Auxin mediates the touch-induced mechanical stimulation of adventitious root formation under windy conditions in Brachypodium distachyon.

BACKGROUND: It is widely perceived that mechanical or thigmomorphogenic stimuli, such as rubbing and bending by passing animals, wind, raindrop, and flooding, broadly influence plant growth and developmental patterning. In particular, wind-driven mechanical stimulation is known to induce the incidence of radial expansion and shorter and stockier statue. Wind stimulation also affects the adaptive propagation of the root system in various plant species. However, it is unknown how plants sense and transmit the wind-derived mechanical signals to launch appropriate responses, leading to the wind-adaptive root growth. RESULTS: Here, we found that Brachypodium distachyon, a model grass widely used for studies on bioenergy crops and cereals, efficiently adapts to wind-mediated lodging stress by forming adventitious roots (ARs) from nonroot tissues. Experimental dissection of wind stimuli revealed that not bending of the mesocotyls but physical contact of the leaf nodes with soil particles triggers the transcriptional induction of a group of potential auxin-responsive genes encoding WUSCHEL RELATED HOMEOBOX and LATERAL ORGAN BOUNDARIES DOMAIN transcription factors, which are likely to be involved in the induction of AR formation. CONCLUSIONS: Our findings would contribute to further understanding molecular mechanisms governing the initiation and development of ARs, which will be applicable to crop agriculture in extreme wind climates.

Developmental Programming of Thermonastic Leaf Movement.

Plants exhibit diverse polar behaviors in response to directional and nondirectional environmental signals, termed tropic and nastic movements, respectively. The ways in which plants incorporate directional information into tropic behaviors is well understood, but it is less well understood how nondirectional stimuli, such as ambient temperatures, specify the polarity of nastic behaviors. Here, we demonstrate that a developmentally programmed polarity of auxin flow underlies thermo-induced leaf hyponasty in Arabidopsis (Arabidopsis thaliana). In warm environments, PHYTOCHROME-INTERACTING FACTOR4 (PIF4) stimulates auxin production in the leaf. This results in the accumulation of auxin in leaf petioles, where PIF4 directly activates a gene encoding the PINOID (PID) protein kinase. PID is involved in polarization of the auxin transporter PIN-FORMED3 to the outer membranes of petiole cells. Notably, the leaf polarity-determining ASYMMETRIC LEAVES1 (AS1) directs the induction of PID to occur predominantly in the abaxial petiole region. These observations indicate that the integration of PIF4-mediated auxin biosynthesis and polar transport, and the AS1-mediated developmental shaping of polar auxin flow, coordinate leaf thermonasty, which facilitates leaf cooling in warm environments. We believe that leaf thermonasty is a suitable model system for studying the developmental programming of environmental adaptation in plants.

ZEITLUPE Contributes to a Thermoresponsive Protein Quality Control System in Arabidopsis.

Cellular proteins undergo denaturation and oxidative damage under heat stress, forming insoluble aggregates that are toxic to cells. Plants possess versatile mechanisms to deal with insoluble protein aggregates. Denatured proteins are either renatured to their native conformations or removed from cellular compartments; these processes are often referred to as protein quality control. Heat shock proteins (HSPs) act as molecular chaperones that assist in the renaturation-degradation process. However, how protein aggregates are cleared from cells in plants is largely unknown. Here, we demonstrate that heat-induced protein aggregates are removed by a protein quality control system that includes the ZEITLUPE (ZTL) E3 ubiquitin ligase, a central circadian clock component in Arabidopsis thaliana ZTL mediates the polyubiquitination of aggregated proteins, which leads to proteasomal degradation and enhances the thermotolerance of plants growing at high temperatures. The ZTL-defective ztl-105 mutant exhibited reduced thermotolerance, which was accompanied by a decline in polyubiquitination but an increase in protein aggregate formation. ZTL and its interacting partner HSP90 were cofractionated with insoluble aggregates under heat stress, indicating that ZTL contributes to the thermoresponsive protein quality control machinery. Notably, the circadian clock was hypersensitive to heat in ztl-105 We propose that ZTL-mediated protein quality control contributes to the thermal stability of the circadian clock.

Thermal adaptation and plasticity of the plant circadian clock.

Contents Summary 1215 I. Introduction 1215 II. Molecular organization of the plant circadian clock 1216 III. Temperature compensation 1219 IV. Temperature regulation of circadian behaviors 1220 V. Thermal adaptation of the clock: evolutionary considerations 1223 VI. Light and temperature information for the clock function - synergic or individual? 1224 VII. Concluding remarks and future prospects 1225 Acknowledgements 1225 References 1225 SUMMARY: Plant growth and development is widely affected by diverse temperature conditions. Although studies have been focused mainly on the effects of stressful temperature extremes in recent decades, nonstressful ambient temperatures also influence an array of plant growth and morphogenic aspects, a process termed thermomorphogenesis. Notably, accumulating evidence indicates that both stressful and nonstressful temperatures modulate the functional process of the circadian clock, a molecular timer of biological rhythms in higher eukaryotes and photosynthetic prokaryotes. The circadian clock can sustain robust and precise timing over a range of physiological temperatures. Genes and molecular mechanisms governing the temperature compensation process have been explored in different plant species. In addition, a ZEITLUPE/HSP90-mediated protein quality control mechanism helps plants maintain the thermal stability of the clock under heat stress. The thermal adaptation capability and plasticity of the clock are of particular interest in view of the growing concern about global climate changes. Considering these circumstances in the field, we believe that it is timely to provide a provoking discussion on the current knowledge of temperature regulation of the clock function. The review also will discuss stimulating ideas on this topic along with ecosystem management and future agricultural innovation.

