Essay 17.3

Know Thy Neighbor through Phytochrome

C. L. Ballaré, A. Scopel, J. J. Casal and R. A. Sánchez, IFEVA, Facultad de Agronomía, Universidad de Buenos Aires and CONICET.

May, 2006

Plants are continuously exposed to a variable environment, and they often experience wide variations both in the abiotic as well as in the biotic components of their surroundings. For growth and development to proceed harmoniously, the plants have to adjust to these changes. This is a formidable task and depends on a sophisticated network of sensing mechanisms. These systems acquire information from the environment and relay this information to a series of control mechanisms that elicit acclimation responses at many levels, from the cell to the whole-plant. Light is one of the richest sources of information and, accordingly, plants have an impressive array of photoreceptors that monitor the radiation environment and initiate interacting signaling networks.

For plants growing in a crowded population, a proper assessment of the competition threat posed by neighboring plants is extremely important. This is particularly evident in the nearly even canopies formed by seedling populations emerged after a disturbance (i.e., after a tillage operation or a gap opened in grassland). Under these conditions, a slight difference in height might imply important differences in light availability.

Plants can detect the presence of neighbors very early, well before mutual shading occurs. Upon detection of the proximity of potential competitors many plants respond with a series of morphological changes, the most conspicuous of which is a strong stimulation of stem elongation (Figure 1). The increased height growth positions the plant to intercept light better when competition finally arrives.

Figure 1 (A) Seedlings of Datura ferox growing at increasing densities (32, 100 and 240 seedlings m^-2, from bottom up) for three weeks show larger stem elongation. (From Ballaré and Casal 2000, reproduced with permission from Elsevier Science.) (B) As an even canopy develops with time, perception of the neighbors stimulates stem elongation, and increased leaf area results in a decrease in light intereception per plant. However, the elongation response precedes mutual shading. (After Ballaré et al. 1988.) (Click image to enlarge.)

The early perception of neighbor proximity is based on the detection of changes in the spectral composition of solar radiation that are produced by interaction of sunlight with green leaves. Leaves effectively absorb photons in the blue (B, 400–500 nm) and red wavebands (R, 500–600 nm) of the solar spectrum. Absorption in the green (400–500 nm), and particularly in the far-red region (FR, 700-800 nm) is weaker and many photons of these wavelengths are back scattered in the form of diffuse radiation. We are sensitive to the green photons that bounce off the leaves (that is why we see leaves as green), but we cannot see FR radiation because our photoreceptors are blind to wavelengths longer than 700 nm. The plant photoreceptors phytochromes, in contrast, are maximally sensitive in the R and FR regions of the spectrum.

As plants grow and the leaf area index (LAI, leaf area per unit ground area) of the canopy increases, the ratio of R to FR radiation (i.e., R:FR) of the light reaching the stems of each individual plant decreases (Figure 2A). In the very low range of LAIs (LAI < 1.0; plants do not shade each other), the R:FR decreases mainly because there is an increase in reflected FR. In dicots with erect main stems, this increase in FR modifies the light environment of the internodes (Figure 2B) without greatly affecting the spectral balance of the leaves, which is dominated by the contribution of direct sunlight. The resulting decrease in R:FR is of enough magnitude to be sensed by phytochrome molecules located in the stem tissue. The lower R:FR causes a reduction in the proportion of phytochromes that are in the active (Pfr) form and this reduction, in turn, stimulates stem elongation. That a sensing mechanism plays a role in the early detection of neighboring plants has been supported by numerous studies, which demonstrated that:

Figure 2 (A) Relationship between R:FR and LAI in canopies of Datura ferox. Measurements were taken at midday using either a cosine-corrected planar surface detector (top graph) placed at the height of maximum leaf density (open symbols) or at ground level (closed symbols), or an integrating cylinder (bottom graph) designed to measure the R:FR of light flux from all compass points parallel to soil surface. (From Ballaré et al. 1987, reproduced with permission from Blackwell Publishing.) (B) Effects of canopy density on the light regime within the first internode obtained with a fibre-optic probe inserted into the stem tissue of Datura ferox plants. A value of 1 in the ordinate represents the photon fluence rate measured at the corresponding wavelenght when the LAI of the canopy was zero. (From Ballaré, Scopel, and Sánchez 1991, reproduced with permission from Blackwell Publishing.) (Click image to enlarge.)

