Phototropin phosphorylation of ROOT PHOTOTROPISM 2 and its role in mediating phototropism, leaf positioning, and chloroplast accumulation movement in Arabidopsis.

Directional movements impact the ability of plants to respond and adjust their growth accordingly to the prevailing light environment. The plasma-membrane associated protein, ROOT PHOTOTROPISM 2 (RPT2) is a key signalling component involved in chloroplast accumulation movement, leaf positioning, and phototropism, all of which are regulated redundantly by the ultraviolet/blue light-activated AGC kinases phototropin 1 and 2 (phot1 and phot2). We recently demonstrated that members of the NON-PHOTOTROPIC HYPOCOTYL 3 (NPH3)/RPT2-like (NRL) family in Arabidopsis thaliana, including RPT2, are directly phosphorylated by phot1. However, whether RPT2 is a substrate for phot2, and the biological significance of phot phosphorylation of RPT2 remains to be determined. Here, we show that RPT2 is phosphorylated by both phot1 and phot2 at a conserved serine residue (S591) within the C-terminal region of the protein. Blue light triggered the association of 14-3-3 proteins with RPT2 consistent with S591 acting as a 14-3-3 binding site. Mutation of S591 had no effect on the plasma membrane localization of RPT2 but reduced its functionality for leaf positioning and phototropism. Moreover, our findings indicate that S591 phosphorylation within the C-terminus of RPT2 is required for chloroplast accumulation movement to low level blue light. Taken together, these findings further highlight the importance of the C-terminal region of NRL proteins and how its phosphorylation contributes to phot receptor signalling in plants.

A kinesin-like protein, KAC, is required for light-induced and actin-based chloroplast movement in Marchantia polymorpha.

Chloroplasts accumulate on the cell surface under weak light conditions to efficiently capture light but avoid strong light to minimize photodamage. The blue light receptor phototropin regulates the chloroplast movement in various plant species. In Arabidopsis thaliana, phototropin mediates the light-induced chloroplast movement and positioning via specialized actin filaments on the chloroplasts, chloroplast-actin filaments. KINESIN-LIKE PROTEIN FOR ACTIN-BASED CHLOROPLAST MOVEMENT (KAC) and CHLOROPLAST UNUSUAL POSITIONING 1 (CHUP1) are pivotal for chloroplast-actin-based chloroplast movement and positioning in land plants. However, the mechanisms by which KAC and CHUP1 regulate chloroplast movement and positioning remain unclear. In this study, we characterized KAC and CHUP1 orthologs in the liverwort Marchantia polymorpha, MpKAC and MpCHUP1, respectively. Their knockout mutants, Mpkack° and Mpchup1k°, impaired the light-induced chloroplast movement. Although Mpchup1k° showed mild chloroplast aggregation, Mpkack° displayed severe chloroplast aggregation, suggesting the greater contribution of MpKAC to the chloroplast anchorage to the plasma membrane. Analysis of the subcellular localization of the functional MpKAC-Citrine indicated that MpKAC-Citrine formed a punctate structure on the plasma membrane. Structure-function analysis of MpKAC revealed that a deletion of the conserved C-terminal domain abrogates the targeting to the plasma membrane and its function. A deletion of the N-terminal motor domain retained the plasma membrane targeting but abrogates the formation of punctate structure and showed severe defect in the light-induced chloroplast movement. Our findings suggest that the formation of the punctate structure on the plasma membrane of MpKAC is essential for chloroplast movement.

Phototropin2 3'UTR overlaps with the AT5G58150 gene encoding an inactive RLK kinase.

