An Evolutionarily Conserved Signaling Mechanism Mediates Far-Red Light Responses in Land Plants

Peroxisomes are eukaryotic organelles with crucial functions in development. Plant peroxisomes participate in various metabolic processes, some of which are co-operated by peroxisomes and other organelles, such as mitochondria and chloroplasts. Defining the complete picture of how these essential organelles divide and proliferate will be instrumental in understanding how the dynamics of peroxisome abundance contribute to changes in plant physiology and development. Research in Arabidopsis thaliana has identified several evolutionarily conserved major components of the peroxisome division machinery, including five isoforms of PEROXIN11 proteins (PEX11), two dynamin-related proteins (DRP3A and DRP3B) and two FISSION1 proteins (FIS1A/BIGYIN and FIS1B). Recent studies in our laboratory have also begun to uncover plant-specific factors. DRP5B is a dual-localized protein that is involved in the division of both chloroplasts and peroxisomes, representing an invention of the plant/algal lineage in organelle division. In addition, PMD1 (peroxisomal and mitochondrial division 1) is a plant-specific protein tail anchored to the outer surface of peroxisomes and mitochondria, mediating the division and/or positioning of these organelles. Lastly, light induces peroxisome proliferation in dark-grown Arabidopsis seedlings, at least in part, through activating the PEX11b gene. The far-red light receptor phyA (phytochrome A) and the transcription factor HYH (HY5 homologue) are key components in this signalling pathway. In summary, pathways for the division and proliferation of plant peroxisomes are composed of conserved and plant-specific factors. The sharing of division proteins by peroxisomes, mitochondria and chloroplasts is also suggesting possible co-ordination in the division of these metabolically associated plant organelles.

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Allosteric deactivation of PIFs and EIN3 by microproteins in light control of plant development

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2002313117 ◽

2020 ◽

Vol 117 (31) ◽

pp. 18858-18868 ◽

Cited By ~ 1

Author(s):

Qingqing Wu ◽

Kunyan Kuang ◽

Mohan Lyu ◽

Yan Zhao ◽

Yue Li ◽

...

Keyword(s):

Transcription Factors ◽

Transcriptional Activity ◽

Environmental Changes ◽

Protein Complexes ◽

Binding Capacity ◽

Negative Control ◽

Light Responses ◽

Developmental Transitions ◽

Evolutionarily Conserved ◽

Target Molecules

Buried seedlings undergo dramatic developmental transitions when they emerge from soil into sunlight. As central transcription factors suppressing light responses, PHYTOCHROME-INTERACTING FACTORs (PIFs) and ETHYLENE-INSENSITIVE 3 (EIN3) actively function in darkness and must be promptly repressed upon light to initiate deetiolation. Microproteins are evolutionarily conserved small single-domain proteins that act as posttranslational regulators in eukaryotes. Although hundreds to thousands of microproteins are predicted to exist in plants, their target molecules, biological roles, and mechanisms of action remain largely unknown. Here, we show that two microproteins, miP1a and miP1b (miP1a/b), are robustly stimulated in the dark-to-light transition.miP1a/bare primarily expressed in cotyledons and hypocotyl, exhibiting tissue-specific patterns similar to those ofPIFs andEIN3. We demonstrate that PIFs and EIN3 assemble functional oligomers by self-interaction, while miP1a/b directly interact with and disrupt the oligomerization of PIFs and EIN3 by forming nonfunctional protein complexes. As a result, the DNA binding capacity and transcriptional activity of PIFs and EIN3 are predominantly suppressed. These biochemical findings are further supported by genetic evidence. miP1a/b positively regulate photomorphogenic development, and constitutively expressingmiP1a/brescues the delayed apical hook unfolding and cotyledon development of plants overexpressingPIFs andEIN3. Our study reveals that microproteins provide a temporal and negative control of the master transcription factors' oligomerization to achieve timely developmental transitions upon environmental changes.

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On the (un)coupling of the chromophore, tongue interactions, and overall conformation in a bacterial phytochrome

Journal of Biological Chemistry ◽

10.1074/jbc.ra118.001794 ◽

2018 ◽

Vol 293 (21) ◽

pp. 8161-8172 ◽

Cited By ~ 20

Author(s):

Heikki Takala ◽

Heli K. Lehtivuori ◽

Oskar Berntsson ◽

Ashley Hughes ◽

Rahul Nanekar ◽

...

Keyword(s):

