Jorge J. Casal

Photoreceptor Signaling Networks in Plant Responses to Shade

The dynamic light environment of vegetation canopies is perceived by phytochromes, cryptochromes, phototropins, and UV RESISTANCE LOCUS 8 (UVR8). These receptors control avoidance responses to preclude exposure to limiting or excessive light and acclimation responses to cope with conditions that cannot be avoided. The low red/far-red ratios of shade light reduce phytochrome B activity, which allows PHYTOCHROME INTERACTING FACTORS (PIFs) to directly activate the transcription of auxin-synthesis genes, leading to shade-avoidance responses. Direct PIF interaction with DELLA proteins links gibberellin and brassinosteroid signaling to shade avoidance. Shade avoidance also requires CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1), a target of cryptochromes, phytochromes, and UVR8. Multiple regulatory loops and the input of the circadian clock create a complex network able to respond even to subtle threats of competition with neighbors while still compensating for major environmental fluctuations such as the day-night cycles.

Phytochromes, Cryptochromes, Phototropin: Photoreceptor Interactions in Plants

Abstract In higher plants, natural radiation simultaneously activates more than one photoreceptor. Five phytochromes (phyA through phyD), two cryptochromes (cry1, cry2) and phototropin have been identified in the model species Arabidopsis thaliana. There is light-dependent epistasis among certain photoreceptor genes because the action of one pigment can be affected by the activity of others. Under red light, phyA and phyB are antagonistic, but under far-red light, followed by brief red light, phyA and phyB are synergistic in the control of seedling morphology and the expression of some genes during de-etiolation. Under short photoperiods of red and blue light, cry1 and phyB are synergistic, but under continuous exposure to the same light field the actions of phyB and cry1 become independent and additive. Phototropic bending of the shoot toward unilateral blue light is mediated by phototropin, but cry1, cry2, phyA and phyB positively regulate the response. Finally, cry2 and phyB are antagonistic in the induction of flowering. At least some of these interactions are likely to result from cross talk of the photoreceptor signaling pathways and uncover new avenues to approach signal transduction. Experiments under natural radiation are beginning to show that the interactions create a phototransduction network with emergent properties. This provides a more robust system for light perception in plants.

Tillering responses to enrichment of red light beneath the canopy in a humid natural grassland

(1) Enrichment of red light at the base of dallisgrass (Paspalum dilatatum Poir.) and smutgrass (Sporobolus indices [L.] R.Br.) plants in a dense humid natural grassland was obtained by use of small light-emitting diodes around the crown of each grass plant. (2) Results of this study supported the hypothesis that modification in light quality by a dense grassland canopy was detrimental to tiller populations. Tillering rates were increased and tiller death delayed until the end of the growing season when additional red light was supplied to the crown of plants. (3) The photocontrol of axillary bud activity may be part of a system whereby the tiller dynamics would be related to resources availability. (4) These results also suggest that maintenance of a grass sward at a high leaf area index might not be a good management strategy for long-term productivity.

Light signals perceived by crop and weed plants

Abstract Light signals perceived by specific plant photoreceptors such as phytochromes, cryptochromes and phototropin play a central role controlling the physiology and development of weed and crop plants. Knowledge about these controls has been gained in the last decade thanks to the combination of eco-physiological experiments under conditions of natural radiation with classical photobiological techniques and genetic and biotechnological tools. This progress has important ramifications for our understanding of the physiology of crop growth and development, as well as the mechanisms of crop–weed competition. In this paper we discuss some of the recent advances in the field of environmental photomorphogenesis and highlight their agricultural implications.

Phytochrome A Mediates the Promotion of Seed Germination by Very Low Fluences of Light and Canopy Shade Light in Arabidopsis.

Seeds of the wild type (WT) and of the phyA and phyB mutants of Arabidopsis thaliana were exposed to single red light (R)/far-red light (FR) pulses predicted to establish a series of calculated phytochrome photoequilibria (Pfr/P). WT and phyB seeds showed biphasic responses to Pfr/P. The first phase, i.e. the very-low-fluence response (VLFR), occurred below Pfr/P = 10-1%. The second phase, i.e. the low-fluence response, occurred above Pfr/P = 3%. The VLFR was similarly induced by either a FR pulse saturating photoconversion or a subsaturating R pulse predicted to establish the same Pfr/P. The VLFR was absent in phyA seeds, which showed a strong low-fluence response. In the field, even brief exposures to the very low fluences of canopy shade light (R/FR ratio < 0.05) promoted germination above dark controls in WT and phyB seeds but not in the phyA mutant. Seeds of the phyA mutant germinated normally under canopies providing higher R/FR ratios or under deep canopy shade light supplemented with R from light-emitting diodes. We propose that phytochrome A mediates VLFR of A. thaliana seeds.