BACKGROUND: This study examines the biological implications of an overlap between two sequences in the Arabidopsis genome, the 3'UTR of the PHOT2 gene and a putative AT5G58150 gene, encoded on the complementary strand. AT5G58150 is a probably inactive protein kinase that belongs to the transmembrane, leucine-rich repeat receptor-like kinase family. Phot2 is a membrane-bound UV/blue light photoreceptor kinase. Thus, both proteins share their cellular localization, on top of the proximity of their loci. RESULTS: The extent of the overlap between 3'UTR regions of AT5G58150 and PHOT2 was found to be 66 bp, using RACE PCR. Both the at5g58150 T-DNA SALK_093781C (with insertion in the promoter region) and 35S::AT5G58150-GFP lines overexpress the AT5G58150 gene. A detailed analysis did not reveal any substantial impact of PHOT2 or AT5G58150 on their mutual expression levels in different light and osmotic stress conditions. AT5G58150 is a plasma membrane protein, with no apparent kinase activity, as tested on several potential substrates. It appears not to form homodimers and it does not interact with PHOT2. Lines that overexpress AT5G58150 exhibit a greater reduction in lateral root density due to salt and osmotic stress than wild-type plants, which suggests that AT5G58150 may participate in root elongation and formation of lateral roots. In line with this, mass spectrometry analysis identified proteins with ATPase activity, which are involved in proton transport and cell elongation, as putative interactors of AT5G58150. Membrane kinases, including other members of the LRR RLK family and BSK kinases (positive regulators of brassinosteroid signalling), can also act as partners for AT5G58150. CONCLUSIONS: AT5G58150 is a membrane protein that does not exhibit measurable kinase activity, but is involved in signalling through interactions with other proteins. Based on the interactome and root architecture analysis, AT5G58150 may be involved in plant response to salt and osmotic stress and the formation of roots in Arabidopsis.

Introgression of a dominant phototropin1 mutant enhances carotenoids and boosts flavour-related volatiles in genome-edited tomato RIN mutants.

The tomato (Solanum lycopersicum) ripening inhibitor (rin) mutation is known to completely repress fruit ripening. The heterozygous (RIN/rin) fruits have extended shelf life, ripen normally, but have inferior taste/flavour. To address this, we used genome editing to generate newer alleles of RIN (rinCR ) by targeting the K-domain. Unlike previously reported CRISPR alleles, the rinCR alleles displayed delayed onset of ripening, suggesting that the mutated K-domain represses the onset of ripening. The rinCR fruits had extended shelf life and accumulated carotenoids at an intermediate level between rin and progenitor line. Besides, the metabolites and hormonal levels in rinCR fruits were more akin to rin. To overcome the negative attributes of rin, we crossed the rinCR alleles with Nps1, a dominant-negative phototropin1 mutant, which enhances carotenoid levels in tomato fruits. The resulting Nps1/rinCR hybrids had extended shelf life and 4.4-7.1-fold higher carotenoid levels than the wild-type parent. The metabolome of Nps1/rinCR fruits revealed higher sucrose, malate, and volatiles associated with tomato taste and flavour. Notably, the boosted volatiles in Nps1/rinCR were only observed in fruits bearing the homozygous Nps1 mutation. The Nps1 introgression into tomato provides a promising strategy for developing cultivars with extended shelf life, improved taste, and flavour.

CHUP1 restricts chloroplast movement and effector-triggered immunity in epidermal cells.

Chloroplast Unusual Positioning 1 (CHUP1) plays an important role in the chloroplast avoidance and accumulation responses in mesophyll cells. In epidermal cells, prior research showed silencing CHUP1-induced chloroplast stromules and amplified effector-triggered immunity (ETI); however, the underlying mechanisms remain largely unknown. CHUP1 has a dual function in anchoring chloroplasts and recruiting chloroplast-associated actin (cp-actin) filaments for blue light-induced movement. To determine which function is critical for ETI, we developed an approach to quantify chloroplast anchoring and movement in epidermal cells. Our data show that silencing NbCHUP1 in Nicotiana benthamiana plants increased epidermal chloroplast de-anchoring and basal movement but did not fully disrupt blue light-induced chloroplast movement. Silencing NbCHUP1 auto-activated epidermal chloroplast defense (ECD) responses including stromule formation, perinuclear chloroplast clustering, the epidermal chloroplast response (ECR), and the chloroplast reactive oxygen species (ROS), hydrogen peroxide (H2O2). These findings show chloroplast anchoring restricts a multifaceted ECD response. Our results also show that the accumulated chloroplastic H2O2 in NbCHUP1-silenced plants was not required for the increased basal epidermal chloroplast movement but was essential for increased stromules and enhanced ETI. This finding indicates that chloroplast de-anchoring and H2O2 play separate but essential roles during ETI.

Insights into degradation and targeting of the photoreceptor channelrhodopsin-1.