(1) the effect of neighboring vegetation on stem elongation can be mimicked by selective mirrors reflecting mainly in the FR region (Figure 3),

Figure 3 Plants of Datura ferox growing in front of selective reflecting mirrors placed at ca. 6 cm south (southern hemisphere) of the plants. Those in front of the mirrors selectively reflecting FR show increased internode elongation. (From Ballaré and Casal 2000, reproduced with permission from Elsevier Science.) (Click image to enlarge.)

(2) the changes in FR are quantitatively correlated with the density and proximity of surrounding vegetation (Figure 2A), and

(3) filtering out FR from the light received by individual internodes can prevent the elongation response at low densities (LAI<1.0) in even canopies (Figure 4).

Figure 4 Elongation of the first internode of Datura ferox seedlings when plants were exposed to background canopies of different LAI. (A) The internodes were surrounded by water filters (open symbols) or by CuSO₄ (FR-blocking) filters maintaining the R:FR constant and high over a range of canopy densities (closed symbols) as illustrated in (B). The dashed line is the extension rate of isolated seedlings with internodes covered by water filters. Exposure times were 3 days. In the bottom of the figure, the photosynthetic photon flux (PPF) intercepted per individual seedling is shown. The dotted line represents PPF intercepted by isolated plants. ((A) from Ballaré, Scopel and Sánchez 1990, reproduced with permission from the American Association for the Advancement of Science. (B) From Ballaré and Casal 2000, reproduced with permission from Elsevier Science.) (Click image to enlarge.)

Genotypes with altered phytochrome composition cannot properly perceive the early warning signal of the presence of neighbors. Cucumber and Arabidopsis mutants lacking phytochrome B (phyB) do not change their elongation rate in response to the light reflected from nearby plants. This suggests that phyB plays a central role in the perception of changes in R:FR ratio brought about by non-shading neighbors. Although phytochrome A (phyA), another member of the phytochrome family, is not directly involved in the responses to R:FR ratio, alterations in its level can greatly affect early neighbor detection. Both phyA Arabidopsis mutants and tobacco and potato overexpressors of phyA lack stem growth responses to FR reflected from neighbors. The lack of phyA likely hinders the perception of the signal because it reduces the sensitivity of phyB to reductions in R:FR. On the other hand, overexpressors of phyA sometimes react to increased FR, producing an inhibition of elongation. This inhibition is likely a reflection of another type of phytochrome response known as high-irradiance response (HIR), which is mediated by phyA and triggered most effectively by FR radiation. When the phyA levels are kept high in the de-etiolated plants by overepression of transgenic phyB, the inhibitory effect of the phyA HIR may counteract the promoting effect of the low R:FR ratio perceived by phyB. This idea is supported by the observations that phyA overexpressors do not show stem growth promotion when FR is added to white light, but they do respond with increased growth when the R:FR ratio is reduced by lowering the R component. Thus too little or too much phyA appears to impair early neighbor detection.

It is clear that early neighbor detection depends on a finely tuned interaction between at least two phytochromes, which includes precise control of their amounts and tissue sensitivity to their active forms. The lack of mention of the actions of other phytochromes and the cryptochromes in neighbor detection does not mean that these photoreceptors do not play any role. It is known that other stable phytochromes can mediate responses to R:FR, and it is likely that in some species or environmental scenarios they contribute to the modulation of plant acclimation to the canopy environment. However, the relevant field experiments to test this possibility have not yet been carried out.

References

Ballaré, C. L., and Casal, J. J. (2000) Light signals perceived by crop and weed plants. Field Crops Research 67(2): 149–160.

Ballaré, C. L., Scopel, A. L., and Sánchez, R. A. (1990) Far-Red radiation reflected from adjacent leaves: An early signal of competition in plant canopies. Science 247: 329–332.

Ballaré, C. L., Scopel, A. L., and Sánchez, R. A. (1991) Photocontrol of stem elongation in plant neighborhoods: Effects of photon fluence rate under natural conditions of radiation. Plant, Cell and Environment 14: 57–65.

Ballaré, C. L., Sánchez, R. A., Scopel, A. L., and Ghersa, C. M. (1988) Morphological responses of Datura ferox seedlings to the presence of neighbours. Their relationship with canopy microclimate. Oecologia 76: 228-293.

Ballaré, C. L., Sánchez, R. A., Scopel, A. L., Casal, J. J., and Ghersa, C. M. (1987) Early detection of neighbor plants by phytochrome perception of spectral changes in reflected sunlight. Plant, Cell and Environment 10: 551–557.

Casal, J. J., Sánchez, R. A., and Vierstra, R. D. (1994) Overexpression of oat phytochrome: A gene differentially affects stem growth responses to red/far red ratio signals characteristic of sparse or dense canopies. Plant, Cell and Environment 17: 409–417.