Plants detect different characteristics of the complex light signal, such as the quantity (intensity or amount of photons), quality (colour or wavelength of the photons), periodicity (relative duration of the light period in a day which changes throughout the year in many regions of the earth) and direction. Light quantity seems to be a major signal for shade tolerance (Smith, 1982). In shade avoidance, by contrast, both light quantity and light quality are important. The combination of these two aspects of the incoming light, in varying proportions depending on the location of the plant, determines the spectrum received. However, the modification of only one of these two aspects of the light environment can induce responses to avoid shade. For example, a plant that is not initially shaded can detect the proximity of other individuals by a specific alteration in light quality. The plant then initiates a set of responses, known as the shade avoidance syndrome (SAS), intended to overgrow neighbouring competitors and/or to adapt to the eventual shading. If despite these adaptive responses the neighbour individuals overgrow and shade the plant, light quantity becomes limiting, that is, there is a reduction in the amount of radiation active for the photosynthesis, resulting in additional SAS responses. This distinction is important because responses to neighbouring vegetation take place before a plant is actually covered by a plant canopy. In addition, the two components altered by the presence of plant canopies (i.e. light quantity and light quality), are controlled by different photoreceptors, phytochromes and cryptochromes (see Sections II and IV), and consequently the molecular mechanisms involved might be different (Franklin, 2008; Pierik et al., 2009). The recognition of these two major components is therefore important and hence some caution should be used when making comparisons between the results obtained with different experimental light treatments.
In this review, we refer to SAS as the plant responses to the proximity of neighbouring vegetation, i.e. those taking place exclusively by changes in light quality. In that way, perception of an environmental signal indicative of plant proximity induces SAS responses that allow the plant to anticipate the shading, avoiding it by overgrowing neighbouring plants or by flowering to ensure the production of viable seeds for the next generation. Indeed, responding plants grow away from neighbours well before those neighbours diminish their actual interception of light. As we will see in the following section, this anticipation is accomplished by responding to a cue that is an excellent indicator not only of plant proximity (neighbour presence) but also of the shade provided by the vegetation canopy (Smith, 1982).
The anticipation of future environmental conditions seems to be a quite extended behaviour in the plant kingdom. Such behaviours do not involve true cognition but define rapid morphological or physiological responses to events, relative to the lifetime of an individual (Karban, 2008). Many deciduous plants living in temperate areas drop leaves in autumn in response to shortening photoperiod as if they were anticipating to cold conditions (normally associated with winter) that have a high probability of damaging leaves and branches and are sub-optimal for photosynthesis (Franklin and Whitelam, 2007). However, in warmer latitudes such as those found in the semiarid conditions of the Mediterranean climate, a shortening photoperiod might be indicative of the proximity of the rainy season, when water and temperature are appropriate for plant growth. Therefore, although the so-called long day plants, such as Arabidopsis thaliana or some varieties of tobacco (Nicotiana tabacum), flower in response to lengthening photoperiod associated with the spring, short day plants, such as rice (Oryza sativa), Japanese morning glory (Pharbitis nil) or Kalanchoe, flower in response to shortening photoperiods associated with autumn (Kobayashi and Weigel, 2007). In addition, the responses evoked by the photoperiodic signal may change with the species. For example, tuberization in all potato species (Solanum tuberosum) is affected by photoperiod, but short day conditions are a strict requirement for tuber formation in only some of them (Jackson, 1999; Martinez-Garcia et al., 2001). Similarly, in shade-avoiding plants, the response to plant proximity might vary with the species and the stage of development (see Section V).
The mechanisms of the anticipatory responses to plant proximity, i.e. the SAS, will be covered in this review, focusing in the signal itself, the phytochrome photoreceptors involved in the perception of this signal and, finally, the molecular mechanisms behind these complex responses. Specifically, we will pay attention to the components with a role in regulating SAS responses mainly based on the analyses of the response of Arabidopsis hypocotyls and their participation in the complex transcriptional networks that mediate this process.
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