In Chlamydomonas, the directly light-gated, plasma membrane-localized cation channels channelrhodopsins ChR1 and ChR2 are the primary photoreceptors for phototaxis. Their targeting and abundance is essential for optimal movement responses. However, our knowledge how Chlamydomonas achieves this is still at its infancy. Here we show that ChR1 internalization occurs via light-stimulated endocytosis. Prior or during endocytosis ChR1 is modified and forms high molecular mass complexes. These are the solely detectable ChR1 forms in extracellular vesicles and their abundance therein dynamically changes upon illumination. The ChR1-containing extracellular vesicles are secreted via the plasma membrane and/or the ciliary base. In line with this, ciliogenesis mutants exhibit increased ChR1 degradation rates. Further, we establish involvement of the cysteine protease CEP1, a member of the papain-type C1A subfamily. ΔCEP1-knockout strains lack light-induced ChR1 degradation, whereas ChR2 degradation was unaffected. Low light stimulates CEP1 expression, which is regulated via phototropin, a SPA1 E3 ubiquitin ligase and cyclic AMP. Further, mutant and inhibitor analyses revealed involvement of the small GTPase ARL11 and SUMOylation in ChR1 targeting to the eyespot and cilia. Our study thus defines the degradation pathway of this central photoreceptor of Chlamydomonas and identifies novel elements involved in its homoeostasis and targeting.

A phytochrome/phototropin chimeric photoreceptor promotes growth of fern gametophytes under limited light conditions.

Many ferns thrive even in low-light niches such as under an angiosperm forest canopy. However, the shade adaptation strategy of ferns is not well understood. Phytochrome 3/neochrome (phy3/neo) is an unconventional photoreceptor, found in the fern Adiantum capillus-veneris, that controls both red and blue light-dependent phototropism and chloroplast photorelocation, which are considered to improve photosynthetic efficiency in ferns. Here we show that phy3/neo localizes not only at the plasma membrane but also in the nucleus. Since both phototropism and chloroplast photorelocation are mediated by membrane-associated phototropin photoreceptors, we speculated that nucleus-localized phy3/neo possesses a previously undescribed biological function. We reveal that phy3/neo directly interacts with Adiantum cryptochrome 3 (cry3) in the nucleus. Plant cryptochromes are blue light receptors that transcriptionally regulate photomorphogenesis; therefore, phy3/neo may function via cry3 to synchronize light-mediated development with phototropism and chloroplast photorelocation to promote fern growth under low-light conditions. Furthermore, we demonstrate that phy3/neo regulates the expression of the Cyclin-like gene AcCyc1 and promotes prothallium expansion growth. These findings provide insight into the shade adaptation strategy of ferns and suggest that phy3/neo plays a substantial role in the survival and growth of ferns during the tiny gametophytic stage under low-light conditions, such as those on the forest floor.

Lights, location, action: Shade avoidance signalling over spatial scales.

Plants growing in dense vegetation stands need to flexibly position their photosynthetic organs to ensure optimal light capture in a competitive environment. They do so through a suite of developmental responses referred to as the shade avoidance syndrome. Belowground, root development is also adjusted in response to aboveground neighbour proximity. Canopies are dynamic and complex environments with heterogenous light cues in the far-red, red, blue and UV spectrum, which can be perceived with photoreceptors by spatially separated plant tissues. Molecular regulation of plant architecture adjustment via PHYTOCHROME-INTERACTING FACTOR (PIF) transcription factors and growth-related hormones such as auxin, gibberellic acid, brassinosteroids and abscisic acid were historically studied without much attention to spatial or tissue-specific context. Recent developments and technologies have, however, sparked strong interest in spatially explicit understanding of shade avoidance regulation. Other environmental factors such as temperature and nutrient availability interact with the molecular shade avoidance regulation network, often depending on the spatial location of the signals, and the responding organs. Here, we aim to review recent advances in how plants respond to heterogenous light cues and integrate these with other environmental signals.

The endoplasmic reticulum membrane-bending protein RETICULON facilitates chloroplast relocation movement in Marchantia polymorpha.

Plant cells alter the intracellular positions of chloroplasts to ensure efficient photosynthesis, a process controlled by the blue light receptor phototropin. Chloroplasts migrate toward weak light (accumulation response) and move away from excess light (avoidance response). Chloroplasts are encircled by the endoplasmic reticulum (ER), which forms a complex network throughout the cytoplasm. To ensure rapid chloroplast relocation, the ER must alter its structure in conjunction with chloroplast relocation movement, but little is known about the underlying mechanism. Here, we searched for interactors of phototropin in the liverwort Marchantia polymorpha and identified a RETICULON (RTN) family protein; RTN proteins play central roles in ER tubule formation and ER network maintenance by stabilizing the curvature of ER membranes in eukaryotic cells. Marchantia polymorpha RTN1 (MpRTN1) is localized to ER tubules and the rims of ER sheets, which is consistent with the localization of RTNs in other plants and heterotrophs. The Mprtn1 mutant showed an increased ER tubule diameter, pointing to a role for MpRTN1 in ER membrane constriction. Furthermore, Mprtn1 showed a delayed chloroplast avoidance response but a normal chloroplast accumulation response. The live cell imaging of ER dynamics revealed that ER restructuring was impaired in Mprtn1 during the chloroplast avoidance response. These results suggest that during the chloroplast avoidance response, MpRTN1 restructures the ER network and facilitates chloroplast movement via an interaction with phototropin. Our findings provide evidence that plant cells respond to fluctuating environmental conditions by controlling the movements of multiple organelles in a synchronized manner.

