Shining Light on the Function of NPH3/RPT2-Like Proteins in Phototropin Signaling

Christie, John M.; Suetsugu, Noriyuki; Sullivan, Stuart; Wada, Masamitsu

doi:10.1104/pp.17.00835

Cited by 59 publications

(100 citation statements)

References 82 publications

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“…Unlike locally controlled short-term responses, longterm acclimation can be observed in both local and distant tissues. Elongation growth of palisade cells is locally controlled via UV-A and blue light photoreceptor phototropins (Kozuka et al, 2011), which also regulate short-term responses of chloroplast movement and stomatal opening (Christie et al, 2018). In contrast, formation of extra palisade cell layers has been seen in leaf primordia and young growing leaves when mature leaves are exposed to HL (Terashima et al, 2006).…”

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confidence: 99%

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

et al. 2019

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Natural light environments are highly variable. Flexible adjustment between light energy utilization and photoprotection is therefore of vital importance for plant performance and fitness in the field. Short-term reactions to changing light intensity are triggered inside chloroplasts and leaves within seconds to minutes, whereas long-term adjustments proceed over hours and days, integrating multiple signals. While the mechanisms of long-term acclimation to light intensity have been studied by changing constant growth light intensity during the day, responses to fluctuating growth light intensity have rarely been inspected in detail. We performed transcriptome profiling in Arabidopsis (Arabidopsis thaliana) leaves to investigate long-term gene expression responses to fluctuating light (FL). In particular, we examined whether responses differ between young and mature leaves or between morning and the end of the day. Our results highlight global reprogramming of gene expression under FL, including that of genes related to photoprotection, photosynthesis, and photorespiration and to pigment, prenylquinone, and vitamin metabolism. The FL-induced changes in gene expression varied between young and mature leaves at the same time point and between the same leaves in the morning and at the end of the day, indicating interactions of FL acclimation with leaf development stage and time of day. Only 46 genes were up-or down-regulated in both young and mature leaves at both time points. Combined analyses of gene coexpression and cis-elements pointed to a role of the circadian clock and light in coordinating the acclimatory responses of functionally related genes. Our results also suggest a possible cross talk between FL acclimation and systemic acquired resistance-like gene expression in young leaves.Adjustments of photosynthetic light energy utilization and photoprotection to changing light intensity are triggered over different time scales. Rapid changes (seconds to minutes) are induced inside chloroplasts by reduction of electron transport chain or upon formation of a [H + ] gradient (DpH) across the thylakoid membrane. Short-term responses have been studied intensively to unveil various regulatory mechanisms involved therein. Reduction of the plastoquinone (PQ) pool by preferential excitation of PSII relative to PSI, for example, leads to activation of thylakoid protein kinase STN7, which phosphorylates PSII light-harvesting complex (LHC) to trigger its displacement from PSII to PSI in a process termed state transition (Bellafiore et al., 2005). Light-dependent acidification of thylakoid lumen protonates the PSBS protein to quickly induce thermal energy dissipation (or nonphotochemical quenching [NPQ]) and thus down-regulate PSII (Li et al., 2000). Lumen acidification also activates a xanthophyll-cycle enzyme, violaxanthin deepoxidase (VDE), to convert violaxanthin to antheraxanthin and zeaxanthin, which enhances NPQ (Niyogi et al., 1998). Furthermore, alternative electron (e 2 ) flows (e.g. waterwater cycle and cyclic e 2...

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confidence: 99%

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

et al. 2019

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“…How this lateral auxin gradient forms in response to phot activation is still not understood (Fankhauser and Christie, 2015). However, members of the NON-PHOTOTROPIC HYPOCOTYL3 (NPH3)/ROOT PHOTOTROPISM2 (RPT2)-like (NRL) family are known to play important roles (Christie et al, 2018).…”

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confidence: 99%

Deetiolation Enhances Phototropism by Modulating NON-PHOTOTROPIC HYPOCOTYL3 Phosphorylation Status

Sullivan

Kharshiing²,

Laird

et al. 2019

Plant Physiol.

