Natural variation in salt-induced root growth phases and their contribution to root architecture plasticity.

The root system architecture of a plant changes during salt stress exposure. Different accessions of Arabidopsis thaliana have adopted different strategies in remodelling their root architecture during salt stress. Salt induces a multiphase growth response in roots, consisting of a stop phase, quiescent phase, recovery phase and eventually a new level of homoeostasis. We explored natural variation in the length of and growth rate during these phases in both main and lateral roots and find that some accessions lack the quiescent phase. Using mathematical models and correlation-based network, allowed us to correlate dynamic traits to overall root architecture and discover that both the main root growth rate during homoeostasis and lateral root appearance are the strongest determinants of overall root architecture. In addition, this approach revealed a trade-off between investing in main or lateral root length during salt stress. By studying natural variation in high-resolution temporal root growth using mathematical modelling, we gained new insights in the interactions between dynamic root growth traits and we identified key traits that modulate overall root architecture during salt stress.

Metal halide perovskite toxicity effects on Arabidopsis thaliana plants are caused by iodide ions.

Highly efficient solar cells containing lead halide perovskites are expected to revolutionize sustainable energy production in the coming years. Perovskites are generally assumed to be toxic because of the lead (Pb), but experimental evidence to support this prediction is scarce. We tested the toxicity of the perovskite MAPbI3 (MA = CH3NH3) and several precursors in Arabidopsis thaliana plants. Both MAPbI3 and the precursor MAI hamper plant growth at concentrations above 5 µM. Lead-based precursors without iodide are only toxic above 500 µM. Iodine accumulation in Arabidopsis correlates with growth inhibition at much lower concentrations than lead. This reveals that perovskite toxicity at low concentrations is caused by iodide ions specifically, instead of lead. We calculate that toxicity thresholds for iodide, but not lead, are likely to be reached in soils upon perovskite leakage. This work stresses the importance to further understand and predict harmful effects of iodide-containing perovskites in the environment.

GENOMES UNCOUPLED1-independent retrograde signaling targets the ethylene pathway to repress photomorphogenesis.

When germinating in the light, Arabidopsis (Arabidopsis thaliana) seedlings undergo photomorphogenic development, characterized by short hypocotyls, greening, and expanded cotyledons. Stressed chloroplasts emit retrograde signals to the nucleus that induce developmental responses and repress photomorphogenesis. The nuclear targets of these retrograde signals are not yet fully known. Here, we show that lincomycin-treated seedlings (which lack developed chloroplasts) show strong phenotypic similarities to seedlings treated with ethylene (ET) precursor 1-aminocyclopropane-1-carboxylic acid, as both signals inhibit cotyledon separation in the light. We show that the lincomycin-induced phenotype partly requires a functioning ET signaling pathway, but could not detect increased ET emissions in response to the lincomycin treatment. The two treatments show overlap in upregulated gene transcripts, downstream of transcription factors ETHYLENE INSENSITIVE3 and EIN3-LIKE1. The induction of the ET signaling pathway is triggered by an unknown retrograde signal acting independently of GENOMES UNCOUPLED1. Our data show how two apparently different stress responses converge to optimize photomorphogenesis.

Circadian Waves of Transcriptional Repression Shape PIF-Regulated Photoperiod-Responsive Growth in Arabidopsis.

Plants coordinate their growth and development with the environment through integration of circadian clock and photosensory pathways. In Arabidopsis thaliana, rhythmic hypocotyl elongation in short days (SD) is enhanced at dawn by the basic-helix-loop-helix (bHLH) transcription factors PHYTOCHROME-INTERACTING FACTORS (PIFs) directly inducing expression of growth-related genes [1-6]. PIFs accumulate progressively during the night and are targeted for degradation by active phytochromes in the light, when growth is reduced. Although PIF proteins are also detected during the day hours [7-10], their growth-promoting activity is inhibited through unknown mechanisms. Recently, the core clock components and transcriptional repressors PSEUDO-RESPONSE REGULATORS PRR9/7/5 [11, 12], negative regulators of hypocotyl elongation [13, 14], were described to associate to G boxes [15], the DNA motifs recognized by the PIFs [16, 17], suggesting that PRR and PIF function might converge antagonistically to regulate growth. Here we report that PRR9/7/5 and PIFs physically interact and bind to the same promoter region of pre-dawn-phased, growth-related genes, and we identify the transcription factor CDF5 [18, 19] as target of this interplay. In SD, CDF5 expression is sequentially repressed from morning to dusk by PRRs and induced pre-dawn by PIFs. Consequently, CDF5 accumulates specifically at dawn, when it induces cell elongation. Our findings provide a framework for recent TIMING OF CAB EXPRESSION 1 (TOC1/PRR1) data [5, 20] and reveal that the long described circadian morning-to-midnight waves of the PRR transcriptional repressors (PRR9, PRR7, PRR5, and TOC1) [21] jointly gate PIF activity to dawn to prevent overgrowth through sequential regulation of common PIF-PRR target genes such as CDF5.

Organ-specific phytohormone synthesis in two Geranium species with antithetical responses to far-red light enrichment.

