LC received predoctoral fellowships from the Spanish Ministerio de Economía y competitividad (MINECO, FPI program), the Agència d’Ajuts Universitaris i de Recerca (AGAUR - Generalitat de Catalunya, FI program) and La Caixa Foundation (INPhINIT fellowship LCF/BQ/IN18/11660004), respectively. JM-R received a International CRAG “Severo Ochoa” postdoctoral program fellowship and a postdoctoral contract (H2020-MSCA-IF-2017 – Proposal 797473) funded by the European Commission. CT received a Marie Curie postdoctoral contract (FP7-PEOPLE821 IEF-2008 – Proposal 237492) funded by the European Commission and a CRAG short-term fellowship. Our research is supported by grants from BBSRC (BB/H006974/1) and Max Planck Society (core grant) to MT, and from MINECO-FEDER (BIO2017-85316-R, and BIO2017-84041-P) and AGAUR (2017-SGR1211, 2017-SGR710 and Xarba) to JFM-G and MRC. We also acknowledge the support of the MINECO for the “Centro de Excelencia Severo Ochoa 2016-2019” award SEV-2015-0533 and by the CERCA Programme /Generalitat de Catalunya.

In view of the extensive literature on phytochrome mutants in the L er accession of Arabidopsis , we sought to secure a phytochrome-null line in the same genetic background for comparative studies. Here we report the isolation and phenotypic characterization of phyABCDE quintuple and phyABDE quadruple mutants in the L er background. Unlike earlier studies, these lines possess a functional allele of FT permitting measurements of photoperiod-dependent flowering behavior. Comparative studies of both classes of mutants establish that phytochromes are dispensable for completion of the Arabidopsis life cycle under red light, despite the lack of a transcriptomic response, and also indicate that phyC is nonfunctional in the absence of other phytochromes. Phytochrome-less plants can produce chlorophyll for photosynthesis under continuous red light, yet require elevated fluence rates for survival. Unexpectedly, our analyses reveal both light-dependent and -independent roles for phytochromes to regulate the Arabidopsis circadian clock. The rapid transition of these mutants from vegetative to reproductive growth, as well as their insensitivity to photoperiod, establish a dual role for phytochromes to arrest and to promote progression of plant development in response to the prevailing light environment.

The phytochrome (phy) family of photoreceptors regulates changes in gene expression in response to red/far-red light signals in part by physically interacting with constitutively nucleus-localized phy-interacting basic helix-loop-helix transcription factors (PIFs). Here, we show that PIF1, the member with the highest affinity for phys, is strongly sensitive to the quality and quantity of light. phyA plays a dominant role in regulating the degradation of PIF1 following initial light exposure, while phyB and phyD and possibly other phys also influence PIF1 degradation after prolonged illumination. PIF1 is rapidly phosphorylated and ubiquitinated under red and far-red light before being degraded with a half-life of ~1 to 2 min under red light. Although PIF1 interacts with phyB through a conserved active phyB binding motif, it interacts with phyA through a novel active phyA binding motif. phy interaction is necessary but not sufficient for the light-induced phosphorylation and degradation of PIF1. Domain-mapping studies reveal that the phy interaction, light-induced degradation, and transcriptional activation domains are located at the N-terminal 150-amino acid region of PIF1. Unlike PIF3, PIF1 does not interact with the two halves of either phyA or phyB separately. Moreover, overexpression of a light-stable truncated form of PIF1 causes constitutively photomorphogenic phenotypes in the dark. Taken together, these data suggest that removal of the negative regulators (e.g., PIFs) by light-induced proteolytic degradation might be sufficient to promote photomorphogenesis.

