Our Work

Work published as an independent group is listed below. A complete list of work I've contributed to can be found here.

REVEILLE2 thermosensitive splicing: a molecular basis for the integration of nocturnal temperature information by the Arabidopsis circadian clock

Allan James, Tally Sharples, Janet Laird, Emily May Armstrong, Wenbin Guo, Nikoleta Tzioutziou, Runxuan Zhang, John Brown, Hugh Nimmo, Matt Jones

Cold stress is one of the major environmental factors that limit growth and yield of plants. However, it is still not fully understood how plants account for daily temperature fluctuations, nor how these temperature changes are integrated with other regulatory systems such as the circadian clock. We demonstrate that REVEILLE2 undergoes alternative splicing after chilling that increases accumulation of a transcript isoform encoding a MYB-like transcription factor. We explore the biological function of REVEILLE2 in Arabidopsis thaliana using a combination of molecular genetics, transcriptomics, and physiology. Disruption of REVEILLE2 alternative splicing alters regulatory gene expression, impairs circadian timing, and improves photosynthetic capacity. Changes in nuclear gene expression are particularly apparent in the initial hours following chilling, with chloroplast gene expression subsequently upregulated. The response of REVEILLE2 to chilling extends our understanding of plants immediate response to cooling. We propose that the circadian component REVEILLE2 restricts plants responses to nocturnal reductions in temperature, thereby enabling appropriate responses to daily environmental changes.

The published version can be found here- New Phytologist.

Inhibition of RNA degradation integrates the metabolic signals induced by osmotic stress into the Arabidopsis circadian system

Putri Prasetyaningrum, Suzanne Litthauer, Franco Vegliani, Martin Battle, Matthew Wood, Xinmeng Liu, Cathryn Dickson, Matt Jones

The circadian clock system acts as an endogenous timing reference that coordinates many metabolic and physiological processes in plants. Previous studies have shown that the application of osmotic stress delays circadian rhythms via 3'-phospho-adenosine 5'-phosphate (PAP), a retrograde signalling metabolite that is produced in response to redox stress within organelles. PAP accumulation leads to the inhibition of exoribonucleases (XRNs), which are responsible for RNA degradation. Interestingly, we are now able to demonstrate that post-transcriptional processing is crucial for the circadian response to osmotic stress. Our data show that osmotic stress increases the stability of specific circadian RNAs, suggesting that RNA metabolism plays a vital role in circadian clock coordination during drought. Inactivation of XRN4 is sufficient to extend circadian rhythms as part of this response, with PRR7 and LWD1 identified as transcripts that are post-transcriptionally regulated to delay circadian progression.

The published version can be found here- J Exp Bot.

Interactions between photosynthesis and the circadian system

Marina Viana Queiroz, Martin Battle, Matt Jones

The rising and setting of the sun provides a regular transition between two starkly different environmental conditions for photosynthetic organisms such as plants. Since photosynthetic organisms rely on light as both an environmental signal and an energy source it is beneficial for plants to respond to and utilize light in a time-dependent manner. This timing information is provided by the circadian system, a complex biological oscillator that provides an internal reference that can be used to modify plants’ responses to light signals. In this review, we will discuss how the circadian system regulates photosynthetic processes, while also exploring how photosynthetic products can themselves feed into the circadian system to optimise interactions between plants and their environment.

The published version can be found here- Burleigh Dodds Science Publishing.

Realising the Environmental Potential of Vertical Farming Systems through Advances in Plant Photobiology

Matthieu de Carbonnel, John Sormonth-Darling, Weiqi Liu, Dmytro Kuziak, Matt Jones

Intensive agriculture is essential to feed increasing populations, yet requires large amounts of pesticide, fertiliser, and water to maintain productivity. One solution to mitigate these issues is the adoption of Vertical Farming Systems (VFS). The self-contained operation of these facilities offers the potential to recycle agricultural inputs, as well as sheltering crops from the effects of climate change. Recent technological advancements in light-emitting diode (LED) lighting technology have enabled VFS to become a commercial reality, although high electrical consumption continues to tarnish the environmental credentials of the industry. In this review, we examine how the inherent use of electricity by VFS can be leveraged to deliver commercial and environmental benefits. We propose that an understanding of plant photobiology can be used to vary VFS energy consumption in coordination with electrical availability from the grid, facilitating demand-side management of energy supplies and promoting crop yield.

