Canopy Light Quality Modulates Stress Responses in Plants

When subject to vegetational shading, shade-avoiding plants detect neighbors by perceiving reduced light quantity and altered light quality. The former includes decreases in the ratio of red to far-red wavelengths (low R:FR) and low blue light ratio (LBL) predominantly detected by phytochromes and cryptochromes, respectively. By integrating multiple signals, plants generate a suite of responses, such as elongation of a variety of organs, accelerated flowering, and reduced branching, which are collectively termed the shade-avoidance syndrome (SAS). To trigger the SAS, interactions between photoreceptors and phytochrome-interacting factors are the general switch for activation of downstream signaling pathways. A number of transcription factor families and phytohormones, especially auxin, gibberellins, ethylene, and brassinosteroids, are involved in the SAS processes. In this review, shade signals, the major photoreceptors involved, and the phenotypic characteristics of the shade-intolerant plant Arabidopsis thaliana are described in detail. In addition, integration of the signaling mechanisms that link photoreceptors with multiple hormone signaling pathways is presented and future research directions are discussed.

/pdf/progress-of-research-on-the-regulatory-pathway-of-the-plant-4tt1jlz7uj.pdf

Progress of Research on the Regulatory Pathway of the Plant Shade-Avoidance Syndrome.

Abstract We present unresolved questions in plant abiotic stress biology as posed by 15 research groups with expertise spanning eco-physiology to cell and molecular biology. Common themes of these questions include the need to better understand how plants detect water availability, temperature, salinity, and rising carbon dioxide (CO2) levels; how environmental signals interface with endogenous signaling and development (e.g. circadian clock and flowering time); and how this integrated signaling controls downstream responses (e.g. stomatal regulation, proline metabolism, and growth versus defense balance). The plasma membrane comes up frequently as a site of key signaling and transport events (e.g. mechanosensing and lipid-derived signaling, aquaporins). Adaptation to water extremes and rising CO2 affects hydraulic architecture and transpiration, as well as root and shoot growth and morphology, in ways not fully understood. Environmental adaptation involves tradeoffs that limit ecological distribution and crop resilience in the face of changing and increasingly unpredictable environments. Exploration of plant diversity within and among species can help us know which of these tradeoffs represent fundamental limits and which ones can be circumvented by bringing new trait combinations together. Better defining what constitutes beneficial stress resistance in different contexts and making connections between genes and phenotypes, and between laboratory and field observations, are overarching challenges.

/pdf/burning-questions-for-a-warming-and-changing-world-15-2zs86jj5.pdf

Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress

Despite the identification of temperature sensors and downstream components involved in promoting stem growth by warm temperatures, when and how previous temperatures affect current plant growth remain unclear. Here we show that hypocotyl growth in Arabidopsis thaliana during the night responds not only to the current temperature but also to preceding daytime temperatures, revealing a short-term memory of previous conditions. Daytime temperature affected the levels of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and LONG HYPOCOTYL 5 (HY5) in the nucleus during the next night. These factors jointly accounted for the observed growth kinetics, whereas nighttime memory of prior daytime temperature was impaired in pif4 and hy5 mutants. PIF4 promoter activity largely accounted for the temperature-dependent changes in PIF4 protein levels. Notably, the decrease in PIF4 promoter activity triggered by cooling required a stronger temperature shift than the increase caused by warming, representing a typical hysteretic effect; this hysteretic pattern required EARLY-FLOWERING 3 (ELF3). Warm temperatures promoted the formation of nuclear condensates of ELF3 in hypocotyl cells during the afternoon but not in the morning. These nuclear speckles showed poor sensitivity to subsequent cooling. We conclude that ELF3 achieves hysteresis and drives the PIF4 promoter into the same behavior, enabling a short-term memory of daytime temperature conditions.

/pdf/hysteresis-in-phytochrome-interacting-factor-4-and-early-24egl698.pdf

Hysteresis in PHYTOCHROME INTERACTING FACTOR 4 and EARLY-FLOWERING 3 dynamics dominates warm daytime memory in Arabidopsis.

Abstract The size of plant organs is highly responsive to environmental conditions. The plant’s embryonic stem, or hypocotyl, displays phenotypic plasticity, in response to light and temperature. The hypocotyl of shade avoiding species elongates to outcompete neighboring plants and secure access to sunlight. Similar elongation occurs in high temperature. However, it is poorly understood how environmental light and temperature cues interact to effect plant growth. We found that shade combined with warm temperature produces a synergistic hypocotyl growth response that dependent on PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) and auxin. This unique but agriculturally relevant scenario was almost totally independent on PIF4 activity. We show that warm temperature is sufficient to promote PIF7 DNA binding but not transcriptional activation and we demonstrate that additional, unknown factor/s must be working downstream of the phyB-PIF-auxin module. Our findings will improve the predictions of how plants will respond to increased ambient temperatures when grown at high density. 