Light and temperature regulation of leaf morphogenesis in Arabidopsis.

Leaves are the main photosynthetic organs in plants, and their anatomy is optimized for light interception and gas exchange. Although each species has a characteristic leaf anatomy, which depends on the genotype, leaves also show a large degree of developmental plasticity. Light and temperature regulate leaf development from primordia differentiation to late stages of blade expansion. While the molecular mechanisms of light and temperature signaling have been mostly studied in seedlings, in the latest years, research has focused on leaf development. Here, I will describe the latest work carried out in the environmental regulation of Arabidopsis leaf development, comparing signaling mechanisms between leaves and seedlings, highlighting the new discoveries, and pointing out the most exciting open questions.

Multifactorial in vivo regulation of the photoreceptor channelrhodopsin-1 abundance.

Oriented movement (phototaxis) is an efficient way to optimize light-driven processes and to avoid photodamage for motile algae. In Chlamydomonas the receptors for phototaxis are the channelrhodopsins ChR1 and ChR2. Both are directly light-gated, plasma membrane-localized cation channels. To optimally adjust its overall light-dependent responses, Chlamydomonas must tightly control the ChRs cellular abundance and integrate their activities into its general photoprotective network. How this is achieved is largely unknown. Here we show that the ChR1 protein level decreases upon illumination in a light-intensity and quality-dependent manner, whereas it is stable in prolonged darkness. Analysis of knockout strains of six major photoreceptors absorbing in the blue-violet range, which is most effective in evoking ChR1 degradation, revealed that only phototropin (PHOT) is involved. Notably, ChR2 degradation was normal in a ΔPHOT strain. Further, our results indicate that a COP1-SPA1 E3 ubiquitin ligase, the transcription factor Hy5 as well as changes in the cellular redox poise and cyclic nucleotide levels are additional components involved in this light acclimation response of Chlamydomonas. Our data highlight the presence of an adaptive framework connecting phototaxis with general photoprotective mechanisms via the use of overlapping signaling components already at the level of the primary photoreceptor.

Photosensory adaptation mechanisms in hypocotyl phototropism: how plants recognize the direction of a light source.

Plants recognize the direction of a light source and exhibit phototropic responses. Physiological studies have predicted that differences in the light intensity received by the cells on the irradiated and shaded sides of a coleoptile or hypocotyl cause differences in the amounts of photoproduct. This hypothetical photoproduct appears to regulate a signaling pathway that controls cell elongation in which cells under lower light intensity elongate more than those under higher light intensity. This results in a bending growth toward a light source and has been proposed as the photoproduct-gradient model of phototropism. In this review, we summarize recent findings on the photosensory adaptation mechanisms involving a blue-light photoreceptor, phototropin1 (phot1), ROOT PHOTOTROPISM2, NONPHOTOTROPIC HYPOCOTYL3 (NPH3), and another photoreceptor family, the phytochromes. The current evidence demonstrates that, in addition to the transition of the phot1-NPH3 photoreceptor complexes to their active state, the presence of a certain population of the phot1-NPH3 complexes showing a steady state, even in a light environment, is essential for recognition of the light source direction in phototropism. This is consistent with the photoproduct-gradient model, and a dissociation state of the phot1-NPH3 complex would be considered an entity of the hypothetical photoproduct in this model.

Reactive Carbonyl Species Inhibit Blue-Light-Dependent Activation of the Plasma Membrane H+-ATPase and Stomatal Opening.