The published version can be found here- MDPI Biology.

Diverse Physiological and Physical Responses among Wild, Landrace and Elite Barley Varieties Point to Novel Breeding Opportunities

Jim Stevens, Matt Jones, Tracy Lawson

Climate change from elevated [CO 2] may reduce water availability to crops through changes in precipitation and higher temperatures. However, agriculture already accounts for 70% of human consumption of water. Stomata, pores in the leaf surface, mediate exchange of water and CO 2 for the plant. In crops including barley, the speed of stomatal response to changing environmental conditions is as important as maximal responses and can thus affect water use efficiency. Wild barleys and landraces which predate modern elite lines offer …

The published version can be found here- MDPI Agronomy.

Plant Defence Mechanisms Are Modulated by the Circadian System

Ghazala Butt, Zainab Qayyum, Matt Jones

Plant health is an important aspect of food security, with pathogens, pests, and herbivores all contributing to yield losses in crops. Plants' defence against pathogens is complex and utilises several metabolic processes, including the circadian system, to coordinate their response. In this review, we examine how plants' circadian rhythms contribute to defence mechanisms, particularly in response to bacterial pathogen attack. Circadian rhythms contribute to many aspects of the plant-pathogen interaction, although significant gaps in our understanding remain to be explored. We conclude that if these relationships are explored further, better disease management strategies could be revealed.

The published version can be found here- MDPI Biology.

Shades of Green: Untying the Knots of Green Photoperception

Martin Battle, Franco Vegliani, and Matt Jones

The development of economical LED technology has enabled the application of different light qualities and quantities to control plant growth. Although we have a comprehensive understanding of plants’ perception of red and blue light, the lack of a dedicated green light sensor has frustrated our utilisation of intermediate wavelengths, with many contradictory reports in the literature. We discuss the contribution of red and blue photoreceptors to green light perception and highlight how green light can be used to improve crop quality. Importantly, our meta-analysis demonstrates that green light perception should instead be considered as a combination of distinct ‘green-’ and ‘yellow-’light induced responses. This distinction will enable clearer interpretation of plants’ behaviour in response to green light as we seek to optimise plant growth and nutritional quality in horticultural contexts.

The published version can be found here- J Exp Bot.

Cryptochromes Integrate Green Light Signals into the Circadian System

Martin Battle and Matt Jones

Plants are acutely sensitive of their light environment, adapting their growth habit and prioritizing developmental decisions to maximize fecundity. In addition to providing an energy source and directional information, light quality also contributes to entrainment of the circadian system, an endogenous timing mechanism that integrates endogenous and environmental signaling cues to promote growth. While plants’ perception of red and blue portions of the spectrum are well defined, green light sensitivity remains enigmatic. In this study we show that low fluence rates of green light are sufficient to entrain and maintain circadian rhythms in Arabidopsis, and that cryptochromes contribute to this response. Importantly, green light responses are distinguishable from low blue light‐induced phenotypes. These data suggest a distinct signaling mechanism enables entrainment of the circadian system in green light‐enriched environments, such as those found in undergrowth and in densely planted monoculture.

The published version can be found here- Plant, Cell and Environment.