The involvement of the microRNA miR165a in the light-dependent mechanisms of regulation of target genes in maize (Zea mays) has been studied. The light-induced change in the content of free miR165a was associated with its binding by the AGO10 protein and not with a change in the rate of its synthesis from the precursor. The use of knockout Arabidopsis plants for the phytochrome A and B genes demonstrated that the presence of an active form of phytochrome B causes an increase in the level of the RNA-induced silencing miR165a complex, which triggers the degradation of target mRNAs. The two fractions of vesicles from maize leaves, P40 and P100 that bind miR165a, were isolated by ultracentrifugation. The P40 fraction consisted of larger vesicles of the size >0.170 µm, while the P100 fraction vesicles were <0.147 µm. Based on the quantitative PCR data, the predominant location of miR165a on the surface of extracellular vesicles of both fractions was established. The formation of the active form of phytochrome upon the irradiation of maize plants with red light led to a redistribution of miR165a, resulting in an increase in its proportion inside P40 vesicles and a decrease in P100 vesicles.

Photoperiod is an important environmental cue. Plants can distinguish the seasons and flower at the right time through sensing the photoperiod. Soybean is a sensitive shortday crop, and the timing of flowering varies greatly at different latitudes, thus affecting yields. Soybean cultivars in high latitudes adapt to the long day by the impairment of two phytochrome genes, PHYA3 and PHYA2, and the legume-specific flowering suppressor, E1. However, the regulating mechanism underlying phyA and E1 in soybean remains largely unknown. Here, we classified the regulation of the E1 family by phyA2 and phyA3 at the transcriptional and posttranscriptional levels, revealing that phyA2 and phyA3 regulate E1 by directly binding to LUX proteins, the critical component of the evening complex, to regulate the stability of LUX proteins. In addition, phyA2 and phyA3 can also directly associate with E1 and its homologs to stabilize the E1 proteins. Therefore, phyA homologs control the core flowering suppressor E1 at both the transcriptional and posttranscriptional levels, to double ensure the E1 activity. Thus, our results disclose a photoperiod flowering mechanism in plants by which the phytochrome A regulates LUX and E1 activity.

• The seasonally synchronized annual growth cycle that is regulated mainly by photoperiod and temperature cues is a crucial adaptive strategy for perennial plants in boreal and temperate ecosystems. • Phytochrome B (phyB), as a light and thermal sensor, has been extensively studied in Arabidopsis. However, the specific mechanisms for how the phytochrome photoreceptors control the phenology in tree species remain poorly understood. • We characterized the functions of PHYB genes and their downstream PHYTOCHROME INTERACTING FACTOR (PIF) targets in the regulation of shade avoidance and seasonal growth in hybrid aspen trees. We show that while phyB1 and phyB2, as phyB in other plants, act as suppressors of shoot elongation during vegetative growth, they act as promoters of tree seasonal growth. Furthermore, while the Populus homologs of both PIF4 and PIF8 are involved in the shade avoidance syndrome (SAS), only PIF8 plays a major role as a suppressor of seasonal growth. • Our data suggest that the PHYB-PIF8 regulon controls seasonal growth through the regulation of FT and CENL1 expression while a genome-wide transcriptome analysis suggests how, in Populus trees, phyB coordinately regulates SAS responses and seasonal growth cessation.

Phytochrome (phy) system in plants comprising a small number of phytochromes with phyA and phyB as major ones is responsible for acquiring light information in the red—far-red region of the solar spectrum. It provides optimal strategy for plant development under changing light conditions throughout all its life cycle beginning from seed germination and seedling establishment to fruiting and plant senescence. The phyA was shown to participate in the regulation of this cycle which is especially evident at its early stages. It mediates three modes of reactions—the very low and low fluence responses (VLFR and LFR) and the high irradiance responses (HIR). The phyA is the sole light receptor in the far-red spectral region responsible for plant’s survival under a dense plant canopy where light is enriched with the far-red component. Its appearance is believed to be one of the main factors of plants′ successful evolution. So far, it is widely accepted that one molecular phyA species is responsible for its complex functional manifestations. In this review, the evidence of the existence of two distinct phyA types—major, light-labile and soluble phyA′ and minor, relatively light-stable and amphiphilic phyA″—is presented as what may account for the diverse modes of phyA action.

