Cycling of clock genes entrained to the solar rhythm enables plants to tell time: data from arabidopsis

Background and Aims An endogenous rhythm synchronized to dawn cannot time photosynthesis-linked genes to peak consistently at noon since the interval between sunrise and noon changes seasonally. In this study, a solar clock model that circumvents this limitation is proposed using two daily timing references synchronized to noon and midnight. Other rhythmic genes that are not directly linked to photosynthesis, and which peak at other times, also find an adaptive advantage in entrainment to the solar rhythm.Methods Fourteen datasets extracted from three published papers were used in a meta-analysis to examine the cyclic behaviour of the Arabidopsis thaliana photosynthesis-related gene CAB2 and the clock oscillator genes TOC1 and LHY in T cycles and N–H cycles.Key Results Changes in the rhythms of CAB2, TOC1 and LHY in plants subjected to non-24-h light:dark cycles matched the hypothesized changes in their behaviour as predicted by the solar clock model, thus validating it. The analysis further showed that TOC1 expression peaked ∼5·5 h after mid-day, CAB2 peaked close to noon, while LHY peaked ∼7·5 h after midnight, regardless of the cycle period, the photoperiod or the light:dark period ratio. The solar clock model correctly predicted the zeitgeber timing of these genes under 11 different lighting regimes comprising combinations of seven light periods, nine dark periods, four cycle periods and four light:dark period ratios. In short cycles that terminated before LHY could be expressed, the solar clock correctly predicted zeitgeber timing of its expression in the following cycle.Conclusions Regulation of gene phases by the solar clock enables the plant to tell the time, by which means a large number of genes are regulated. This facilitates the initiation of gene expression even before the arrival of sunrise, sunset or noon, thus allowing the plant to ‘anticipate’ dawn, dusk or mid-day respectively, independently of the photoperiod.     

Ecological implications of plants' ability to tell the time

The circadian clock (the endogenous mechanism that anticipates diurnal cycles) acts as a central coordinator of plant activity. At the molecular and organism level, it regulates key traits for plant fitness, including seed germination, gas exchange, growth and flowering, among others. In this article, we explore current evidence on the effect of the clock for the scales of interest to ecologists. We begin by synthesizing available knowledge on the effect of the clock on biosphere–atmosphere interactions and observe that, at least in the systems where it has been tested, the clock regulates gas exchange from the leaf to the ecosystem level, and we discuss its implications for estimates of the carbon balance. Then, we analyse whether incorporating the action of the clock may help in elucidating the effects of climate change on plant distributions. Circadian rhythms are involved in regulating the range of temperatures a species can survive and affects plant interactions. Finally, we review the involvement of the clock in key phenological events, such as flowering time and seed germination. Because the clock may act as a common mechanism affecting many of the diverse branches of ecology, our ultimate goal is to stimulate further research into this pressing, yet unexplored, topic.     

How plants see themselves--self-incompatibility in flowering plants

Plants have been propagating themselves by cloning for millennia. It is, however, widely recognised that mixing genes with other individuals of the same species makes better evolutionary sense, as it provides the variation that is the raw material for natural selection. How, then, do some plants prevent self-fertilisation?     

How plants sense temperature

Confronted to changes in temperatures, plants readjust their biochemical makeup to adapt and survive. The fact that temperature changes can induce cellular responses indicates that temperature is sensed and that the temperature signal is transduced into the cell. While the signalling pathways triggered temperature changes are well described, the way plants sense temperature is often considered as elusive. This review is focused on the mechanisms by which plants sense temperature. We show that plants have no internal thermometer as such, but that the very alterations in cellular equilibria triggered by temperature changes act as networked thermostats to sense heat and cold. Amongst these temperature-sensitive devices, we identified membrane fluidity, protein conformation, cytoskeleton depolymerization, and metabolic reactions. Besides, other molecular switches are proposed. A model of the temperature sensing “machinery” is proposed. Finally, we discuss the specificities of temperature sensing, showing that signalling events can feed-back perception steps.     

How plants grow up

A plant's lateral structures, such as leaves,branches and flowers, literally hinge on the shoot axis,making its integrity and growth fundamental to plant form.In all plants, subapical proliferation within the shoot tip displaces cells downward to extrude the cylindrical stem.Following the transition to flowering, many plants show extensive axial elongation associated with increased subapical proliferation and expansion. However, the cereal grasses also elongate their stems, called culms, due to activity within detached intercalary meristems which displaces cells upward, elevating the grain-bearing inflorescence. Variation in culm length within species is especially relevant to cereal crops, as demonstrated by the high-yielding semi-dwarfed cereals of the Green Revolution. Although previously understudied, recent renewed interest the regulation of subapical and intercalary growth suggests that control of cell division planes,boundary formation and temporal dynamics of differentiation, are likely critical mechanisms coordinating axial growth and development in plants.     

