Antony N. Dodd

Circadian Control of Chloroplast Transcription by a Nuclear-Encoded Timing Signal

Synchronizing Photosynthetic Capacity Coordination of photosynthetic activity with sunlight benefits plant productivity. Noordally et al. (p. 1316) analyzed how the Arabidopsis circadian clock keeps the chloroplasts working in tune with the Sun. SIGMA FACTOR5 (SIG5) is encoded in the cell nucleus and reflects circadian cycles with changes in its own transcript abundance. SIG5 acts, however, in the chloroplast, where it supports photosystem II production. In plants, day/night information is communicated from a nuclear-encoded circadian oscillator to the chloroplast. Circadian timekeeping in plants increases photosynthesis and productivity. There are circadian oscillations in the abundance of many chloroplast-encoded transcripts, but it is not known how the circadian clock regulates chloroplast transcription or the photosynthetic apparatus. We show that, in Arabidopsis, nuclear-encoded SIGMA FACTOR5 (SIG5) controls circadian rhythms of transcription of several chloroplast genes, revealing one pathway by which the nuclear-encoded circadian oscillator controls rhythms of chloroplast gene expression. We also show that SIG5 mediates the circadian gating of light input to a chloroplast-encoded gene. We have identified an evolutionarily conserved mechanism that communicates circadian timing information between organelles with distinct genetic systems and have established a new level of integration between eukaryotic circadian clocks and organelles of endosymbiotic origin.

The circadian clock has transient plasticity of period and is required for timing of nocturnal processes in Arabidopsis

A circadian rhythm matched to the phase and period of the day-night cycle has measurable benefits for land plants. We assessed the contribution of circadian period to the phasing of cellular events with the light : dark cycle. We also investigated the plasticity of circadian period within the Arabidopsis circadian oscillator. We monitored the circadian oscillator in wild-type and circadian period mutants under light : dark cycles of varying total duration. We also investigated changes in oscillator dynamics during and after the transition from light : dark cycles to free running conditions. Under light : dark cycles, dawn and dusk were anticipated differently when the circadian period was not resonant with the environmental period (T cycle). Entrainment to T cycles differing from the free-running period caused a short-term alteration in oscillator period. The transient plasticity of period was described by existing mathematical models of the Arabidopsis circadian network. We conclude that a circadian period resonant with the period of the environment is particularly important for anticipation of dawn and the timing of nocturnal events; and there is short-term and transient plasticity of period of the Arabidopsis circadian network.

The circadian regulation of photosynthesis

Correct circadian regulation increases plant productivity, and photosynthesis is circadian-regulated. Here, we discuss the regulatory basis for the circadian control of photosynthesis. We discuss candidate mechanisms underpinning circadian oscillations of light harvesting and consider how the circadian clock modulates CO2 fixation by Rubisco. We show that new techniques may provide a platform to better understand the signalling pathways that couple the circadian clock with the photosynthetic apparatus. Finally, we discuss how understanding circadian regulation in model systems is underpinning research into the impact of circadian regulation in crop species.

Interactions between circadian clocks and photosynthesis for the temporal and spatial coordination of metabolism

All plant productivity, including the food that we eat, arises from the capture of solar energy by plants. At most latitudes sunlight is available for only part of the 24 h day due to the rotation of the planet. This rhythmic and predictable alteration in the environment has driven the evolution of the circadian clock, which has an extremely pervasive influence upon plant molecular biology, physiology and phenology. A number of recent studies have demonstrated that the circadian clock is integrated very closely with photosynthesis and its metabolic products. We consider the coupling of the circadian oscillator with carbohydrate biochemistry and the connections between the nuclear-encoded circadian clock and processes within chloroplasts. We describe how this might provide adaptations to optimize plant performance in an environment that varies both predictably upon a daily and seasonal basis, and unpredictably due to the weather.

NO-Mediated [Ca2+]cyt Increases Depend on ADP-Ribosyl Cyclase Activity in Arabidopsis

ADP-ribosyl cyclase activity in Arabidopsis is up-regulated by nitric oxide to increase the cellular concentration of cyclic ADP ribose and free Ca2+. Cyclic ADP ribose (cADPR) is a Ca2+-mobilizing intracellular second messenger synthesized from NAD by ADP-ribosyl cyclases (ADPR cyclases). In animals, cADPR targets the ryanodine receptor present in the sarcoplasmic/endoplasmic reticulum to promote Ca2+ release from intracellular stores to increase the concentration of cytosolic free Ca2+ in Arabidopsis (Arabidopsis thaliana), and cADPR has been proposed to play a central role in signal transduction pathways evoked by the drought and stress hormone, abscisic acid, and the circadian clock. Despite evidence for the action of cADPR in Arabidopsis, no predicted proteins with significant similarity to the known ADPR cyclases have been reported in any plant genome database, suggesting either that there is a unique route for cADPR synthesis or that a homolog of ADPR cyclase with low similarity might exist in plants. We sought to determine whether the low levels of ADPR cyclase activity reported in Arabidopsis are indicative of a bona fide activity that can be associated with the regulation of Ca2+ signaling. We adapted two different fluorescence-based assays to measure ADPR cyclase activity in Arabidopsis and found that this activity has the characteristics of a nucleotide cyclase that is activated by nitric oxide to increase cADPR and mobilize Ca2+.