Phytochromes are believed to be solely responsible for red and far-red light perception, but this has never been definitively tested. To directly address this hypothesis, a phytochrome triple mutant (phyAphyBphyC) was generated in rice (Oryza sativa L. cv. Nipponbare) and its responses to red and far-red light were monitored. Since rice only has three phytochrome genes (PHYA, PHYB and PHYC), this mutant is completely lacking any phytochrome. Rice seedlings grown in the dark develop long coleoptiles while undergoing regular circumnutation. The phytochrome triple mutants also show this characteristic skotomorphogenesis, even under continuous red or far-red light. The morphology of the triple mutant seedlings grown under red or far-red light appears completely the same as etiolated seedlings, and they show no expression of the light-induced genes. This is direct evidence demonstrating that phytochromes are the sole photoreceptors for perceiving red and far-red light, at least during rice seedling establishment. Furthermore, the shape of the triple mutant plants was dramatically altered. Most remarkably, triple mutants extend their internodes even during the vegetative growth stage, which is a time during which wild-type rice plants never elongate their internodes. The triple mutants also flowered very early under long day conditions and set very few seeds due to incomplete male sterility. These data indicate that phytochromes play an important role in maximizing photosynthetic abilities during the vegetative growth stage in rice.

Light signals perceived by a group of photoreceptors have profound effects on the physiology, growth, and development of plants. The red/far-red light–absorbing phytochromes (phys) modulate these aspects by intricately regulating gene expression at multiple levels. Here, we report the identification and functional characterization of an RNA-binding splicing factor, SWAP1 (SUPPRESSOR-OF-WHITE-APRICOT/SURP RNA-BINDING DOMAIN-CONTAINING PROTEIN1). Loss-of-function swap1-1 mutant is hyposensitive to red light and exhibits a day length–independent early flowering phenotype. SWAP1 physically interacts with two other splicing factors, (SFPS) SPLICING FACTOR FOR PHYTOCHROME SIGNALING and (RRC1) REDUCED RED LIGHT RESPONSES IN CRY1CRY2 BACKGROUND 1 in a light-independent manner and forms a ternary complex. In addition, SWAP1 physically interacts with photoactivated phyB and colocalizes with nuclear phyB photobodies. Phenotypic analyses show that the swap1sfps, swap1rrc1, and sfpsrrc1 double mutants display hypocotyl lengths similar to that of the respective single mutants under red light, suggesting that they function in the same genetic pathway. The swap1sfps double and swap1sfpsrrc1 triple mutants display pleiotropic phenotypes, including sterility at the adult stage. Deep RNA sequencing (RNA-seq) analyses show that SWAP1 regulates the gene expression and pre–messenger RNA (mRNA) alternative splicing of a large number of genes, including those involved in plant responses to light signaling. A comparative analysis of alternative splicing among single, double, and triple mutants showed that all three splicing factors coordinately regulate the alternative splicing of a subset of genes. Our study uncovered the function of a splicing factor that modulates light-regulated alternative splicing by interacting with photoactivated phyB and other splicing factors.

Phytochrome B (phyB) is an excellent light quality and quantity sensor that can detect subtle changes in the light environment. The relative amounts of the biologically active photoreceptor (phyB Pfr) are determined by the light conditions and light independent thermal relaxation of Pfr into the inactive phyB Pr, termed thermal reversion. Little is known about the regulation of thermal reversion and how it affects plants’ light sensitivity. In this study we identified several serine/threonine residues on the N-terminal extension (NTE) of Arabidopsis thaliana phyB that are differentially phosphorylated in response to light and temperature, and examined transgenic plants expressing nonphosphorylatable and phosphomimic phyB mutants. The NTE of phyB is essential for thermal stability of the Pfr form, and phosphorylation of S86 particularly enhances the thermal reversion rate of the phyB Pfr–Pr heterodimer in vivo. We demonstrate that S86 phosphorylation is especially critical for phyB signaling compared with phosphorylation of the more N-terminal residues. Interestingly, S86 phosphorylation is reduced in light, paralleled by a progressive Pfr stabilization under prolonged irradiation. By investigating other phytochromes (phyD and phyE) we provide evidence that acceleration of thermal reversion by phosphorylation represents a general mechanism for attenuating phytochrome signaling.