Reactive oxygen species (ROS) play a central role in plant responses to biotic and abiotic stresses. ROS stimulate stomatal closure by inhibiting blue light (BL)-dependent stomatal opening under diverse stresses in the daytime. However, the stomatal opening inhibition mechanism by ROS remains unclear. In this study, we aimed to examine the impact of reactive carbonyl species (RCS), lipid peroxidation products generated by ROS, on BL signaling in guard cells. Application of RCS, such as acrolein and 4-hydroxy-(E)-2-nonenal (HNE), inhibited BL-dependent stomatal opening in the epidermis of Arabidopsis thaliana. Acrolein also inhibited H+ pumping and the plasma membrane H+-ATPase phosphorylation in response to BL. However, acrolein did not inhibit BL-dependent autophosphorylation of phototropins and the phosphorylation of BLUE LIGHT SIGNALING1 (BLUS1). Similarly, acrolein affected neither the kinase activity of BLUS1 nor the phosphatase activity of protein phosphatase 1, a positive regulator of BL signaling. However, acrolein inhibited fusicoccin-dependent phosphorylation of H+-ATPase and stomatal opening. Furthermore, carnosine, an RCS scavenger, partially alleviated the abscisic-acid- and hydrogen-peroxide-induced inhibition of BL-dependent stomatal opening. Altogether, these findings suggest that RCS inhibit BL signaling, especially H+-ATPase activation, and play a key role in the crosstalk between BL and ROS signaling pathways in guard cells.

Temperature Sensing in Plants: On the Dawn of Molecular Thermosensor Research.

Although many studies on plant growth and development focus on the effects of light, a growing number of studies dissect plant responses to temperature and the underlying signaling pathways. The identity of plant thermosensing molecules (thermosensors) acting upstream of the signaling cascades in temperature responses was elusive until recently. During the past six years, a set of plant thermosensors has been discovered, representing a major turning point in the research on plant temperature responses and signaling. Here, we review these newly discovered plant thermosensors, which can be classified as sensors of warmth or cold. We compare between plant thermosensors and those from other organisms and attempt to define the subcellular thermosensing compartments in plants. In addition, we discuss the notion that photoreceptive thermosensors represent a novel class of thermosensors, the roles of which have yet to be described in non-plant systems.

Transcriptome, metabolome and suppressor analysis reveal an essential role for the ubiquitin-proteasome system in seedling chloroplast development.

BACKGROUND: Many regulatory circuits in plants contain steps of targeted proteolysis, with the ubiquitin proteasome system (UPS) as the mediator of these proteolytic events. In order to decrease ubiquitin-dependent proteolysis, we inducibly expressed a ubiquitin variant with Arg at position 48 instead of Lys (ubK48R). This variant acts as an inhibitor of proteolysis via the UPS, and allowed us to uncover processes that are particularly sensitive to UPS perturbation. RESULTS: Expression of ubK48R during germination leads to seedling death. We analyzed the seedling transcriptome, proteome and metabolome 24 h post ubK48R induction and confirmed defects in chloroplast development. We found that mutations in single genes can suppress seedling lethality, indicating that a single process in seedlings is critically sensitive to decreased performance of the UPS. Suppressor mutations in phototropin 2 (PHOT2) suggest that a contribution of PHOT2 to chloroplast protection is compromised by proteolysis inhibition. CONCLUSIONS: Overall, the results reveal protein turnover as an integral part of a signal transduction chain that protects chloroplasts during development.

The green light gap: a window of opportunity for optogenetic control of stomatal movement.

Green plants are equipped with photoreceptors that are capable of sensing radiation in the ultraviolet-to-blue and the red-to-far-red parts of the light spectrum. However, plant cells are not particularly sensitive to green light (GL), and light which lies within this part of the spectrum does not efficiently trigger the opening of stomatal pores. Here, we discuss the current knowledge of stomatal responses to light, which are either provoked via photosynthetically active radiation or by specific blue light (BL) signaling pathways. The limited impact of GL on stomatal movements provides a unique option to use this light quality to control optogenetic tools. Recently, several of these tools have been optimized for use in plant biological research, either to control gene expression, or to provoke ion fluxes. Initial studies with the BL-activated potassium channel BLINK1 showed that this tool can speed up stomatal movements. Moreover, the GL-sensitive anion channel GtACR1 can induce stomatal closure, even at conditions that provoke stomatal opening in wild-type plants. Given that crop plants in controlled-environment agriculture and horticulture are often cultivated with artificial light sources (i.e. a combination of blue and red light from light-emitting diodes), GL signals can be used as a remote-control signal that controls stomatal transpiration and water consumption.

Molecular insights into the phototropin control of chloroplast movements.