Integration of light and circadian signals that regulate chloroplast transcription by a nuclear-encoded sigma factor

Summary We investigated the signalling pathways that regulate chloroplast transcription in response to environmental signals. One mechanism controlling plastid transcription involves nuclear‐encoded sigma subunits of plastid‐encoded plastid RNA polymerase. Transcripts encoding the sigma factor SIG5 are regulated by light and the circadian clock. However, the extent to which a chloroplast target of SIG5 is regulated by light‐induced changes in SIG5 expression is unknown. Moreover, the photoreceptor signalling pathways underlying the circadian regulation of chloroplast transcription by SIG5 are unidentified. We monitored the regulation of chloroplast transcription in photoreceptor and sigma factor mutants under controlled light regimes in Arabidopsis thaliana. We established that a chloroplast transcriptional response to light intensity was mediated by SIG5; a chloroplast transcriptional response to the relative proportions of red and far red light was regulated by SIG5 through phytochrome and photosynthetic signals; and the circadian regulation of chloroplast transcription by SIG5 was predominantly dependent on blue light and cryptochrome. Our experiments reveal the extensive integration of signals concerning the light environment by a single sigma factor to regulate chloroplast transcription. This may originate from an evolutionarily ancient mechanism that protects photosynthetic bacteria from high light stress, which subsequently became integrated with higher plant phototransduction networks.

Circadian regulation of chloroplasts

Circadian rhythms produce a biological measure of time that increases plant performance. The mechanisms that underlie this increase in productivity require investigation to provide information that will underpin future crop improvement. There is a growing body of evidence that a sophisticated signalling network interconnects the circadian oscillator and chloroplasts. We consider this in the context of circadian signalling to chloroplasts and the relationship between retrograde signalling and circadian regulation. We place circadian signalling to chloroplasts by sigma factors within an evolutionary context. We describe selected recent developments in the integration of light and circadian signals that control chloroplast gene expression.

The energy-signalling hub SnRK1 is important for sucrose-induced hypocotyl elongation

An energy signaling pathway, photoperiod, and light intensity regulate sugar-induced hypocotyl elongation. Emerging seedlings respond to environmental conditions such as light and temperature to optimize their establishment. Seedlings grow initially through elongation of the hypocotyl, which is regulated by signaling pathways that integrate environmental information to regulate seedling development. The hypocotyls of Arabidopsis (Arabidopsis thaliana) also elongate in response to sucrose. Here, we investigated the role of cellular sugar-sensing mechanisms in the elongation of hypocotyls in response to Suc. We focused upon the role of SnRK1, which is a sugar-signaling hub that regulates metabolism and transcription in response to cellular energy status. We also investigated the role of TPS1, which synthesizes the signaling sugar trehalose-6-P that is proposed to regulate SnRK1 activity. Under light/dark cycles, we found that Suc-induced hypocotyl elongation did not occur in tps1 mutants and overexpressors of KIN10 (AKIN10/SnRK1.1), a catalytic subunit of SnRK1. We demonstrate that the magnitude of Suc-induced hypocotyl elongation depends on the day length and light intensity. We identified roles for auxin and gibberellin signaling in Suc-induced hypocotyl elongation under short photoperiods. We found that Suc-induced hypocotyl elongation under light/dark cycles does not involve another proposed sugar sensor, HEXOKINASE1, or the circadian oscillator. Our study identifies novel roles for KIN10 and TPS1 in mediating a signal that underlies Suc-induced hypocotyl elongation in light/dark cycles.

UV-B antagonises shade avoidance and increases levels of the flavonoid quercetin in coriander (Coriandrum sativum)

Despite controlling a diverse array of regulatory processes in plants, UV-B wavelengths (280–315u2009nm) are attenuated by common greenhouse materials such as glass and polycarbonate and are therefore depleted in many commercial growing environments. In this study, we analysed the architecture, pigment accumulation and antioxidant capacity of coriander (Coriandrum sativum, also known as cilantro) plants grown with and without supplementary UV-B (1.5 µmol m−2 s−1). We demonstrate that UV-B limits stem elongation responses to neighbour proximity perception (shade avoidance), promoting a more compact plant architecture. In addition, UV-B increased leaf quercetin content and total antioxidant capacity. Arabidopsis thaliana mutants deficient in flavonoid biosynthesis were not impaired in shade avoidance inhibition, suggesting that UV-B-induced flavonoid synthesis is not a component of this response. Our results indicate that UV-B supplementation may provide a method to manipulate the architecture, flavour and nutritional content of potted herbs whilst reducing the deleterious impacts of dense planting on product quality.

A new link between plant metabolism and circadian rhythms

The rotation of the Earth around its axis generates 24 h cycles of environmental change, such as daily rhythms of light and temperature. Circadian clocks, cellular biological oscillators that generate 24-hour rhythms of gene expression and metabolism, are thought to synchronize the functioning of organisms with these daily environmental changes. Circadian regulation enables organisms to anticipate environmental changes such as dawn and dusk, and co-ordinate their metabolism, physiology and behaviour with daily changes in the environment. This is particularly important for plants, which cannot move to escape environmental challenges.