Light signals perceived by crop and weed plants

Transcription

1 Field Crops Research 67 (2000) 149±160 Light signals perceived by crop and weed plants Carlos L. Ballare *, Jorge J. Casal IFEVA, Agricultural Plant Physiology and Ecology Research Institute, University of Buenos Aires and CONICET, Av. San Martin 4453, 1417 Buenos Aires, Argentina Abstract Light signals perceived by speci c 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 rami cations 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 eld of environmental photomorphogenesis and highlight their agricultural implications. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Biotechnology; Cryptochrome; Photomorphogenesis; Phytochrome; Plant density; Shade avoidance; Yield 1. Introduction Solar radiation is an essential determinant of crop yield in many ways Ð via photosynthesis, sunlight fuels crop growth and development. Solar radiation is also a major determinant of the energy balance of the soil and the plants, and drives water and nutrient transport. In addition, light perceived by speci c photoreceptors (non-photosynthetic pigments) including phytochromes, cryptochromes and phototropin, induces photomorphogenic responses, in uencing both the pattern of investment of captured * Corresponding author. Tel.: , ext. 8101; fax: addresses: ballare@ifeva.edu.ar (C.L. BallareÂ), casal@ifeva.edu.ar (J.J. Casal) resources and the ability of the plant to capture further resources. The effects of light signals perceived by these photoreceptors can be different for the crop and the accompanying weeds. Consequently, photomorphogenic responses of crop and weed plants are predicted to alter the interactions between these two components of the system. In this paper we outline the current state of knowledge about photomorphogenic controls of plant development in crop canopies, and highlight areas in which the manipulation of photomorphogenesis could be used to alter crop±weed interactions and crop yield. For more comprehensive discussions of the agricultural implications of photomorphogenic signaling, the reader is referred to previous reviews by Smith (1992), Ballare et al. (1992b, 1995a, 1997), SaÂnchez et al. (1993), and Holt (1995) /00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S (00)

2 150 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149± Processes controlled by photomorphogenic mechanisms 2.1. Seed germination The seeds of a large number of weed species require light for germination (Baskin and Baskin, 1998; Casal and SaÂnchez, 1998). Weed seeds are frequently dispersed during crop harvest and buried during soil preparation for fallow. These seeds experience prolonged periods of darkness in the soil, until some of them become brie y exposed to light during subsequent tillage operations. This brief exposure to light is enough to induce germination of signi cant quantities of weed seeds (Scopel et al., 1991; Botto et al., 1998b). The ability of weed seeds to germinate in response to very brief exposures to light can be acquired during burial (Taylorson, 1972; Scopel et al., 1991). This sensitization has been interpreted as a transition from the low- uence to the very-low- uence response modes of phytochrome action (Scopel et al., 1991). For some species, this sensitization process is believed to be dependent on exposure to low temperatures during winter; however, this is not always the case. In Datura ferox, sensitization occurs at relatively warm temperatures (Scopel et al., 1991), and the process is in uenced by depth of burial, showing an optimum around 5 cm, and it is impaired by the presence of plant cover (Botto et al., 1998a). Phytochrome A, a specialized member of the phytochrome family, operates like an antenna in the perception of these very-low- uences of light (Botto et al., 1996; Shinomura et al., 1996). Very often, weed seeds that require brief exposures to light to induce germination will not germinate when exposed to prolonged periods of intense sunlight on the surface of the soil (Botto et al., 1998a). The seeds of most crops do not require light to germinate and are normally buried in complete darkness. Very likely, this sowing practice has been a pressure for selection against a light requirement for germination in the case of crop seeds. Genetic differences in seed photoresponses are not only observed between crops and weeds but also among different weed species. Seeds of many weeds only germinate when present very close to or on the surface of the soil and in the absence of vegetation cover. In this case, the stimulus is not a brief pulse of light but the high red to far-red photon ratio (R:FR) of sunlight (Deregibus et al., 1994; Insausti et al., 1995). The R:FR of sunlight reaching bare soil is approximately 1.1 during most part of the day (Smith and Holmes, 1977); when light reaches green plant organs, the R:FR decreases due to selective light absorption (strong for R, weak for FR), transmission and re ection (both weak for R and strong for FR); see Holmes and Smith (1977). Small reductions of the R:FR (for instance from 1.1 to 0.8 or 0.9) are enough to inhibit or reduce germination in several species, including Lolium multi orum, Silene gallica, and Brassica campestris (Deregibus et al., 1994; Batlla et al., 2000). These slightly reduced R:FR ratios are typical of sparse canopies, with leaf area indexes below one. Changes in R:FR that regulate seed germination are perceived by other members of the phytochrome family (phytochrome B is quantitatively the most important); see Botto et al. (1995). These examples illustrate how versatile phytochrome-mediated light perception can be. Whereas some seeds are able to distinguish between full darkness and milliseconds of light, others are able to distinguish between full sunlight and light with slightly decreased R:FR. The perception of these signals allows weed seeds to germinate simultaneously with (or slightly earlier than) the crop, when photosynthetic light and other resources are abundant Shoot elongation and branching After seedling emergence, mutual plant shading and competition for photosynthetic light becomes intense when the canopy begins to close. However, interference between crop and weed seedlings can be established much earlier. The re ection of FR by green plant parts lowers the R:FR of horizontally propagated light before there is a signi cant degree of mutual plant shading (Ballare et al., 1987). In turn, this modi es the light environment in the stem tissue, and elicits changes in stem elongation rate (Ballare et al., 1990); see Fig. 1. Phytochrome B appears to play an important role perceiving this early signal of competition (Whitelam and Smith, 1991; Ballare et al., 1991a; Yanovsky et al., 1995a). The pattern of distribution of the products of photosynthesis is altered in this way before photosynthesis is reduced by mutual shading. The most characteristic effects of reduced R:FR are enhanced axis elongation and reduced branching.

3 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149± Fig. 1. Photomorphogenic responses of Datura ferox to the proximity of neighbors. Left panels: Effects of increasing plant density on plant morphology and stand architecture. Notice the increase in plant height with density, particularly in the plants located at the center of the high density stand. Top right: Selective mirrors used to mimic the proximity of neighbors; the mirror on the right-hand side re ects FR with high ef ciency, which promotes shoot elongation in plants grown under full sunlight. Bottom right: Collar lters used to alter the light environment of individual internodes in plants grown in real canopies. When the lters were lled with copper sulfate, which absorbs FR, the elongation response at low densities was abolished. For details, see Ballare et al. (1987, 1990). Increased stem growth has been observed in many cultivated and weedy dicots (e.g., Morgan and Smith, 1979). In grasses, low R:FR can reduce tillering and enhance leaf sheath growth (Casal et al., 1985). These processes are so sensitive to R:FR that stem growth of Sinapis alba seedlings can be increased by more than 50% in response to FR back re ected by green fences placed to the South (Southern hemisphere) to avoid shading the target plant (Ballare et al., 1987); see Fig. 2. Similarly, plants of Paspalum dilatatum grown in pots placed at low densities (<7 plants m 2 ) do not shade each other but show a reduction of tillering of 40% compared to isolated controls (Casal et al., 1986). Qualitatively similar results were obtained by Davis and Simmons (1994) working with barley. In P. dilatatum, the reduction in tillering was fully reversible by the addition of small (photosynthetically negligible) amounts of R to the base of the plants (Casal et al., 1986). In L. multi orum micro swards, reductions in plant tillering in response to plant density precede changes in dry matter gain. Low R:FR reduce the rate of site lling, i.e., the ratio between number of tillers and tiller bud positions (leaves); see Casal et al. (1987). At least in L. multi orum, small to moderate reductions in R:FR (e.g., to 0.5) have strong effects on tillering and there is no obvious indication of further inhibition by more intense reductions of the R:FR (Casal et al., 1987). With continued canopy growth, mutual shading becomes more intense. R:FR is further reduced and can go down to approximately 0.1 at the base of dense stands. The low R:FR signal, which immediately after emergence is detectable only on vertically oriented organs, becomes also intense at the level of the leaves.