Conformational Changes ◽

Structural Changes ◽

Deinococcus Radiodurans ◽

Red Light ◽

Light Responses ◽

Structural Mechanism ◽

Weakly Coupled ◽

Activity State ◽

Conserved Tyrosine

Phytochromes are photoreceptors in plants, fungi, and various microorganisms and cycle between metastable red light–absorbing (Pr) and far-red light–absorbing (Pfr) states. Their light responses are thought to follow a conserved structural mechanism that is triggered by isomerization of the chromophore. Downstream structural changes involve refolding of the so-called tongue extension of the phytochrome-specific GAF-related (PHY) domain of the photoreceptor. The tongue is connected to the chromophore by conserved DIP and PRXSF motifs and a conserved tyrosine, but the role of these residues in signal transduction is not clear. Here, we examine the tongue interactions and their interplay with the chromophore by substituting the conserved tyrosine (Tyr263) in the phytochrome from the extremophile bacterium Deinococcus radiodurans with phenylalanine. Using optical and FTIR spectroscopy, X-ray solution scattering, and crystallography of chromophore-binding domain (CBD) and CBD–PHY fragments, we show that the absence of the Tyr263 hydroxyl destabilizes the β-sheet conformation of the tongue. This allowed the phytochrome to adopt an α-helical tongue conformation regardless of the chromophore state, hence distorting the activity state of the protein. Our crystal structures further revealed that water interactions are missing in the Y263F mutant, correlating with a decrease of the photoconversion yield and underpinning the functional role of Tyr263 in phytochrome conformational changes. We propose a model in which isomerization of the chromophore, refolding of the tongue, and globular conformational changes are represented as weakly coupled equilibria. The results also suggest that the phytochromes have several redundant signaling routes.

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FIN5 Positively Regulates Far-red Light Responses in Arabidopsis thaliana

Plant and Cell Physiology ◽

10.1093/pcp/pcg071 ◽

2003 ◽

Vol 44 (6) ◽

pp. 565-572 ◽

Cited By ~ 2

Author(s):

Dae-Shik Cho ◽

Sung-Hyun Hong ◽

Hong-Gil Nam ◽

Moon-Soo Soh

Keyword(s):

Arabidopsis Thaliana ◽

Red Light ◽

Light Responses

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Ultra-High-Density QTL Marker Mapping for Seedling Photomorphogenesis Mediating Arabidopsis Establishment in Southern Patagonia

Frontiers in Plant Science ◽

10.3389/fpls.2021.677728 ◽

2021 ◽

Vol 12 ◽

Author(s):

Daniel Matsusaka ◽

Daniele Filiault ◽

Diego H. Sanchez ◽

Javier F. Botto

Keyword(s):

Complex Traits ◽

Red Light ◽

High Density ◽

Potential Candidate ◽

Hypocotyl Length ◽

Light Responses ◽

Wide Range ◽

Southern Patagonia ◽

Ril Population ◽

Wild Accessions

Arabidopsis thaliana shows a wide range of genetic and trait variation among wild accessions. Because of its unparalleled biological and genomic resources, Arabidopsis has a high potential for the identification of genes underlying ecologically important complex traits, thus providing new insights on genome evolution. Previous research suggested that distinct light responses were crucial for Arabidopsis establishment in a peculiar ecological niche of southern Patagonia. The aim of this study was to explore the genetic basis of contrasting light-associated physiological traits that may have mediated the rapid adaptation to this new environment. From a biparental cross between the photomorphogenic contrasting accessions Patagonia (Pat) and Columbia (Col-0), we generated a novel recombinant inbred line (RIL) population, which was entirely next-generation sequenced to achieve ultra-high-density saturating molecular markers resulting in supreme mapping sensitivity. We validated the quality of the RIL population by quantitative trait loci (QTL) mapping for seedling de-etiolation, finding seven QTLs for hypocotyl length in the dark and continuous blue light (Bc), continuous red light (Rc), and continuous far-red light (FRc). The most relevant QTLs, Rc1 and Bc1, were mapped close together to chromosome V; the former for Rc and Rc/dark, and the latter for Bc, FRc, and dark treatments. The additive effects of both QTLs were confirmed by independent heterogeneous inbred families (HIFs), and we explored TZP and ABA1 as potential candidate genes for Rc1 and Bc1QTLs, respectively. We conclude that the Pat × Col-0 RIL population is a valuable novel genetic resource to explore other adaptive traits in Arabidopsis.

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A Multifaceted Action of Phytochrome B in Plant Environmental Adaptation

Frontiers in Plant Science ◽

10.3389/fpls.2021.659712 ◽

2021 ◽

Vol 12 ◽

Author(s):

Jae Young Kim ◽

June-Hee Lee ◽

Chung-Mo Park

Keyword(s):

Red Light ◽

Environmental Adaptation ◽

Signaling Cascades ◽

Adaptive Behaviors ◽

Environmental Cues ◽

Plant Responses ◽

Light Illumination ◽

Light Responses ◽

And Performance

Light acts as a vital external cue that conveys surrounding information into plant growth and performance to facilitate plants to coordinate with changing environmental conditions. Upon exposure to light illumination, plants trigger a burst of molecular and physiological signaling cascades that induces not only photomorphogenic responses but also diverse adaptive behaviors. Notably, light responses and photomorphogenic traits are often associated with plant responses to other environmental cues, such as heat, cold, drought, and herbivore and pathogen attack. Growing evidence in recent years demonstrate that the red/far-red light-absorbing phytochrome (phy) photoreceptors, in particular phyB, play an essential role in plant adaptation responses to abiotic and biotic tensions by serving as a key mediator of information flow. It is also remarkable that phyB mediates the plant priming responses to numerous environmental challenges. In this minireview, we highlight recent advances on the multifaceted role of phyB during plant environmental adaptation. We also discuss the biological relevance and efficiency of the phy-mediated adaptive behaviors in potentially reducing fitness costs under unfavorable environments.

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