Evolutionary Studies Illuminate the Structural-Functional Model of Plant Phytochromes

Mathews, Sarah

doi:10.1105/tpc.109.072280

Cited by 107 publications

(105 citation statements)

References 148 publications

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“…Phytochromes are encoded by three genes (PHYA, PHYB, and PHYC) in most monocot species whereas eudicot plant species possess additional genes (PHYD-F) derived from PHYB duplications (7,8). Studies in model plant species have shown that PHYA is required for growth in deep shade and for seedling deetiolation (9) whereas members of the PHYB clade play major roles in shade-avoidance responses (10,11).…”

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confidence: 99%

PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod

Chen¹,

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

182

228

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Phytochromes are dimeric proteins that function as red and far-red light sensors influencing nearly every phase of the plant life cycle. Of the three major phytochrome families found in flowering plants, PHYTOCHROME C (PHYC) is the least understood. In Arabidopsis and rice, PHYC is unstable and functionally inactive unless it heterodimerizes with another phytochrome. However, when expressed in an Arabidopsis phy-null mutant, wheat PHYC forms signaling active homodimers that translocate into the nucleus in red light to mediate photomorphogenic responses. Tetraploid wheat plants homozygous for loss-of-function mutations in all PHYC copies (phyC AB ) flower on average 108 d later than wild-type plants under long days but only 19 d later under short days, indicating a strong interaction between PHYC and photoperiod. This interaction is further supported by the drastic down-regulation in the phyC AB mutant of the central photoperiod gene PHOTOPERIOD 1 (PPD1) and its downstream target FLOWERING LOCUS T1, which are required for the promotion of flowering under long days. These results implicate light-dependent, PHYC-mediated activation of PPD1 expression in the acceleration of wheat flowering under inductive long days. Plants homozygous for the phyC AB mutations also show altered profiles of circadian clock and clock-output genes, which may also contribute to the observed differences in heading time. Our results highlight important differences in the photoperiod pathways of the temperate grasses with those of well-studied model plant species.

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mentioning

confidence: 99%

PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod

Chen¹,

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

182

228

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“…Examples include a long N-terminal extension (NTE) in plant Phys and pervasive sequence variations within the PAS, GAF, and PHY domains and the downstream OPM (3,4). For a more authoritative view, we present the crystal structure of a Phy PSM from a seed plant, that of PhyB from Arabidopsis thaliana, and extensively characterize its solution and photochemical properties.…”

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confidence: 99%

“…This information then regulates nearly all aspects of plant growth and development from seed germination to senescence. Notably, seed plants typically express three Phy isoforms (PhyA, PhyB, and PhyC) that control distinct and overlapping photoresponses, with PhyB having a dominant role in green tissues (2,3).…”

mentioning

confidence: 99%

Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome

Burgie

Bussell

Walker

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

201

327

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Many aspects of plant photomorphogenesis are controlled by the phytochrome (Phy) family of bilin-containing photoreceptors that detect red and far-red light by photointerconversion between a dark-adapted Pr state and a photoactivated Pfr state. Whereas 3D models of prokaryotic Phys are available, models of their plant counterparts have remained elusive. Here, we present the crystal structure of the photosensing module (PSM) from a seed plant Phy in the Pr state using the PhyB isoform from Arabidopsis thaliana. The PhyB PSM crystallized as a head-to-head dimer with strong structural homology to its bacterial relatives, including a 5(Z)syn, 10(Z)syn, 15(Z)anti configuration of the phytochromobilin chromophore buried within the cGMP phosphodiesterase/adenylyl cyclase/FhlA (GAF) domain, and a well-ordered hairpin protruding from the Phy-specific domain toward the bilin pocket. However, its Per/Arnt/Sim (PAS) domain, knot region, and helical spine show distinct structural differences potentially important to signaling. Included is an elongated helical spine, an extended β-sheet connecting the GAF domain and hairpin stem, and unique interactions between the region upstream of the PAS domain knot and the bilin A and B pyrrole rings. Comparisons of this structure with those from bacterial Phys combined with mutagenic studies support a toggle model for photoconversion that engages multiple features within the PSM to stabilize the Pr and Pfr end states after rotation of the D pyrrole ring. Taken together, this Arabidopsis PhyB structure should enable molecular insights into plant Phy signaling and provide an essential scaffold to redesign their activities for agricultural benefit and as optogenetic reagents.G iven the importance of sunlight to their survival and growth, plants have adopted a collection of photoreceptors and interconnected signaling cascades to optimize their photosynthetic potential and synchronize their lifecycles with circadian and seasonal rhythms. Chief among these are the phytochromes (Phys), a family of bilin (or open-chain tetrapyrrole)-containing red/far-red light-absorbing photoreceptors that provides spatial and time-dependent information by sensing the fluence rate, direction, duration, and color of a plant's light environment (1, 2). This information then regulates nearly all aspects of plant growth and development from seed germination to senescence. Notably, seed plants typically express three Phy isoforms (PhyA, PhyB, and PhyC) that control distinct and overlapping photoresponses, with PhyB having a dominant role in green tissues (2, 3).Phys are homodimers with each sister polypeptide divided into an N-terminal photosensory module (PSM) that absorbs light followed by an output module (OPM) that promotes dimerization and presumably, relays the light signals (1, 4). The PSM sequentially contains a Per/Arnt/Sim (PAS) domain of unknown function, a cGMP phosphodiesterase/adenylyl cyclase/FhlA (GAF) domain that cradles the bilin, and a Phy-specific (PHY) domain that stabilizes the photoactivated ...

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“…Certain groups of plants, such as diploid grasses, have only one copy of PHYA, PHYB, and PHYC, although lineage-specific duplications and losses of phytochrome genes have occurred in many groups of flowering plants (Mathews 2010). Phytochrome mutants in the model plant systems Arabidopsis (Arabidopsis thaliana, Brassicaceae) and rice (Oryza sativa, Poaceae) have contributed to the elucidation of the functional roles of the various phytochromes.…”

mentioning

confidence: 99%

“…Flowering plants typically contain three types of phytochromes referred to as PHYTOCHROME A (PHYA), PHY-TOCHROME B (PHYB), and PHYTOCHROME C (PHYC) (Mathews 2010). Certain groups of plants, such as diploid grasses, have only one copy of PHYA, PHYB, and PHYC, although lineage-specific duplications and losses of phytochrome genes have occurred in many groups of flowering plants (Mathews 2010).…”

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confidence: 99%

PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon

et al. 2014

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We show that in the temperate grass, Brachypodium distachyon, PHYTOCHROME C (PHYC), is necessary for photoperiodic flowering. In loss-of-function phyC mutants, flowering is extremely delayed in inductive photoperiods. PHYC was identified as the causative locus by utilizing a mapping by sequencing pipeline (Cloudmap) optimized for identification of induced mutations in Brachypodium. In phyC mutants the expression of Brachypodium homologs of key flowering time genes in the photoperiod pathway such as GIGANTEA (GI), PHOTOPERIOD 1 (PPD1/PRR37), CONSTANS (CO), and florigen/FT are greatly attenuated. PHYC also controls the day-length dependence of leaf size as the effect of day length on leaf size is abolished in phyC mutants. The control of genes upstream of florigen production by PHYC was likely to have been a key feature of the evolution of a long-day flowering response in temperate pooid grasses.

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Evolutionary Studies Illuminate the Structural-Functional Model of Plant Phytochromes

Cited by 107 publications

References 148 publications

PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod

PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod

Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome

PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon

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