4 152 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149±160 Fig. 2. Remote detection of plant neighbors. Mustard plants placed in front of green grass fences (left panels), which re ect FR and lower the R:FR of the side light, grow taller than the counterparts placed in front of similar fences that were bleached by the application of a herbicide (right panels). For details, see Ballare et al. (1987). At least in S. alba, treatment of the leaves with low R:FR induces a promotion of stem growth that persists for many hours, even after the low R:FR signal is eliminated (Casal and Smith, 1988). In addition, mutual shading reduces the photon ux density at all wavelengths, rst in the stem and later in the leaves, particularly those leaves placed in lower strata. The reduction in the blue waveband is perceived by cryptochromes (in particular cryptochrome 1) and the reduction of FR is perceived by phytochrome A (Yanovsky et al., 1995a, 1998). These changes in the light environment also trigger morphological responses, such as increased stem elongation (Ballare et al., 1991b). Photomorphogenic responses may involve changes in the partitioning of photoassimilates. The lh mutant of cucumber is de cient in phytochrome B and exhibits constitutively exaggerated stem growth, characteristic of plants grown in dense stands (LoÂpez Juez et al., 1992). This mutant has heavier stems than the wild type, but the difference in dry weight is not as large as the difference in length; the lh mutant has a lower dry weight to length ratio (Casal et al., 1994), which corresponds to a decreased stem diameter. Leaf growth (area, dry weight) and root growth are concomitantly reduced. The situation can be different in plants exposed to treatments of low R:FR that are restricted to the stem. In an experiment with Amaranthus quitensis, a low R:FR treatment applied to the stem increased stem length and dry weight but did not affect leaf or root growth (Ballare et al., 1991c). Consequently, plants of this weed receiving low R:FR in the internodes accumulated more dry matter than the high R:FR controls. Apparently, the low R:FR stimulus increased stem sink strength, and indirectly enhanced photosynthesis. In S. alba, the same treatment increased stem length but hardly affected stem dry matter (Casal et al., 1995). In the latter species, stem dry weight is enhanced by low R:FR when this signal also reaches the leaves. When only one leaf of the pair attached to the rst internode is exposed to low

5 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149± R:FR, this leaf shows increased activity of sucrosephosphate synthase (an enzyme involved in the control of sucrose export from the leaves) increased export of labeled carbon, and reduced growth compared to the control under high R:FR (Yanovsky et al., 1995b). This indicates that although stem growth and dry matter partitioning are correlated, changes in dry matter allocation are not the mere result of changes in stem elongation Organ orientation Plants also respond to changes in the light environment with changes in the orientation of whole shoots and individual leaves. Differential growth of illuminated and shaded sides of the stem results in phototropic bending of the shoot toward gaps in the canopy. The gradient of blue light, perceived by the photoreceptor phototropin, plays a crucial role in this response (Liscum and Briggs, 1995; Christie et al., 1998). Plants are also able to perceive horizontal gradients of R:FR and redirect their shoots toward canopy gaps, where the R:FR ratio is high (Novoplansky et al., 1990; Ballare et al., 1992a). These movements involve the action of phytochrome B (Ballare et al., 1992a), and are thought to be of particular importance for the colonization of patchy canopies (Regnier and Bakelana, 1995; Ballare et al., 1995b). Interestingly, the parasite plant Cuscuta plani ora shows exactly the opposite response, and moves toward sources of low R:FR (Orr et al., 1996). This response is likely to help the parasite to nd host plants. In some species, individual leaves can also be reoriented by changes in turgor taking place at the point of insertion of the petiole or of the lamina. This movement occurs in response to gradients of blue light (Ritter and Koller, 1994) but can also be modulated by the R:FR ratio (Casal and Sadras, 1987). Very often, the leaves adopt a position normal to the main axis of incident radiation, increasing the amount of radiation intercepted. Depending on the species and even on growth conditions, the movement may be the opposite, reducing radiation load (Woolley et al., 1984). Tillers appear with an upright position in grass plants and gradually adopt a more prostrate habit with time (Gibson et al., 1992). This movement, articulated at the base of the tillers, is less pronounced in plants grown at high densities than in plants grown low densities (Gibson et al., 1992). Low R:FR often cause a more erect position of the tillers (Casal et al., 1990). Similarly, Arabidopsis thaliana plants respond to crowding in monocultures by producing leaves with erect petioles, and this response is mediated by phytochrome B (Ballare and Scopel, 1997). Taken together, these observations indicate that plants respond to photomorphogenic signals in dense canopies with changes in shoot geometry that increase the likelihood of intercepting photosynthetic light (active ``foraging'' for light); see Ballare et al. (1995b) Leaf senescence Incident light undergoes gradual extinction within plant canopies due to absorption by chlorophyll. This creates a vertical gradient of irradiance and of R:FR (Holmes and Smith, 1977). The leaves placed at lower strata of the canopy are exposed