PIF4 enhances the expression of SAUR genes to promote growth in response to nitrate.

Nitrate supply is fundamental to support shoot growth and crop performance, but the associated increase in stem height exacerbates the risks of lodging and yield losses. Despite their significance for agriculture, the mechanisms involved in the promotion of stem growth by nitrate remain poorly understood. Here, we show that the elongation of the hypocotyl of Arabidopsis thaliana, used as a model, responds rapidly and persistently to upshifts in nitrate concentration, rather than to the nitrate level itself. The response occurred even in shoots dissected from their roots and required NITRATE TRANSPORTER 1.1 (NRT1.1) in the phosphorylated state (but not NRT1.1 nitrate transport capacity) and NIN-LIKE PROTEIN 7 (NLP7). Nitrate increased PHYTOCHROME INTERACTING FACTOR 4 (PIF4) nuclear abundance by posttranscriptional mechanisms that depended on NRT1.1 and phytochrome B. In response to nitrate, PIF4 enhanced the expression of numerous SMALL AUXIN-UP RNA (SAUR) genes in the hypocotyl. The growth response to nitrate required PIF4, positive and negative regulators of its activity, including AUXIN RESPONSE FACTORs, and SAURs. PIF4 integrates cues from the soil (nitrate) and aerial (shade) environments adjusting plant stature to facilitate access to light.

EARLY FLOWERING 3 represses the nighttime growth response to sucrose in Arabidopsis.

Plant growth depends on the supply of carbohydrates produced by photosynthesis. Exogenously applied sucrose promotes the growth of the hypocotyl in Arabidopsis thaliana seedlings grown under short days. Whether this effect of sucrose is stronger under the environmental conditions where the light input for photosynthesis is limiting remains unknown. We characterised the effects of exogenous sucrose on hypocotyl growth rates under light compared to simulated shade, during different portions of the daily cycle. The strongest effects of exogenous sucrose occurred under shade and during the night; i.e., the conditions where there is reduced or no photosynthesis. Conversely, a faster hypocotyl growth rate, predicted to enhance the demand of carbohydrates, did not associate to a stronger sucrose effect. The early flowering 3 (elf3) mutation strongly enhanced the impact of sucrose on hypocotyl growth during the night of a white-light day. This effect occurred under short, but not under long days. The addition of sucrose enhanced the fluorescence intensity of ELF3 nuclear speckles. The elf3 mutant showed increased abundance of PHYTOCHROME INTERACTING FACTOR4 (PIF4), which is a transcription factor required for a full response to sucrose. Sucrose increased PIF4 protein abundance by post-transcriptional mechanisms. Under shade, elf3 showed enhanced daytime and reduced nighttime effects of sucrose. We conclude that ELF3 modifies the responsivity to sucrose according to the time of the daily cycle and the prevailing light or shade conditions.

Phytochrome B links the environment to transcription.

Phytochrome B (phyB) senses the difference between darkness and light, the level of irradiance, the red/far-red ratio, and temperature. Thanks to these sensory capacities, phyB perceives whether plant organs are buried in the soil, exposed to full sunlight, in the presence of nearby vegetation, and/or under risk of heat stress. In some species, phyB perceives seasonal daylength cues. phyB affects the activity of several transcriptional regulators either by direct physical interaction or indirectly by physical interaction with proteins involved in the turnover of transcriptional regulators. Typically, interaction of a protein with phyB has either negative or positive effects on the interaction of the latter with a third party, this being another protein or DNA. Thus, phyB mediates the context-dependent modulation of the transcriptome underlying changes in plant morphology, physiology, and susceptibility to biotic and abiotic stress. phyB operates as a dynamic switch that improves carbon balance, prioritizing light interception and photosynthetic capacity in open places and the projection of the shoot towards light in the soil, under shade and in warm conditions.

Neighbour signals perceived by phytochrome B increase thermotolerance in Arabidopsis.

Due to the preeminence of reductionist approaches, understanding of plant responses to combined stresses is limited. We speculated that light-quality signals of neighbouring vegetation might increase susceptibility to heat shocks because shade reduces tissue temperature and hence the likeness of heat shocks. In contrast, plants of Arabidopsis thaliana grown under low-red/far-red ratios typical of shade were less damaged by heat stress than plants grown under simulated sunlight. Neighbour signals reduce the activity of phytochrome B (phyB), increasing the abundance of PHYTOCHROME-INTERACTING FACTORS (PIFs). The phyB mutant showed high tolerance to heat stress even under simulated sunlight, and a pif multiple mutant showed low tolerance under simulated shade. phyB and red/far-red ratio had no effects on seedlings acclimated with nonstressful warm temperatures before the heat shock. The phyB mutant showed reduced expression of several fatty acid desaturase (FAD) genes and less proportion of fully unsaturated fatty acids and electrolyte leakage of membranes exposed to heat shocks. Red-light-activated phyB also reduced thermotolerance of dark-grown seedlings but not via changes in FADs expression and membrane stability. We propose that the reduced photosynthetic capacity linked to thermotolerant membranes would be less costly under shade, where the light input limits photosynthesis.