Alternative splicing provides a proactive mechanism for the diurnal CONSTANS dynamics in Arabidopsis photoperiodic flowering.

The circadian clock control of CONSTANS (CO) transcription and the light-mediated stabilization of its encoded protein coordinately adjust photoperiodic flowering by triggering rhythmic expression of the floral integrator flowering locus T (FT). Diurnal accumulation of CO is modulated sequentially by distinct E3 ubiquitin ligases, allowing peak CO to occur in the late afternoon under long days. Here we show that CO abundance is not simply targeted by E3 enzymes but is also actively self-adjusted through dynamic interactions between two CO isoforms. Alternative splicing of CO produces two protein variants, the full-size COα and the truncated COß lacking DNA-binding affinity. Notably, COß, which is resistant to E3 enzymes, induces the interaction of COα with CO-destabilizing E3 enzymes but inhibits the association of COα with CO-stabilizing E3 ligase. These observations demonstrate that CO plays an active role in sustaining its diurnal accumulation dynamics during Arabidopsis photoperiodic flowering.

LATE ELONGATED HYPOCOTYL regulates photoperiodic flowering via the circadian clock in Arabidopsis.

BACKGROUND: Plants constantly monitor changes in photoperiod or day length to trigger the flowering cycle at the most appropriate time of the year. It is well established that photoperiodic flowering is intimately associated with the circadian clock in Arabidopsis. In support of this notion, many clock-defective mutants exhibit altered photoperiodic sensitivity in inducing flowering. LATE ELONGATED HYPOCOTYL (LHY) and its functional paralogue CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) constitute the core of the circadian clock together with TIMING OF CAB EXPRSSION 1 (TOC1). While it is known that TOC1 contributes to the timing of flowering entirely by modulating the clock function, molecular mechanisms by which LHY and CCA1 regulate flowering time have not been explored. RESULTS: We investigated how LHY and CCA1 regulate photoperiodic flowering through molecular genetic and biochemical studies. It was found that LHY-defective mutants (lhy-7 and lhy-20) exhibit accelerated flowering under both long days (LDs) and short days (SDs). Consistent with the accelerated flowering phenotypes, gene expression analysis revealed that expression of the floral integrator FLOWERING LOCUS T (FT) is up-regulated in the lhy mutants. In addition, the expression peaks of GIGANTEA (GI) and FLAVIN-BINDING, KELCH REPEAT, F-BOX PROTEIN 1 (FKF1) genes, which constitute the clock output pathway that is linked with photoperiodic flowering, were advanced by approximately 4 h in the mutants. Furthermore, the up-regulation of FT disappeared when the endogenous circadian period is matched to the external light/dark cycles in the lhy-7 mutant. Notably, whereas CCA1 binds strongly to FT gene promoter, LHY does not show such DNA-binding activity. CONCLUSIONS: Our data indicate that the advanced expression phases of photoperiodic flowering genes are associated with the clock defects in the lhy mutants and responsible for the reduced photoperiodic sensitivity of the mutant flowering, demonstrating that LHY regulates photoperiodic flowering via the circadian clock, similar to what has been shown with TOC1. It is notable that while LHY regulates photoperiodic flowering in a similar manner as with TOC1, the underlying molecular mechanism would be somewhat distinct from that exerted by CCA1 in Arabidopsis.

Protein quality control is essential for the circadian clock in plants.

Extreme environmental conditions, such as heat and cold, often disturb cellular proteostasis, resulting in protein denaturation and oxidative damage that threaten cell viability. Therefore, living organisms have evolved versatile protein quality control mechanisms that clear damaged proteins from cellular compartments. It has been shown that a repertoire of molecular chaperones, including heat shock proteins (HSPs), works together with ubiquitin-proteasome systems in this biochemical process in animals and yeast. However, the protein quality control systems have not been well-characterized in plants. We have recently reported that the E3 ubiquitin ligase ZEITLUPE (ZTL), a central component of the plant circadian clock, constitutes a protein quality control system in conjunction with HSP90, which is responsible for clearing denatured protein aggregates at high temperatures. The ZTL-HSP90 protein complexes are colocalized in insoluble fractions in heat-exposed plants. Notably, lack of ZTL reduces protein polyubiquitination and disrupts the robustness of circadian rhythms under heat stress conditions, providing a novel role of ZTL: it mediates a heat-responsive protein quality control to sustain the clock function. We summarize the potential roles of ZTL in thermal responses and stability of the circadian clock in plants.