/pdf/pif7-is-a-master-regulator-of-thermomorphogenesis-in-shade-3968jw8o.pdf

PIF7 is a master regulator of thermomorphogenesis in shade

When exposed to neighbour cues, competitive plants increase stem growth to reduce the degree of current or future shade. The aim of this work is to investigate the impact of weather conditions on the magnitude of shade avoidance responses in Arabidopsis thaliana. We first generated a growth rate database under controlled conditions and elaborated a model that predicts daytime hypocotyl growth as a function of the activity of the main photosensory receptors (phytochromes A and B, cryptochromes 1 and 2) in combination with light and temperature inputs. We then incorporated the action of thermal amplitude to account for its effect on selected genotypes, which correlates with the dynamics of the growth-promoting transcription factor PHYTOCHROME-INTERACTING FACTOR 4. The model predicted growth rate in the field with reasonable accuracy. Thus, we used the model in combination with a worldwide data set of current and future whether conditions. The analysis predicted enhanced shade avoidance responses as a result of higher temperatures due to the geographical location or global warming. Irradiance and thermal amplitude had no effects. These trends were also observed for our local growth rate measurements. We conclude that, if water and nutrients do not become limiting, warm environments enhance the shade avoidance response.

Shade avoidance responses become more aggressive in warm environments.

Shade and warmth promote the growth of the stem, but the degree of mechanistic convergence and functional association between these responses is not clear. We analysed the quantitative impact of mutations and natural genetic variation on the hypocotyl growth responses of Arabidopsis thaliana to shade and warmth, the relationship between the abundance of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and growth stimulation by shade or warmth, the effects of both cues on the transcriptome and the consequences of warm temperature on carbon balance. Growth responses to shade and warmth showed strong genetic linkage and similar dependence on PIF4 levels. Temperature increased growth and phototropism even within a range where damage by extreme high temperatures is unlikely to occur in nature. Both cues enhanced the expression of growth-related genes and reduced the expression of photosynthetic genes. However, only warmth enhanced the expression of genes involved in responses to heat. Warm temperatures substantially increased the amount of light required to compensate for the daily carbon dioxide balance. We propose that the main ecological function of hypocotyl growth responses to warmth is to increase the access of shaded photosynthetic organs to light, which implies functional convergence with shade avoidance.

/pdf/functional-convergence-of-growth-responses-to-shade-and-1f5utv4x7t.pdf

Functional convergence of growth responses to shade and warmth in Arabidopsis.

When exposed to neighbour signals, competitive plants increase the growth of the stem to reduce the degree of current or future shade. Plants can experience similar neighbour cues under different weather conditions and the aim of this work is to investigate the impact of daily average temperature and irradiance and thermal amplitude on the magnitude of shade-avoidance responses in Arabidopsis thaliana. For this purpose, we first generated a growth database and elaborated under controlled conditions a model that predicts hypocotyl growth during the photoperiod as a function of the light-modulated activity of the main photo-sensory receptors (phytochromes A and B, cryptochromes 1 and 2), temperature-modulated activity of phytochrome B and an independent temperature input. Thermal amplitude (lower temperatures during the morning and afternoon that at midday) reduced growth of genotypes with normally fast morning growth, and this effect was incorporated to the model. Thermal amplitude also decreased the abundance of the growth-promoting transcription factor PHYTOCHROME-INTERACTING FACTOR 4. The model predicted growth in the field through different seasons with reasonable accuracy. Then, we used the model in combination with a worldwide dataset of current and future whether conditions. The analysis predicted enhanced shade-avoidance responses as a result of higher temperatures due to the geographical location or global warming. Irradiance and thermal amplitude had no effects. These trends were also observed for our local growth measurements. We conclude that, if water and nutrients do not become limiting, warm environments enhance the shade avoidance response.

/pdf/shade-avoidance-responses-become-more-aggressive-in-warm-2dh556ztxk.pdf

Sofía Romero-Montepaone

Papers

Shade avoidance responses become more aggressive in warm environments.

Functional convergence of growth responses to shade and warmth in Arabidopsis.

Shade-avoidance responses become more aggressive in warm environments