Phytochrome B enhances plant growth, biomass and grain yield in field-grown maize.

BACKGROUND AND AIMS: Phytochrome B (phyB) is a photosensory receptor important for the control of plant plasticity and resource partitioning. Whether phyB is required to optimize plant biomass accumulation in agricultural crops exposed to full sunlight is unknown. Here we investigated the impact of mutations in the genes that encode either phyB1 or phyB2 on plant growth and grain yield in field crops of Zea mays sown at contrasting population densities. METHODS: Plants of maize inbred line France 2 wild type (WT) and the isogenic mutants lacking either phyB1 or phyB2 (phyB1 and phyB2) were cultivated in the field during two seasons. Plants were grown at two densities (9 and 30 plants m-2), irrigated and without restrictions of nutrients. Leaf and stem growth, leaf anatomy, light interception, above-ground biomass accumulation and grain yield were recorded. KEY RESULTS: At high plant density, all the lines showed similar kinetics of biomass accumulation. However, compared with the WT, the phyB1 and phyB2 mutations impaired the ability to enhance plant growth in response to the additional resources available at low plant density. This effect was largely due to a reduced leaf area (fewer cells per leaf), which compromised light interception capacity. Grain yield was reduced in phyB1 plants. CONCLUSIONS: Maize plants grown in the field at relatively low densities require phyB1 and phyB2 to sense the light environment and optimize the use of the available resources. In the absence of either of these two light receptors, leaf expansion is compromised, imposing a limitation to the interception of photosynthetic radiation and growth. These observations suggest that genetic variability at the locus encoding phyB could offer a breeding target to improve crop growth capacity in the field.

Reduced expression of selected FASCICLIN-LIKE ARABINOGALACTAN PROTEIN genes associates with the abortion of kernels in field crops of Zea mays (maize) and of Arabidopsis seeds.

Abortion of fertilized ovaries at the tip of the ear can generate significant yield losses in maize crops. To investigate the mechanisms involved in this process, 2 maize hybrids were grown in field crops at 2 sowing densities and under 3 irrigation regimes (well-watered control, drought before pollination, and drought during pollination), in all possible combinations. Samples of ear tips were taken 2-6 days after synchronous hand pollination and used for the analysis of gene expression and sugars. Glucose and fructose levels increased in kernels with high abortion risk. Several FASCICLIN-LIKE ARABINOGALACTAN PROTEIN (FLA) genes showed negative correlation with abortion. The expression of ZmFLA7 responded to drought only at the tip of the ear. The abundance of arabinogalactan protein (AGP) glycan epitopes decreased with drought and pharmacological treatments that reduce AGP activity enhanced the abortion of fertilized ovaries. Drought also reduced the expression of AthFLA9 in the siliques of Arabidopsis thaliana. Gain- and loss-of-function mutants of Arabidopsis showed a negative correlation between AthFLA9 and seed abortion. On the basis of gene expression patterns, pharmacological, and genetic evidence, we propose that stress-induced reductions in the expression of selected FLA genes enhance abortion of fertilized ovaries in maize and Arabidopsis.

Multiple links between shade avoidance and auxin networks.

Auxin has emerged as a key player in the adjustment of plant morphology to the challenge imposed by variable environmental conditions. Shade-avoidance responses, including the promotion of stem and petiole growth, leaf hyponasty, and the inhibition of branching, involve an intimate connection between light and auxin signalling. Low activity of photo-sensory receptors caused by the presence of neighbouring vegetation enhances the activity of PHYTOCHROME INTERACTING FACTORs (PIFs), which directly promote the expression of genes involved in auxin biosynthesis, conjugation, transport, perception, and signalling. In seedlings, neighbour signals increase auxin levels in the foliage, which then moves to the stem, where it reaches epidermal tissues to promote growth. However, this model only partially accounts for shade-avoidance responses (which may also occur in the absence of increased auxin levels), and understanding the whole picture will require further insight into the functional significance of the multiple links between shade and auxin networks.

Phytochrome B Nuclear Bodies Respond to the Low Red to Far-Red Ratio and to the Reduced Irradiance of Canopy Shade in Arabidopsis.

The current consensus is that plant responses to canopy shade involve the perception of low red to far-red ratios (R:FRs) by phytochrome B (phyB), which leads to the direct activation of auxin synthesis genes by PHYTOCHROME INTERACTING FACTORs (PIFs). In addition to its effect on R:FRs, shade also reduces irradiance, but whether shade-induced drops in irradiance affect phyB activity has not been demonstrated. To address this issue, we investigated whether irradiance and R:FRs have similar effects on the nuclear distribution of phyB in petiole cells of light-grown plants. Under high-irradiance white light, phyB formed large nuclear bodies. Lowering irradiance without changing R:FRs or lowering R:FRs by adding far-red light led to the appearance of small nuclear bodies containing phyB. Large nuclear bodies remained but with some concomitant reduction in diameter. The appearance of small nuclear bodies was rapid, stable, and reversible upon the return to high irradiance and high R:FRs. High levels of red light but not of blue light were enough to restrain the formation of small phyB nuclear bodies. Irradiance was effective within the range found in natural canopies and even under relatively low R:FRs. The promotion of leaf hyponasty by lowering irradiance was impaired in phyB and pif mutants, as previously reported for the response to R:FRs. The expression of auxin-related genes showed a similar hierarchy of response to low R:FRs and low irradiance. We propose that phyB is able to perceive not only the low R:FRs, but also the low irradiance of shade.