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Phototropin (phot) receptor kinases play important roles in promoting plant growth by controlling light-capturing processes, such as phototropism. Phototropism is mediated through the action of NON-PHOTOTROPIC HYPOCOTYL3 (NPH3), which is dephosphorylated following phot activation. However, the functional significance of this early signaling event remains unclear. Here, we show that the onset of phototropism in dark-grown (etiolated) seedlings of Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) is enhanced by greening (deetiolation). Red and blue light were equally effective in promoting phototropism in Arabidopsis, consistent with our observations that deetiolation by phytochrome or cryptochrome was sufficient to enhance phototropism. Increased responsiveness did not result from an enhanced sensitivity to the phytohormone auxin, nor does it involve the phot-interacting protein, ROOT PHOTOTROPISM2. Instead, deetiolated seedlings showed attenuated levels of NPH3 dephosphorylation and diminished relocalization of NPH3 from the plasma membrane during phototropism. Likewise, etiolated seedlings that lack the PHYTOCHROME-INTERACTING FACTORS (PIFs) PIF1, PIF3, PIF4, and PIF5 displayed reduced NPH3 dephosphorylation and enhanced phototropism, consistent with their constitutive photomorphogenic phenotype in darkness. Phototropic enhancement could also be achieved in etiolated seedlings by lowering the light intensity to diminish NPH3 dephosphorylation. Thus, phototropism is enhanced following deetiolation through the modulation of a phosphorylation rheostat, which in turn sustains the activity of NPH3. We propose that this dynamic mode of regulation enables young seedlings to maximize their establishment under changing light conditions, depending on their photoautotrophic capacity.

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“…It is critical for a multi-organ plant to position itself relative to the Earth (gravitropism) and the sun (phototropism) for proper development, as well as the means to communicate between the different parts of the organism through systemic signaling (Vandenbrink et al 2014). Wolffia has lost many genes of the NPH3/RPT2-Like family (NRL),which are required for several auxin-mediated growth processes, including phototropism (root and shoot), petiole positioning, leaf expansion, chloroplast accumulation, stomatal opening and circadian control of PSII photosynthetic efficiency (Christie et al 2018). NPH3 is the founding member of the NRL family with a close paralog DOT3 that fail to exhibit phototropism and have aberrant venation patterning in Arabidopsis mutants respectively (Petricka et al 2008;Motchoulski and Liscum 1999).…”

Section: Discussionmentioning

confidence: 99%

Genome and time-of-day transcriptome of Wolffia australiana link morphological extreme minimization with un-gated plant growth

Michael

Ernst

Hartwick

et al. 2020

Preprint

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Wolffia is the fastest growing plant genus on Earth with a recorded doubling time of less than a day. Wolffia has a dramatically reduced body plan, primarily growing through a continuous, budding-type asexual reproduction with no obvious phase transition. Most plants are bound by the 24-hour light-dark cycle with the majority of processes such as gene expression partitioned or phased to a specific time-of-day (TOD). However, the role that TOD information and the circadian clock plays in facilitating the growth of a fast-growing plant is unknown. Here we generated draft reference genomes for Wolffia australiana (Benth.) Hartog & Plas to monitor gene expression over a two-day time course under light-dark cycles. Wolffia australiana has the smallest genome size in the genus at 357 Mb and has a dramatically reduced gene set at 15,312 with a specific loss of root (WOX5), vascular (CASP), circadian (TOC1), and light-signaling (NPH3) genes. Remarkably, it has also lost all but one of the NLR genes that are known to be involved in innate immunity. In addition, only 13% of its genes cycle, which is far less than in other plants, with an overrepresentation of genes associated with carbon processing and chloroplast-related functions. Despite having a focused set of cycling genes, TOD cis-elements are conserved in W. australiana, consistent with the overall conservation of transcriptional networks. In contrast to the model plants Arabidopsis thaliana and Oryza sativa, the reduction in cycling genes correlates with fewer pathways under TOD control in Wolffia, which could reflect a release of functional gating. Since TOD networks and the circadian clock work to gate activities to specific times of day, this minimization of regulation may enable Wolffia to grow continuously with optimal economy. Wolffia is an ideal model to study the transcriptional control of growth and the findings presented here could serve as a template for plant improvement.

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Shining Light on the Function of NPH3/RPT2-Like Proteins in Phototropin Signaling

Cited by 59 publications

References 82 publications

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

Deetiolation Enhances Phototropism by Modulating NON-PHOTOTROPIC HYPOCOTYL3 Phosphorylation Status

Genome and time-of-day transcriptome of Wolffia australiana link morphological extreme minimization with un-gated plant growth

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