Chloroplast movements are controlled by ultraviolet/blue light through phototropins. In Arabidopsis thaliana, chloroplast accumulation at low light intensities and chloroplast avoidance at high light intensities are observed. These responses are controlled by two homologous photoreceptors, the phototropins phot1 and phot2. Whereas chloroplast accumulation is triggered by both phototropins in a partially redundant manner, sustained chloroplast avoidance is elicited only by phot2. Phot1 is able to trigger only a small, transient chloroplast avoidance, followed by the accumulation phase. The source of this functional difference is not fully understood at either the photoreceptor or the signalling pathway levels. In this article, we review current understanding of phototropin functioning and try to dissect the differences that result in signalling to elicit two distinct chloroplast responses. First, we focus on phototropin structure and photochemical and biochemical activity. Next, we analyse phototropin expression and localization patterns. We also summarize known photoreceptor systems controlling chloroplast movements. Finally, we focus on the role of environmental stimuli in controlling phototropin activity. All these aspects impact the signalling to trigger chloroplast movements and raise outstanding questions about the mechanism involved.

Engineering the phototropin photocycle improves photoreceptor performance and plant biomass production.

The ability to enhance photosynthetic capacity remains a recognized bottleneck to improving plant productivity. Phototropin blue light receptors (phot1 and phot2) optimize photosynthetic efficiency in Arabidopsis thaliana by coordinating multiple light-capturing processes. In this study, we explore the potential of using protein engineering to improve photoreceptor performance and thereby plant growth. We demonstrate that targeted mutagenesis can decrease or increase the photocycle lifetime of Arabidopsis phototropins in vitro and show that these variants can be used to reduce or extend the duration of photoreceptor activation in planta Our findings show that slowing the phototropin photocycle enhanced several light-capturing responses, while accelerating it reduced phototropin's sensitivity for chloroplast accumulation movement. Moreover, plants engineered to have a slow-photocycling variant of phot1 or phot2 displayed increased biomass production under low-light conditions as a consequence of their improved sensitivity. Together, these findings demonstrate the feasibility of engineering photoreceptors to manipulate plant growth and offer additional opportunities to enhance photosynthetic competence, particularly under suboptimal light regimes.

Phylogenomics-Based Reconstruction and Molecular Evolutionary Histories of Brassica Photoreceptor Gene Families.

Photosensory proteins known as photoreceptors (PHRs) are crucial for delineating light environments in synchronization with other environmental cues and regulating their physiological variables in plants. However, this has not been well studied in the Brassica genus, which includes several important agricultural and horticultural crops. Herein, we identified five major PHR gene families-phytochrome (PHY), cryptochrome (CRY), phototropin (PHOT), F-box containing flavin binding proteins (ZTL/FKF1/LKP2), and UV RESISTANCE LOCUS 8 (UVR8)-genomic scales and classified them into subfamilies based on their phylogenetic clustering with Arabidopsis homologues. The molecular evolution characteristics of Brassica PHR members indicated indirect expansion and lost one to six gene copies at subfamily levels. The segmental duplication was possibly the driving force of the evolution and amplification of Brassica PHRs. Gene replication retention and gene loss events of CRY, PHY, and PHOT members found in diploid progenitors were highly conserved in their tetraploid hybrids. However, hybridization events were attributed to quantitative changes in UVR8 and ZTL/FKF1/LKP2 members. All PHR members underwent purifying selection. In addition, the transcript expression profiles of PHR genes in different tissue and in response to exogenous ABA, and abiotic stress conditions suggested their multiple biological significance. This study is helpful in understanding the molecular evolution characteristics of Brassica PHRs and lays the foundation for their functional characterization.

FERONIA is involved in phototropin 1-mediated blue light phototropic growth in Arabidopsis.

Plant shoot phototropism is triggered by the formation of a light-driven auxin gradient leading to bending growth. The blue light receptor phototropin 1 (phot1) senses light direction, but how this leads to auxin gradient formation and growth regulation remains poorly understood. Previous studies have suggested phot1's role for regulated apoplastic acidification, but its relation to phototropin and hypocotyl phototropism is unclear. Herein, we show that blue light can cause phot1 to interact with and phosphorylate FERONIA (FER), a known cell growth regulator, and trigger downstream phototropic bending growth in Arabidopsis hypocotyls. fer mutants showed defects in phototropic growth, similar to phot1/2 mutant. FER also interacts with and phosphorylates phytochrome kinase substrates, the phot1 downstream substrates. The phot1-FER pathway acts upstream of apoplastic acidification and the auxin gradient formation in hypocotyl under lateral blue light, both of which are critical for phototropic bending growth in hypocotyls. Our study highlights a pivotal role of FER in the phot1-mediated phototropic cell growth regulation in plants.