Stem transcriptome reveals mechanisms to reduce the energetic cost of shade-avoidance responses in tomato.

While the most conspicuous response to low red/far-red ratios (R:FR) of shade light perceived by phytochrome is the promotion of stem growth, additional, less obvious effects may be discovered by studying changes in the stem transcriptome. Here, we report rapid and reversible stem transcriptome responses to R:FR in tomato (Solanum lycopersicum). As expected, low R:FR promoted the expression of growth-related genes, including those involved in the metabolism of cell wall carbohydrates and in auxin responses. In addition, genes involved in flavonoid synthesis, isoprenoid metabolism, and photosynthesis (dark reactions) were overrepresented in clusters showing reduced expression in the stem of low R:FR-treated plants. Consistent with these responses, low R:FR decreased the levels of flavonoids (anthocyanin, quercetin, kaempferol) and selected isoprenoid derivatives (chlorophyll, carotenoids) in the stem and severely reduced the photosynthetic capacity of this organ. However, lignin contents were unaffected. Low R:FR reduced the stem levels of jasmonate, which is a known inducer of flavonoid synthesis. The rate of stem respiration was also reduced in low R:FR-treated plants, indicating that by downsizing the stem photosynthetic apparatus and the levels of photoprotective pigments under low R:FR, tomato plants reduce the energetic cost of shade-avoidance responses.

Cryptochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis.

Green light added to blue light has been proposed to shift cryptochromes from their semireduced active form to the reduced, inactive state. Whether the increased proportion of green light observed under leaf canopies compared to open places reduces cryptochrome-mediated effects remained to be elucidated. Here we report that the length of the hypocotyl of Arabidopsis (Arabidopsis thaliana) seedlings grown under controlled conditions decreased linearly with increasing blue/green ratios of the light within the range of ratios found in natural environments. This effect was stronger under higher irradiances. We developed a model, parameterized on the basis of field experiments including photoreceptor mutants, where hypocotyl growth of seedlings exposed to different natural radiation environments was related to the action and interaction of phytochromes and cryptochromes. Adding the blue/green ratio of the light in the term involving cryptochrome activity improved the goodness of fit of the model, thus supporting a role of the blue/green ratio under natural radiation. The blue/green ratio decreased sharply with increasing shade by green grass leaves to one-half of the values observed in open places. The impact of blue/green ratio on cryptochrome-mediated inhibition of hypocotyl growth was at least as large as that of irradiance. We conclude that cryptochrome is a sensor of blue irradiance and blue/green ratio.

Low red/far-red ratios delay spike and stem growth in wheat.

The responses to low red light/far-red light (R/FR) ratios simulating dense stands were evaluated in wheat (Triticum aestivum L) cultivars released at different times in the 20th century and consequently resulting from an increasingly prolonged breeding and selection history. While tillering responses to the R/FR ratio were unaffected by the cultivars, low R/FR ratios reduced grain yield per plant (primarily grain number and secondarily grain weight per plant) particularly in modern cultivars. Low R/FR ratios delayed spike growth and development, reduced the expression of spike marker genes, accelerated the development of florets already initiated, and reduced the number of fertile florets at anthesis. It is noteworthy that low R/FR ratios did not promote stem or leaf sheath growth and therefore the observed reduction of yield cannot be accounted for as a consequence of divergence of resources towards increased plant stature. It is proposed that the regulation of yield components by the R/FR ratio could help plants to adjust to the limited availability of resources under crop conditions.

Metabolic responses to red/far-red ratio and ontogeny show poor correlation with the growth rate of sunflower stems.

In sparse canopies, low red to far-red (R/FR) ratios reach only vertically-oriented stems, which respond with faster rates of extension. It is shown here that this signal also promotes stem dry matter accumulation in sunflower (Helianthus annuus) but not in mustard (Sinapis alba L.). Physically blocking internode extension growth also blocked internode recovery of labelled carbon fed to the leaves, indicating that increased carbon accumulation is partially a consequence of increased extension growth in sunflower. However, low R/FR also promoted carbon accumulation in the lower section of the internode, where extension growth was unaffected. Although the levels of many soluble metabolites and of cell-wall carbohydrates increased in the stem in response to low R/FR, allowing conservation of their concentration, sucrose was present at a lower concentration under low R/FR. This change is anticipated to favour carbon unloading from the stem phloem. Low R/FR also reduced the levels of selected fatty acids, fatty acid alcohols, and sterols. Compared with the lower section, the upper section of the internode showed higher levels of organic acids, amino acids, fatty acids, and sterols. It is concluded that the promotion of stem extension growth by low R/FR ratios causes increased dry matter gain in sunflower internodes by a mechanism that is largely independent of changes in metabolism, since, whilst both low R/FR and ontogeny alter the metabolic profile, the changes do not correlate with the observed growth responses.