Arabidopsis JMJD5/JMJ30 Acts Independently of LUX ARRHYTHMO Within the Plant Circadian Clock to Enable Temperature Compensation

Matt Jones, Kengo Morohashi, Erich Grotewold, and Stacey Harmer

The circadian system ensures that plants respond appropriately to environmental change by predicting regular transitions that occur during diel cycles. In order to be most useful, the circadian system needs to be compensated against daily and seasonal changes in temperature that would otherwise alter the pace of this biological oscillator. We demonstrate that an evening-phased protein, the putative histone demethylase JMJD5, contributes to temperature compensation. JMJD5 is co-expressed with components of the Evening Complex, an agglomeration of proteins including EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHYMO (LUX), which also integrates temperature changes into the molecular clockwork. One role of the Evening Complex is to regulate expression of PSEUDORESPONSE REGULATOR9 (PRR9) and PRR7, important components of the temperature compensation mechanism. Surprisingly we find that LUX, but not other Evening Complex components, is dispensable for clock function at low temperatures. Further genetic analysis suggests JMJD5 acts in a parallel pathway to LUX within the circadian system. Although an intact JMJD5 catalytic domain is required for its function within the clock, our findings suggest JMJD5 does not directly regulate H3K36 methylation at circadian loci. Such data refine our understanding of how JMDJ5 acts within the Arabidopsis circadian system.

The published version can be found here- Frontiers in Plant Science.

Retrograde signalling as an informant of circadian timing

Matt Jones

The circadian system comprises of interlocking transcriptional–translational feedback loops that regulate gene expression and consequently modulate plant development and physiology. In order to maximize utility, the circadian system is entrained by changes in temperature and light, allowing endogenous rhythms to be synchronized with both daily and seasonal environmental change. While a great deal of environmental information is decoded by a suite of photoreceptors, it is also becoming apparent that changes in cellular metabolism also contribute to circadian timing, either through the stimulation of metabolic pathways or through the accumulation of metabolic intermediates as a consequence of environmental stress. As the source of many of these metabolic byproducts, mitochondria and chloroplasts have begun to be viewed as environmental sensors, and rapid advancement of this field is revealing the complex web of signalling pathways initiated by organelle perturbation. This review will highlight recent advances in our understanding of how this metabolic regulation influences circadian timing.

The published version can be found here- New Phytologist.

Using light to improve commercial value

Matt Jones

The plasticity of plant morphology has evolved to maximize reproductive fitness in response to prevailing environmental conditions. Leaf architecture elaborates to maximize light harvesting, while the transition to flowering can either be accelerated or delayed to improve an individual’s fitness. One of the most important environmental signals is light, with plants using light for both photosynthesis and as an environmental signal. Plants perceive different wavelengths of light using distinct photoreceptors. Recent advances in LED technology now enable light quality to be manipulated at a commercial scale, and as such opportunities now exist to take advantage of plants’ developmental plasticity to enhance crop yield and quality through precise manipulation of a crop's lighting regime. This review will discuss how plants perceive and respond to light, and consider how these specific signaling pathways can be manipulated to improve crop yield and quality.

The published version can be found here- Horticulture Research.

SAL1-PAP retrograde signalling extends circadian period by reproducing the loss of exoribonuclease (XRN) activity

Suzanne Litthauer and Matt Jones

Plants have developed an internal timing mechanism, the circadian system, that serves to synchronise physiological and metabolic functions with daily cues such as dawn and dusk, and provides plants with an advantage in adapting to changing and challenging conditions. We have recently shown that the SAL1-PAP-XRN retrograde signalling pathway, which is proposed to regulate plant responses under stress conditions, also acts within the circadian system. Here we provide further evidence of circadian regulation by SAL1-PAP-XRN signalling, thereby affirming a link between molecular timekeeping and abiotic stress response mechanisms.

The published version can be found here- Plant Signalling & Behaviour.

Offprint copies of the final version are available on request, but cannot be posted online due to licensing restrictions- Contact me.