to low levels of photosynthetically active radiation and to low R:FR, and both signals co-operate to accelerate leaf senescence (Rousseaux et al., 1996). In sun ower crops, leaf senescence can be delayed by the addition of R, that increases the R:FR perceived by phytochrome, but not by supplementary green light, that increases photosynthetically active radiation but makes a negligible contribution to phytochrome status (Rousseaux et al., 1996). The response to R:FR is local and not systemic. Irradiation of restricted portions of the leaf with FR accelerates senescence of that particular region (Rousseaux et al., 1997). Under certain conditions, changes in R:FR can also affect tiller senescence (Deregibus et al., 1985; but see Skinner and Simmons, 1993) Flowering Sowing date determines the photoperiod to which the plants are exposed. The transition of the apex to the reproductive stage is affected in many species by the length of the daily light period. Long-day plants ower or ower earlier when the photoperiod is longer than a given length. Short-day plants ower or ower earlier when the photoperiod is shorter than a given length. Neutral plants do not respond to photoperiod. These differences can be found among different species but also among different genotypes within a given species. Plants of Pisum sativum or A. thaliana lacking phytochrome A as well as plants of A. thaliana

6 154 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149±160 lacking cryptochrome 2 show late owering under long days (Johnson et al., 1994; Weller et al., 1995; Guo et al., 1998). Both species are long-day plants and the effects of the mutations indicate that phytochrome A and the blue light receptor cryptochrome 2 are involved in photoperiod sensing. Measurement of day length involves the interaction of the light on/off signal with a circadian clock and, in addition, light is involved in the synchronization of the circadian clock (Somers et al., 1998). The role played by these and other photoreceptors in the two actions of light has not been fully elucidated. In some cases, owering may be accelerated by high compared to low stand densities (Kirby, 1967; Weston, 1982; Yu et al., 1998). A similar effect has been observed in response to low compared to high R:FR ratios. In addition, mutants of P. sativum or Sorghum bicolor (a short-day plant) lacking phytochrome B, and of A. thaliana lacking phytochrome B, D or E also ower earlier than the wild types (Goto et al., 1991; Weller et al., 1995; Childs et al., 1997; Devlin et al., 1998, 1999). Taken together, these observations indicate that the low R:FR of dense canopies, perceived by phytochromes B, D and E, accelerate owering Tuber and bulb formation The production of tubers and bulbs shows a pattern of response to photomorphogenic signals comparable to that of the owering response. Tuberization in potato is often inhibited by long days, although there is considerable genetic variability. Phytochrome A participates in this response (Izaguirre, Yanovsky, Gatz, Thomas and Casal, unpublished data). Transgenic plants of potato with reduced levels of phytochrome B (due to expression of an anti-sense gene) show early tuber production even under long days (Jackson et al., 1996). This indicates that low R:FR typical of plant canopies could accelerate tuberization. Actually, this is the case for bulb production in onions (Mondal et al., 1986) Fruit set Only a few studies have investigated the role of photomorphogenic signals in determining patterns of fruit set and abortion. This situation is hardly surprising given the enormous dif culties involved in manipulating the light environment of full-grown, reproductive crops in the eld. Heindl and Brun (1983) reported that supplementary R applied to the lower canopy strata of eld-grown soybean crops reduced ower and fruit abortion. The lighting treatment was perceived by the primordia themselves. These studies as well as experiments under controlled-environmental conditions (e.g., Myers et al., 1987) indicated that it may be feasible to reduce reproductive abscission and increase yield by manipulating the light responses of reproductive primordia. Of course the relationships between abortion and grain yield will depend greatly on the balance between source and sink limitations, an issue that has often been discussed on the basis of correlative evidences and of experimental manipulations that may have had several side effects on the physiology of the crops. The techniques available at present to genetically manipulate photomorphogenic responses should provide ideal tools to address these issues in a more straightforward way. 3. Manipulation of photomorphogenesis Photomorphogenic responses in eld crops can be manipulated by changing the light environment or by altering the sensitivity of the crop plants to photomorphogenic light signals. Alterations in the light environment (as used in horticultural crops; e.g., McMahon and Kelly, 1990; Kasperbauer, 1992) are not feasible over large areas of land, but the manipulation of the timing of tillage operations and the use of poly-crops and relay crops offers some room for inducing variations in the light environment to which crops and weeds are exposed. In addition, it was proposed sometime ago that the photomorphogenic behavior of crop plants could be modi ed in order to increase crop yields (Smith, 1992; Ballare et al., 1992b; SaÂnchez et al., 1993), and some experiments have been conducted that shed light about the potential advantages and limitations of this approach. In the following we will brie y discuss the results of recent eld studies on the consequences of manipulating photomorphogenic signals and responses.