How plants make tubes

The plant body requires the transport of various materials over large distances. Two cell types that bear a striking resemblance morphologically are the cells specialized for water transport and those responsible for the transport of oxygen: xylem and lysigenous aerenchyma, respectively. Each of these cell types undergoes programmed cell death and cellular autolysis, resulting in the production of a functional space within the plant body. The major morphological difference observed is the presence of the lignified secondary wall in water-conducting tissues. The prevalence of tubular structures in other plant tissues suggests that the ability to form spaces through cellular autolysis is a fundamental paradigm in plant development and evolution.     

How plants split hairs

The unicellular three-branched trichomes, or 'hairs', of Arabidopsis provide a model system for studying cell morphogenesis in plants. Recent results, including the characterization of a newly identified mutant with multicellular trichomes, have led to a new view of how trichome morphogenesis might be controlled.     

How plants sense low oxygen

The recent identification of the oxygen-sensing mechanism in plants is a breakthrough in plant physiology. The presence of a conserved N-terminal motif on some ethylene responsive factors (ERFs), targets the protein for post-translational modifications finally leading to degradation under normoxia and thus providing a mechanism for sensing the presence of oxygen. The stabilization of the N-terminus under low oxygen activates these ERFs, which regulate low oxygen core genes that enable plants to tolerate abiotic stress such as flooding. Additional mechanisms that signal low-oxygen probably also exist, and the production of reactive oxygen species (ROS) has been observed under low oxygen, suggesting that ROS might be part of the network involved in plant acclimation. Here, we review the most recent findings related to oxygen sensing.     

How plants communicate using the underground information superhighway

The rhizosphere is a densely populated area in which plant roots must compete with invading root systems of neighboring plants for space, water, and mineral nutrients, and with other soil-borne organisms, including bacteria and fungi. Root-root and root-microbe communications are continuous occurrences in this biologically active soil zone. How do roots manage to simultaneously communicate with neighboring plants, and with symbiotic and pathogenic organisms within this crowded rhizosphere? Increasing evidence suggests that root exudates might initiate and manipulate biological and physical interactions between roots and soil organisms, and thus play an active role in root-root and root-microbe communication.     

How Sphagnum bogs down other plants

Recent research on the organo-chemical composition of Sphagnum and on the fate of its litter has further clarified how this plant builds acidic, nutrient-poor, cold and anoxic peat bogs. The bog environment helps Sphagnum to outcompete other plants for light. Its morphology, anatomy, physiology and composition make it an effective ecosystem engineer and at the same time benefit the plant in the short term. This may have facilitated the evolution of the genus.     

How plants cope with biotic interactions

In their natural environment, plants interact with many different organisms. The nature of these interactions may range from positive, for example interactions with pollinators, to negative, such as interactions with pathogens and herbivores. In this special issue, the contributors provide several examples of how plants manage both positive and negative biotic interactions. This review aims to relate their findings to what we know about the complex natural environments in which plants have evolved. Molecular analyses of plant genomes and expression profiles have shown how intricately plants may regulate responses to single or multiple biotic interactions. Plant responses are fine-tuned by signalling hormone interactions. When multiple organisms interact with a single plant this may result in antagonistic or synergistic effects. The emerging fields of ecogenomics and metabolomics undoubtedly will refine our understanding of the multilayered regulation that plants use to manage relationships with their biotic environment. However, we can only understand why plants have such an intricate regulatory apparatus if we consider the ecological context of plant biotic interactions.     

How plants cope with complete submergence

Flooding is a widespread phenomenon that drastically reduces the growth and survival of terrestrial plants. The dramatic decrease of gas diffusion in water compared with in air is a major problem for terrestrial plants and limits the entry of CO(2) for photosynthesis and of O(2) for respiration. Responses to avoid the adverse effects of submergence are the central theme in this review. These include underwater photosynthesis, aerenchyma formation and enhanced shoot elongation. Aerenchyma facilitates gas diffusion inside plants so that shoot-derived O(2) can diffuse to O(2)-deprived plant parts, such as the roots. The underwater gas-exchange capacity of leaves can be greatly enhanced by a thinner cuticle, reorientation of the chloroplasts towards the epidermis and increased specific leaf area (i.e. thinner leaves). At the same time, plants can outgrow the water through increased shoot elongation, which in some species is preceded by an adjustment of leaf angle to a more vertical position. The molecular regulatory networks involved in these responses, including the putative signals to sense submergence, are discussed and suggestions made on how to unravel the mechanistic basis of the induced expression of various adaptations that alleviate O(2) shortage underwater.