3'-Phosphoadenosine 5'-Phosphate Accumulation Delays the Circadian System

Suzanne Litthauer, Kai X Chan, and Matt Jones

The circadian system optimizes cellular responses to stress, but the signaling pathways that convey the metabolic consequences of stress into this molecular timekeeping mechanism remain unclear. Redox regulation of the SAL1 phosphatase during abiotic stress initiates a signaling pathway from chloroplast to nucleus by regulating the accumulation of a metabolite, 3'-phosphoadenosine 5'-phosphate (PAP). Consequently, PAP accumulates in response to redox stress and inhibits the activity of exoribonucleases (XRNs) in the nucleus and cytosol. We demonstrated that osmotic stress induces a lengthening of circadian period and that genetically inducing the SAL1-PAP-XRN pathway in plants lacking either SAL1 or XRNs similarly delays the circadian system. Exogenous application of PAP was also sufficient to extend circadian period. Thus, SAL1-PAP-XRN signaling likely regulates circadian rhythms in response to redox stress. Our findings exemplify how two central processes in plants, molecular timekeeping and responses to abiotic stress, can be interlinked to regulate gene expression.

The published version can be found here- Plant Physiology.

Interplay of Circadian Rhythms and Light in the Regulation of Photosynthesis-Derived Metabolism

Matt Jones

Alternating periods of day and night confer an environmental rhythm upon terrestrial plants. Seasonal changes in light intensity and duration (as well as integrals of temperature) inform developmental decisions that directly impact upon plant growth. In response to the selective pressure of these daily rhythms, plants have evolved an endogenous, biological oscillator that coincides with these patterns. These circadian rhythms allow plants to anticipate daily transitions and consequently allocate specific metabolic functions to certain times of day. The circadian system also has a dramatic effect upon development, with the external coincidence model describing how plants measure day length to induce flowering under inductive conditions. Plants’ responses to environmental change are therefore a distillation of direct responses to abiotic factors and moderating factors derived from endogenous biological rhythms. This review summarizes our understanding of how metabolic processes are governed by these interactions, with particular attention to carbon and redox metabolism, two processes derived from photosynthesis.

The published version can be found here- Springer.

Offprint copies of the final version are available on request, but cannot be posted online due to licensing restrictions- Contact me.

Natural Variation Of Circadian Rhythms In Kalanchoë Species

Kathryn Malpas and Matt Jones

Plants have evolved an internal body clock- the circadian system- that allows the optimization of behavior during the day by anticipating regular environmental change. This timing mechanism also serves as an internal reference to control flowering time. One observable consequence of the circadian system is the rhythmic regulation of processes that underlie photosynthesis, which persists after plants are transferred to constant conditions. Many cacti and succulents use Crassulacean Acid Metabolism (CAM) as a modification of the predominant C3 method of photosynthesis to limit water loss. CAM allows the temporal separation of carbon capture from the atmosphere and the Calvin-Benson cycle, and so separates stomatal opening from some of the biochemical aspects of photosynthesis. Here we document the diversity of circadian rhythms in several Kalanchoë species and reveal differences in the period, phase and amplitude of circadian outputs derived from regulation of the photosynthetic apparatus.

The published version can be found here- Haseltonia.

Offprint copies of the final version are available on request, but cannot be posted online due to licensing restrictions- Contact me.

Phototropins do not Alter Accumulation of Evening-phased Circadian Transcripts Under Blue Light

Suzanne Litthauer, Martin Battle and Matt Jones

A short addendum to our first phototropin paper (below). The circadian system induces rhythmic variation in a suite of biochemical and physiological processes that serves to optimise plant growth in diel cycles. To be of greatest utility, these rhythmic behaviours are coordinated with regular environmental changes such as the rising and setting of the sun. Photoreceptors, and metabolites produced during photosynthesis, act to synchronise the internal timing mechanism with lighting cues. We have recently shown that phototropins help maintain robust rhythms of photosynthetic operating efficiency (ϕPSII or Fq'/Fm') under blue light, although rhythmic accumulation of morning-phased circadian transcripts in the nucleus was unaffected. Here we report that evening-phased nuclear clock transcripts were also unaffected. We also observe that rhythms of nuclear clock transcript accumulation are maintained in phototropin mutant plants under a fluctuating lighting regime that induced a loss of Fq'/Fm' rhythms.