7 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149± Manipulation of the light environment Soil tillage promotes weed seed germination and it has been shown that, for some species, this promotion is caused by light. Thus, daytime tillage often results in larger uxes of germination compared with nighttime tillage (Hartmann and Nezadal, 1990; Scopel et al., 1994; Botto et al., 1998b). Covering of the tillage implements during cultivation was shown to reduce the germination response of dicot weeds in experiments carried out in the Willamette Valley (Oregon, USA); in the same experiments arti cial illumination during nighttime tillage promoted weed seedling emergence (Scopel et al., 1994). Furthermore, covering the soil with opaque screens after tillage did not affect the number of emerging seedlings, compared with plots covered with clear screens, in experiments carried out in San Claudio, Buenos Aires (Botto et al., 1998b). Collectively these results indicate that the photoinduction of weed seed germination during tillage depends mainly, if not exclusively, on the photons that hit the seeds while the soil is being disturbed by the cultivation tools (Scopel et al., 1994; Botto et al., 1998b). Therefore, the manipulation of the light environment during tillage could be a useful tool to reduce weed seedling emergence (Fig. 3). A few eld experiments have been carried out to test this hypothesis; the results in some cases have been promising, but a lot of variability is apparent in the data available at present (Hartmann and Nezadal, 1990; Jensen, 1992; Ascard, 1994; Scopel et al., 1994; Buhler, 1997; Botto et al., 1998b). This variability is not surprising; in fact the seeds of many weed species can germinate in complete darkness, and for a given species the light requirement can uctuate on a seasonal basis (Baskin and Baskin, 1998). In addition, for a particular weed ora, the importance of light as a trigger of germination may depend on the type of implement used to cultivate the soil. Botto et al. (1998b) found large differences in seedling densities between nighttime Fig. 3. Promotion of weed seedling emergence by daytime tillage. The experiments were conducted in the Willamette Valley, Oregon, USA with a mould-board plow followed by two passes of a dual-action disc harrow. The predominant weed is Amaranthus retro exus. For details, see Scopel et al. (1994).