Plants growing in high densities experience a reduced red (R) to far-red (FR) light ratio and shade-intolerant species respond with accelerated elongation growth to reach the top of the canopy: the shade avoidance syndrome (SAS). FR-enriched light inactivates phytochrome photoreceptors, which results in subsequent action of several plant hormones regulating growth. SAS is adaptive for shade-intolerant plants, but is suppressed in shade-tolerant plant species. Inspired by a previously published transcriptome analysis, we use two species of the genus Geranium here to study the involvement of auxin, brassinosteroids (BRs), and gibberellins (GAs) in supplemental FR-induced elongation growth. G. pyrenaicum, a shade-avoiding species, strongly induces auxin and gibberellin levels, but not BR, in elongating petioles. We show that, in this species, FR light perception, hormone synthesis, and growth are local and restricted to the petiole, and not the leaf lamina. Using chemical hormone inhibitors, we confirm the essential role of auxin and GAs in supplemental FR-induced elongation growth. Shade-tolerant G. robertianum does not display the change in hormone levels upon FR light enrichment, resulting in the lack of a shade avoidance response.

Molecular Profiles of Contrasting Shade Response Strategies in Wild Plants: Differential Control of Immunity and Shoot Elongation.

Plants growing at high densities elongate their shoots to reach for light, a response known as the shade avoidance syndrome (SAS). Phytochrome-mediated detection of far-red light reflection from neighboring plants activates growth-promoting molecular pathways leading to SAS However, it is unknown how plants that complete their life cycle in the forest understory and are shade tolerant prevent SAS when exposed to shade. Here, we show how two wild Geranium species from different native light environments regulate contrasting responses to light quality cues. A comparative RNA sequencing approach unveiled the molecular underpinnings of their contrasting growth responses to far-red light enrichment. It also identified differential phytochrome control of plant immunity genes and confirmed that far-red enrichment indeed contrastingly affects resistance against Botrytis cinerea between the two species. Furthermore, we identify a number of candidate regulators of differential shade avoidance. Three of these, the receptor-like kinases FERONIA and THESEUS1 and the non-DNA binding bHLH protein KIDARI, are functionally validated in Arabidopsis thaliana through gene knockout and/or overexpression studies. We propose that these components may be associated with either showing or not showing shade avoidance responses.

Integration of Phytochrome and Cryptochrome Signals Determines Plant Growth during Competition for Light.

Plants in dense vegetation perceive their neighbors primarily through changes in light quality. Initially, the ratio between red (R) and far-red (FR) light decreases due to reflection of FR by plant tissue well before shading occurs. Perception of low R:FR by the phytochrome photoreceptors induces the shade avoidance response [1], of which accelerated elongation growth of leaf-bearing organs is an important feature. Low R:FR-induced phytochrome inactivation leads to the accumulation and activation of the transcription factors PHYTOCHROME-INTERACTING FACTORs (PIFs) 4, 5, and 7 and subsequent expression of their growth-mediating targets [2, 3]. When true shading occurs, transmitted light is especially depleted in red and blue (B) wavelengths, due to absorption by chlorophyll [4]. Although the reduction of blue wavelengths alone does not occur in nature, long-term exposure to low B light induces a shade avoidance-like response that is dependent on the cryptochrome photoreceptors and the transcription factors PIF4 and PIF5 [5-7]. We show in Arabidopsis thaliana that low B in combination with low R:FR enhances petiole elongation similar to vegetation shade, providing functional context for a low B response in plant competition. Low B potentiates the low R:FR response through PIF4, PIF5, and PIF7, and it involves increased PIF5 abundance and transcriptional changes. Low B attenuates a low R:FR-induced negative feedback loop through reduced gene expression of negative regulators and reduced HFR1 levels. The enhanced response to combined phytochrome and cryptochrome inactivation shows how multiple light cues can be integrated to fine-tune the plant's response to a changing environment.

Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis.

In dense stands of plants, such as agricultural monocultures, plants are exposed simultaneously to competition for light and other stresses such as pathogen infection. Here, we show that both salicylic acid (SA)-dependent and jasmonic acid (JA)-dependent disease resistance is inhibited by a simultaneously reduced red:far-red light ratio (R:FR), the early warning signal for plant competition. Conversely, SA- and JA-dependent induced defences did not affect shade-avoidance responses to low R:FR. Reduced pathogen resistance by low R:FR was accompanied by a strong reduction in the regulation of JA- and SA-responsive genes. The severe inhibition of SA-responsive transcription in low R:FR appeared to be brought about by the repression of SA-inducible kinases. Phosphorylation of the SA-responsive transcription co-activator NPR1, which is required for full induction of SA-responsive transcription, was indeed reduced and may thus play a role in the suppression of SA-mediated defences by low R:FR-mediated phytochrome inactivation. Our results indicate that foraging for light through the shade-avoidance response is prioritised over plant immune responses when plants are simultaneously challenged with competition and pathogen attack.

Shade tolerance: when growing tall is not an option.

Two different plant strategies exist to deal with shade: shade avoidance and shade tolerance. All shade-exposed plants optimize photosynthesis to adapt to the decrease in light quality and quantity. When shaded, most species in open habitats express the shade-avoidance syndrome, a growth response to escape shade. Shade-tolerant species from forest understories cannot outgrow surrounding trees and adopt a tolerance response. Unlike shade avoidance, virtually nothing is known about regulation of shade tolerance. In this opinion article, we discuss potential modes of molecular regulation to adopt a shade-tolerance rather than a shade-avoidance strategy. We argue that molecular approaches using model and non-model species should help identify the molecular pathways that underpin shade tolerance, thus providing knowledge for further crop improvement.