Phytochromes and seed germination

The control of seed germination by red and far-red light is one of the earliest documented phytochrome-mediated processes Phytochrome is now known to be a small family of photoreceptors whose apoproteins are encoded by different genes Phytochrome B (phyB) is present in dry seeds and affects germination of dark imbibed seeds but other phytochromes could also be involved Phytochrome A (phyA) appears after several hours of imbibition and mediates very-low-fluence responses PhyB and other phytochromes different from phyA mediate the classical low-fluence responses The phytochrome involved in high-irradiance responses of seed germination (inhibition of germination under continuous far-red) has not been unequivocally established, although phyA is the most likely candidate Phytochrome can affect embryo growth capacity and/or the constraint imposed by the tissues surrounding the embryo At least in some species, gibberellins participate in the signalling process In the field, phyA has been implicated in the perception of light during soil cultivations, and phyB would be involved in the perception of red/far-red ratios associated with the presence of gaps in the canopy This review describes recent advances in phytochrome research, particularly those derived from the analysis of germination in specific mutants, and their connection with traditional observations on phytochrome control of seed germination

The effect of plant density on tillering: The involvement of R/FR ratio and the proportion of radiation intercepted per plant

Abstract Plants of Paspalum dilatatum and Lolium multiflorum were grown in pots at different densities. Half of the plants at each density received additional red light at their bases by means of light-emitting diodes. Density reduced both the proportion of incident radiation intercepted per plant and the red/far-red ratio of the light at plant bases. Tillering decreased with density in both species. P. dilatatum plants also had fewer reproductive tillers and expanded leaves and a higher mortality of young vegetative tillers in denser stands. In both species the enrichment with red light did not increase tillering of isolated plants, but increased it in stands grown at relatively low densities with small degrees of mutual shading. At these densities P. dilatatum plants achieved the number of tillers of isolated plants. Moreover, red light increased vegetative tiller death in the P. dilatatum dense canopy. These results suggest that low red/far-red ratios might preclude morphogenic responses to density before an important depletion in energy availability takes place.

Phytochrome regulation of branching in Arabidopsis.

The red light:far-red light ratio perceived by phytochromes controls plastic traits of plant architecture, including branching. Despite the significance of branching for plant fitness and productivity, there is little quantitative and mechanistic information concerning phytochrome control of branching responses in Arabidopsis (Arabidopsis thaliana). Here, we show that in Arabidopsis, the negative effects of the phytochrome B mutation and of low red light:far-red light ratio on branching were largely due to reduced bud outgrowth capacity and an increased degree of correlative inhibition acting on the buds rather than due to a reduced number of leaves and buds available for branching. Phytochrome effects on the degree of correlative inhibition required functional BRANCHED1 (BRC1), BRC2, AXR1, MORE AXILLARY GROWTH2 (MAX2), and MAX4. The analysis of gene expression in selected buds indicated that BRC1 and BRC2 are part of different gene networks. The BRC1 network is linked to the growth capacity of specific buds, while the BRC2 network is associated with coordination of growth among branches. We conclude that the branching integrators BRC1 and BRC2 are necessary for responses to phytochrome, but they contribute differentially to these responses, likely acting through divergent pathways.

Maize Leaves Turn Away from Neighbors

In commercial crops, maize (Zea mays) plants are typically grown at a larger distance between rows (70 cm) than within the same row (16–23 cm). This rectangular arrangement creates a heterogeneous environment in which the plants receive higher red light (R) to far-red light (FR) ratios from the interrow spaces. In field crops, the hybrid Dekalb 696 (DK696) showed an increased proportion of leaves toward interrow spaces, whereas the experimental hybrid 980 (Exp980) retained random leaf orientation. Mirrors reflecting FR were placed close to isolated plants to simulate the presence of neighbors in the field. In addition, localized FR was applied to target leaves in a growth chamber. During their expansion, the leaves of DK696 turned away from the low R to FR ratio signals, whereas Exp980 leaves remained unaffected. On the contrary, tillering was reduced and plant height was increased by low R to FR ratios in Exp980 but not in DK696. Isolated plants preconditioned with low R/FR-simulating neighbors in a North-South row showed reduced mutual shading among leaves when the plants were actually grouped in North-South rows. These observations contradict the current view that phytochrome-mediated responses to low R/FR are a relic from wild conditions, detrimental for crop yield.

Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis.

In open places, plants are exposed to higher fluence rates of photosynthetically active radiation and to higher red to far-red ratios than under the shade of neighbor plants. High fluence rates are known to increase stomata density. Here we show that high, compared to low, red to far-red ratios also increase stomata density in Arabidopsis (Arabidopsis thaliana). High red to far-red ratios increase the proportion of phytochrome B (phyB) in its active form and the phyB mutant exhibited a constitutively low stomata density. phyB increased the stomata index (the ratio between stomata and epidermal cells number) and the level of anphistomy (by increasing stomata density more intensively in the adaxial than in the abaxial face). phyB promoted the expression of FAMA and TOO MANY MOUTHS genes involved in the regulation of stomata development in young leaves. Increased stomata density resulted in increased transpiration per unit leaf area. However, phyB promoted photosynthesis rates only at high fluence rates of photosynthetically active radiation. In accordance to these observations, phyB reduced long-term water-use efficiency estimated by the analysis of isotopic discrimination against 13CO2. We propose a model where active phyB promotes stomata differentiation in open places, allowing plants to take advantage of the higher irradiances at the expense of a reduction of water-use efficiency, which is compensated by a reduced leaf area.