8 156 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149±160 and daytime cultivation when they used a moldboard plow for primary cultivation but such differences were not apparent in elds tilled with a chisel plow. Thus the impact of manipulating the tillage photoenvironment on weed seedling recruitment should be tested on a case-by-case basis. Since the acquisition of light sensitivity during burial is, at least for some weed species, affected by such factors as depth in the soil and vegetation cover (Botto et al., 1998a), it might be possible to manipulate the degree of light sensitivity of weed seed banks by managing these factors during the fallow period. Very little work has been carried out to investigate the consequences for crop±weed competition of altering the photomorphogenic light environment. Ghersa et al. (1994) and MartõÂnez-Ghersa and Ghersa (1999) modi ed the light environment of wheat crops during the initial stages of canopy development. They used screens and/or relay crops of summer annual species to cause a reduction in the photon ux density and R:FR received at the soil surface, and studied competitive interactions between wheat and the annual weed L. multi orum. Although the light treatments were imposed only for short periods (the lters were removed a few days after sowing and the plants of the relay crop were killed by the rst frosts), they had a persistent effect on competitive balance. For example, the use of a summer relay crop during the period of seedling emergence greatly affected L. multi orum plants, reducing biomass production, and improving the growth and yield of wheat. MartõÂnez-Ghersa and Ghersa (1999) speculated that these results might be interpreted on the basis of differences in photomorphogenic sensitivity between wheat and L. multi orum. They argued that the reduction in R:FR imposed by the open canopy of the relay crop affected the germination of the weed and its morphological development. These responses did not occur in the wheat, which bene ted from a lower plasticity, because the ltering treatments were short-lived. The treatments used by MartõÂnez- Ghersa and Ghersa (1999) altered several parameters of the light environment at the same time; therefore, as the authors acknowledged, it is dif cult to reach conclusions about the underlying mechanisms. However, their results indicate that there is room for developing weed control technologies on the basis of an understanding of photosensory processes in crop canopies. Unfortunately, because most of the research on weed control strategies is fueled by herbicide manufacturers, these alternative approaches to weed management have not received much attention Manipulation of crop photomorphogenesis The alteration of photomorphogenically driven plant responses to population density might be used to alter yield:density relationships and increase crop yield. It has been proposed that plants impaired in photomorphogenic perception could employ the photoassimilates normally invested in elongation responses to sustain economically more productive functions, such as the growth of harvestable organs (Smith, 1992). Because variation in morphological sensitivity to light signals is known to exist among cultivars of the same species (e.g., Casal, 1988; Knauber and Banowetz, 1992), alterations of crop plant photomorphogenic behavior may be achieved by conventional breeding techniques. A short-cut to suppress or greatly reduce morphological responses to FR is by transgenic overexpression of phytochrome A (McCormac et al., 1992). The overexpressed phytochrome A somehow interferes with normal R:FR perception by other members of the phytochrome family, resulting in plants that do not respond to FR with increased elongation, or that even display inhibition of elongation in response to FR (McCormac et al., 1992; Ballare et al., 1994; Casal and SaÂnchez, 1994). Partial support for the hypothesis that reduced photomorphogenic plasticity is an advantage in crop plants has been provided by eld experiments with tobacco plants (Robson et al., 1996). In those experiments, ectopic overexpression of a PHYA cdna resulted in plants that lacked normal elongation responses to increased canopy density; at high densities, the phytochrome A overexpressors presented larger harvest indexes (leaf:stem dry weight ratio) than the wild type, which displayed normal morphological responses to crowding. Unfortunately, absolute data on leaf yield were not reported in that study. Experiments with other species suggest that the partitioning bene ts that can be obtained by suppressing morphological responses to FR can be small if any (Ballare et al., 1991c; Yanovsky et al., 1995b). Moreover, scenarios in which an increased sensitivity to FR may entail partitioning bene ts have been described (e.g., by suppressing unproductive tillering in cereals;

9 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149± Casal, 1988; Ballare et al., 1997). Clearly, a larger number of studies, involving eld experiments with different species and agronomic conditions, will be necessary to evaluate the bene ts of this technology. Thiele et al. (1999) investigated the effects of phytochrome B overexpression in potato. They found that plants expressing an Arabidopsis PHYB cdna under the CaMV 35S promoter had higher rates of photosynthesis per unit leaf area than wild type plants and a ``light-exaggerated'' phenotype characterized by semidwar sm, increased apical dominance, smaller and thicker leaves, and increased anthocyanin levels. Experiments carried out with potted plants in a greenhouse revealed that phytochrome B overexpression retarded leaf senescence and increased tuber yield (g/plant) in plants harvested when the aerial parts were totally senescent. The increased tuber yield per plant was accompanied by a