Regulatory Components of Shade Avoidance Syndrome

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Abstract

Competition for light has an important impact on plant development. Plants sense the presence of nearby competitor vegetation as a change in the light quality, i.e. a reduced red to far-red ratio. The responses to shade are generally referred to as the shade avoidance syndrome (SAS), and involve various developmental changes aimed to outgrow the neighbouring plants, and are characterized by enhanced elongation, reduced leaf expansion, decreased branching and ultimately early flowering. These responses can be detrimental in agriculture, because they induce reallocation of resources into elongation growth at the expense of harvestable organs, hence lowering the crop yield. Genetic analyses performed on the SAS response of seedlings have shown the involvement of several transcription factors in the regulation of this response. At least in a few cases, it has been shown that phytochrome rapidly regulates the expression levels of several modulators of hormone responsiveness, rapidly linking shade perception, massive changes in gene expression and modification of hormone sensitivity of the responsive tissues. Here we develop our view on how shade-modulated changes in the transcriptional profiles result in complex SAS responses.

Introduction

In both natural and agricultural plant communities, resources are frequently limited, and competition between individuals often results in plastic developmental responses for adaptation to the specific resource shortage. Light is probably amongst the most important resources for plant growth and limitations in its supply compromise survival and growth. As a consequence, evolution has shaped plant mechanisms and strategies to maximize light acquisition and modify the patterns of development to reconcile their sessile nature with the variability in the environmental light supply. In natural conditions, one of the situations in which light might become limited is under high density, such as those found in forests and prairies, where a mixture of different species growing in dense conditions might eventually result in shading and, therefore, in a shortage of solar energy for photosynthesis.

In a situation of light shortage, plants have evolved to either tolerate or avoid shading caused by nearby competitors. Shade tolerance is a concept that refers to the capacity of a given plant to tolerate low light levels. From a physiological point of view, shade tolerance of a given plant is defined as the minimum light quantity (see Section III) under which a plant can survive (Valladares and Niinemets, 2008). But from a biological point of view, to define a species as shade tolerant, the whole life cycle of the plant from early survival and growth to reproduction must be considered. Thus, although many plants can tolerate low-intensity light conditions, only a fraction of them can reproduce under these conditions. These include the elephant ear (Alocasia macrorrhiza) (Kirschbaum et al., 1988, Noguchi et al., 1996), holly (Ilex aquifolium L.) (Valladares et al., 2005), impatiens (Impatiens balsamina), and several coleus (Solenostemon scutellarioidies) and Fuchsia cultivars (http://www.extension.umn.edu/distribution/horticulture/DG8464.html). Shade tolerance is a complex property of plants that is achieved by different sets of responses in different species, such as alterations in leaf physiology and biochemistry, leaf anatomy and morphology and/or plant architecture. In general, under low light, shade tolerants tend to adapt to a highly conservative utilization of resources, commonly accompanied by very low growth rates and by structural and biochemical changes intended to enhance the efficiency of photosynthetic energy transduction and to reduce respiration losses (Smith, 1982, Valladares and Niinemets, 2008). Morphologically, growth of shade-tolerant species under low light conditions typically results in thinner leaves, reduced apical dominance, high branching frequency and low elongation response. In addition, plants accumulate higher chlorophyll content per leaf area or leaf dry mass (Valladares and Niinemets, 2008). By contrast, shade-avoiding species growing under ‘shade’(see Section V) generally tend to adapt their development to favour internode extension at the expense of leaf development, and to increase apical dominance (which reduces branching frequency), allowing the young leaves to escape from shade.

Section snippets

The Shade Avoidance Syndrome: A Set of Responses to Anticipate to Plant Canopy Shade

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

The Low Red to Far Red Ratio Light: A Reliable Signal of Plant Proximity

The radiation coming from the sun is called daylight (Smith, 1982). In open conditions, i.e. when a plant grows under low plant density and there is no or little vegetation in the vicinity, the daylight spectrum is relatively constant (Fig. 1) (Franklin, 2008, Smith, 1982, Vandenbussche et al., 2005). The range of light we will discuss in here includes the spectrum visible for the human eye (from ∼400 nm, blue light, to 700 nm, red light, R) and the far-red (FR) region (from 700 up to 800 nm).

Photoreceptors Involved in the Regulation of SAS: The Phytochromes

In a signalling pathway, the stimulus is perceived by a receptor and transduced by various intermediate molecules to achieve the final responses. In the case of the SAS, the receptors are the R and FR light-absorbing phytochromes, which initiate the signalling cascade when they perceive a reduced R:FR signal. The phytochrome photoreceptors exist in two photoconvertible forms, the Pr and Pfr. Phytochromes are synthesized in the cytoplasm in the inactive R-absorbing Pr form (λmax of absorbance at

How and When: SAS Responses in Different Organs and Developmental Stages

To experimentally distinguish between effects of light quantity and light quality, each factor should be modified independently in the laboratory. Therefore, to study exclusively the effect of light quality, i.e. to compare the effect of high and low R:FR light on a specific response, both light conditions have to provide the same irradiation in the region of the spectrum that provides the PAR (400–700 nm). One accepted approach is to use light generated from fluorescent tubes that provides

Molecular Mechanisms in SAS Signalling

Variation in hypocotyl elongation and flowering time in response to low R:FR in over 100 Arabidopsis ecotypes showed wide variation in the extent of these responses between ecotypes, but little correlation between variation in flowering and elongation. For example, several ecotypes displayed greatly attenuated early flowering responses to the simulated shade signal, but exhibited pronounced hypocotyl elongation (Botto and Smith, 2002). This lack of correlation suggested the existence of

Cross Talk of SAS Signalling With Other Regulatory Pathways

Since many factors besides SAS signalling regulate seedling responses modulated by simulated shade (i.e. hypocotyl elongation, and cotyledon and primary leaf expansion), it is expected that at least some of these different signalling pathways leading to growth stimulation or repression converge, providing a means to integrate light and other environment information with endogenous developmental programmes, such as those controlled by the circadian clock, temperature and phytohormones.

Spatial and Temporal Aspects of the SAS Signalling

Much of our understanding of the molecular components involved in the regulation of the SAS comes mainly from the analyses of whole seedling responses in Arabidopsis. However, models describing the action of phytochromes, its interacting partners and their effect on gene expression are usually restricted to single cells. Although the obvious fact that these regulatory and/or transcriptional networks are in the multicellular context of a plant (where not all the cells are expressing the same

Concluding Remarks: From Master Genes to Regulatory Modules of the SAS Responses

A recurrent goal in the field is to identify what genes are actual master regulators of the SAS morphological responses. For this purpose, functional analyses of some of the hundreds of PAR genes described by different laboratories (Devlin et al., 2003, Franklin and Whitelam, 2007, Salter et al., 2003, Tao et al., 2008) has been an ongoing strategy (summarized in Table I). With this goal in mind, HFR1 was reported as a master regulator of SAS (Sessa et al., 2005). However, its master (central)

Acknowledgements

The authors thank M. Rodríguez-Concepción for his comments on the manuscript. Financial support of JB-T and MS-M came from the CSIC (JAEdoc and JAEpre Programmes, respectively). AG and MG received predoctoral fellowships from FPU and FPI programmes, respectively, of the Spanish Ministry of Science and Innovation (MICINN). NC-E received a predoctoral fellowship from the Gobierno de Chile. Our research is supported by grants from the Generalitat de Catalunya (Xarxa de Referència en Biotecnologia

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