The published version can be found here- Plant Signalling & Behaviour.

Phototropins Maintain Robust Circadian Oscillation of PSII Operating Efficiency Under Blue Light

Suzanne Litthauer, Martin Battle, Tracy Lawson, and Matt Jones

Measurement of circadian rhythms of PSII operating efficiency in the chloroplast reveals a distinct physiological circadian output compared to previously reported delayed fluorescence methods. Phototropins are required for the maintenance of these chlorophyll fluorescence rhythms under dim blue light (while not affecting rhythms of nuclear gene expression) via a signalling cascade independent of NPH3.

The published version can be found here- The Plant Journal.

A Constitutively Active Allele of Phytochrome B Maintains Circadian Robustness in the Absence of Light

Matt Jones, Wei Hu, Suzanne Litthauer, J. Clark Lagarias, and Stacey Harmer

The sensitivity of the circadian system to light allows entrainment of the clock, permitting coordination of plant metabolic function and flowering time across seasons. Light affects the circadian system both via photoreceptors, such as phytochromes and cryptochromes, and sugar production by photosynthesis. In the present studies, we introduce a constitutively active version of phytochrome B (phyB-Y276H, YHB) into both wild-type and phytochrome null backgrounds of Arabidopsis thaliana to distinguish the effects of photoreceptor signalling on clock function from those of photosynthesis. We find that the YHB mutation is sufficient to phenocopy red light input into the circadian mechanism and to sustain robust rhythms in steady-state mRNA levels even in plants grown without light or exogenous sugars. The pace of the clock is insensitive to light intensity in YHB plants, indicating that light input to the clock is constitutively activated by this allele. Mutation of YHB so that it is retained in the cytoplasm abrogates its effects on clock function, indicating that nuclear localization of phytochrome is necessary for its clock regulatory activity. We also demonstrate a role for phytochrome C as part of the red light sensing network that modulates phytochrome B signalling input into the circadian system. Our findings indicate that phytochrome signaling in the nucleus plays a critical role in sustaining robust clock function under red light, even in the absence of photosynthesis or exogenous sources of energy.

The published version can be found here- Plant Physiology.

Mutation of Arabidopsis SPLICEOSOMAL TIMEKEEPER LOCUS1 Causes Circadian Clock Defects

Matt Jones, Brian Williams, Jim McNicol, Craig G. Simpson, John W. S. Brown, and Stacey Harmer

The circadian clock plays a crucial role in coordinating plant metabolic and physiological functions with predictable environmental variables, such as dusk and dawn, while also modulating responses to biotic and abiotic challenges. Much of the initial characterization of the circadian system has focused on transcriptional initiation, but it is now apparent that considerable regulation is exerted after this key regulatory step. Transcript processing, protein stability, and cofactor availability have all been reported to influence circadian rhythms in a variety of species. We used a genetic screen to identify a mutation within a putative RNA binding protein (SPLICEOSOMAL TIMEKEEPER LOCUS1 [STIPL1]) that induces a long circadian period phenotype under constant conditions. STIPL1 is a homolog of the spliceosomal proteins TFP11 (Homo sapiens) and Ntr1p (Saccharomyces cerevisiae) involved in spliceosome disassembly. Analysis of general and alternative splicing using a high-resolution RT-PCR system revealed that mutation of this protein causes less efficient splicing of most but not all of the introns analyzed. In particular, the altered accumulation of circadian-associated transcripts may contribute to the observed mutant phenotype. Interestingly, mutation of a close homolog of STIPL1, STIP-LIKE2, does not cause a circadian phenotype, which suggests divergence in function between these family members. Our work highlights the importance of posttranscriptional control within the clock mechanism.

The published version can be found here- Plant Cell.