decreased weight of individual tubers, indicating that a decreased apical dominance imposed by high phytochrome B levels also led to increased stolon formation. A problem that can arise with crop plants that are impaired in their capacity to perceive photomorphogenic signals of crowding (e.g., phytochrome A overexpressors) is that they will inevitably have a reduced ability to ``forage'' for light (see Ballare et al., 1997; BallareÂ, 1999). This can result in delayed soil cover (Ballare et al., 1995a), and increased size inequality among individual crop plants (Ballare et al., 1994, 1997), with negative consequences on crop yield (Hedley and Ambrose, 1981; Ballare and Scopel, 1997). A re nement of the overexpression technology consists of directing the overexpression of the foreign photoreceptor genes to speci c tissues or organs by using appropriate promoters (Ballare et al., 1995a). In principle this approach could be used to make particular organs blind to certain proximity signals (such as the increase in re ected FR) without compromising the general photomorphogenic competence of the plant. Rousseaux et al. (1997) analyzed the responses to localized applications of FR of tobacco plants that overexpressed phytochrome A under various promoters. They found that plants that expressed a PHYA cdna from oat under a CAB promoter presented very high levels of total phytochrome A in the leaves, but displayed relatively low PHYA expression in the stem tissue. In these plants, FR applied to the leaves failed to elicit the senescence responses that were observed in the wild type counterparts (such as reduced speci c leaf mass, nitrate reductase activity or chlorophyll content); however, the CAB:PHYA plants presented signi cant elongation responses to FR treatments applied to the internodes. These results demonstrate that it is feasible to molecularly mask particular organs to FR by targeting the overexpression of a PHYA construct. This approach might be used, for example, to suppress or reduce ower or fruit abortion responses that are triggered locally by the light climate experienced by individual reproductive structures (Heindl and Brun, 1983). Modi cations of crop plant photomorphogenesis using transgenic technology are also likely to have an impact on the competitive relationships between weeds and crops. The incorporation of a reduced photomorphogenic plasticity is predicted to negatively affect the ability of the crops to compete with weeds for light, particularly when the weeds are closely related to the crop and have similar phenology and morphology. For example Schmitt et al. (1995) showed that transgenic tobacco plants that overexpressed phytochrome A and had reduced elongation responses to low R:FR were suppressed in the competition with the wild type in high density stands. In contrast, in situations where the crop plants have a large initial advantage over the weeds (e.g., because of an earlier emergence or a much larger initial size), a genotype that partitions most of its assimilates to lateral expansion (as it is the case with phytochrome A overexpressors in tobacco) might be advantageous for suppressing small weeds seedlings (Dr. J. Weiner, Royal Veterinary & Agricultural University, Frederiksberg, Denmark; pers. comm., 1999). Clearly competition with weeds needs to be taken into consideration when designing new crops with altered photomorphogenesis, and these considerations need to involve issues such as the growth architecture and morphological plasticity of the weeds, as well as agronomic variables such as planting density and patterns. There seems to be considerable potential for interdisciplinary research in this area, which has hardly been explored. 4. Future perspectives Light signals perceived by speci c photoreceptor systems control the morphology, temporal develop-

10 158 C.L. BallareÂ, J.J. Casal / Field Crops Research 67 (2000) 149±160 ment and partitioning patterns of crops and weeds. All these processes have enormous importance in de ning the outcome of competition for light in crop stands. The availability of biotechnological tools to alter features of the photomorphogenesis of cultivated plants provides an unprecedented opportunity to study the role of particular photomorphogenic signals and photoreceptor systems in the processes of intra- and interspeci c competition. In addition, these tools can be used to investigate broader issues of crop ecophysiology, such as the impact of manipulating assimilate allocation, fruit abortion, leaf area duration, apical dominance and shoot architecture. The application of these new tools to address classical physiological problems calls for collaborative research. In order to be effective, this research should be based on eld experiments using real crop canopies. Studies with individual plants in pot experiments are an important rst step, but the results of these studies cannot be directly scaled up to predict the impacts of photomorphogenic manipulations at the crop level. Acknowledgements We thank Drs. Rodolfo SaÂnchez and Ana Scopel for useful discussions over many years. The work in our laboratories is supported by grants from the Consejo Nacional de Investigaciones CientõÂ cas y TeÂcnicas ``CONICET'' and the Agencia Nacional de PromocioÂn CientõÂ ca y TecnoloÂgica ``ANPCyT'' (C.L.B. and J.C.C) and the Universidad de Buenos Aires (J.J.C.). References Ascard, J., Soil cultivation in darkness reduced weed emergence. Acta Hort. 372, 167±177. BallareÂ, C.L., Keeping up with the neighbours. Phytochrome sensing and other signalling mechanisms. Trends Plant Sci. 4, 97±102. BallareÂ, C.L., Scopel, A.L., Phytochrome signaling in plant canopies. Testing its population-level consequences using photoreceptor mutants of Arabidopsis. Funct. 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