Regulatory Components of Shade Avoidance Syndrome
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
References (143)
- et al.
The true story of the HD-Zip family
Trends Plant Sci.
(2007) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms
Trends Plant Sci.
(1999)- et al.
Light signaling: back to space
Trends Plant Sci.
(2008) - et al.
Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks
Trends Plant Sci.
(2007) - et al.
JAZ repressors set the rhythm in jasmonate signaling
Curr. Opin. Plant Biol.
(2008) - et al.
The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1
Curr. Biol.
(2004) - et al.
High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4
Curr. Biol.
(2009) - et al.
Molecular players regulating the jasmonate signalling network
Curr. Opin. Plant Biol.
(2005) Circadian clock function in Arabidopsis thaliana: time beyond transcription
Trends Cell Biol.
(2008)- et al.
Light and shade in the photocontrol of arabidopsis growth
Trends Plant Sci.
(2002)
Light-regulated nuclear localization of phytochromes
Curr. Opin. Plant Biol.
Dawning of a new era: photomorphogenesis as an integrated molecular network
Curr. Opin. Plant Biol.
Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses
Cell
PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein
Cell
Releasing the brakes of plant growth: how GAs shutdown DELLA proteins
J. Exp. Bot.
Mechanistic duality of transcription factor function in phytochrome signaling
Proc. Natl. Acad. Sci. U.S.A.
Decoding of light signals by plant phytochromes and their interacting proteins
Annu. Rev. Plant Biol.
Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence
Plant Cell Environ
Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings
Plant J.
Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction
Plant Cell
The role of GRAS proteins in plant signal transduction and development
Planta
Differential genetic variation in adaptive strategies to a common environmental signal in Arabidopsis accession: phytochrome-mediated shade avoidance
Plant Cell Environ
PAR1 and PAR2 integrate shade and hormone transcriptional networks
Plant Signal Behav.
A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 Gene of arabidopsis
Plant Physiol
Both phyA and phyB mediate light-imposed repression of PHYA gene expression in Arabidopsis
Plant Physiol
Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity
Genes Dev.
The Arabidopsis athb-2 and -4 genes are strongly induced by far-red-rich light
Plant J.
Persistent effects of changes in phytochrome status on internode growth in light-grown mustard: occurrence, kinetics and locus of perception
Planta
Phytochrome effects on the relationship between chlorophyll and steady-state levels of thylakoid polypeptides in light-grown tobacco
Plant Physiol
Light signal transduction in higher plants. Annu. Rev. Genet
Genetic regulation of development in sorghum bicolor: VI. The ma(3) allele results in abnormal phytochrome physiology
Plant Physiol
The JAZ family of repressors is the missing link in jasmonate signalling
Nature
The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy
Plant Mol. Biol.
A molecular framework for light and gibberellin control of cell elongation
Nature
Phytochromes differentially regulate seed germination responses to light quality and temperature cues during seed maturation
Plant Cell Environ
The rosette habit of Arabidopsis thaliana is dependent upon phytochrome action: novel phytochromes control internode elongation and flowering time
Plant J.
Phytochrome E influences internode elongation and flowering time in Arabidopsis
Plant Cell
Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time
Plant Physiol
Photophysiology of the elongated internode (ein) mutant of Brassica rapa: ein mutant lacks a detectable phytochrome B-like polypeptide
Plant Physiol
A genomic analysis of the shade avoidance response in Arabidopsis
Plant Physiol
DELLA protein function in growth responses to canopy signals
Plant J.
Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis
Plant J.
A constitutive shade-avoidance mutant implicates TIR-NBS-LRR proteins in Arabidopsis photomorphogenic development
Plant Cell
HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction
Genes Dev.
Phenotypic characterization of a photomorphogenic mutant
Plant J.
Photoreceptors in Arabidopsis thaliana: light perception, signal transduction and entrainment of the endogenous clock
Planta
Coordinated regulation of Arabidopsis thaliana development by light and gibberellins
Nature
Shade avoidance
New Phytol
Light-quality regulation of freezing tolerance in Arabidopsis thaliana
Nat. Genet.
Transgenerational plasticity is adaptive in the wild, Science
Science
Cited by (64)
Revisiting ABR editing in the period 2006–2012 and recent developments
2021, Advances in Botanical ResearchCitation Excerpt :Finally, two other aspects of environmental physiology were discussed: the first one concerns the perception of light and the syndrome of shade avoidance. Several transcription factors which modify the hormone sensitivity and growth response were described (Martinez-Garcia et al., 2010). The second one reviewed cold signaling and cold tolerance (Ruelland, Vaultier, Zachowski, & Hurry, 2009).
Crop photosynthetic response to light quality and light intensity
2021, Journal of Integrative AgricultureThe shady side of leaf development: the role of the REVOLUTA/KANADI1 module in leaf patterning and auxin-mediated growth promotion
2017, Current Opinion in Plant BiologyCitation Excerpt :This contrasts shade conditions, where the R:FR ratio is low due to far-red reflection from neighbouring vegetation. In this situation, PHYB is in its inactive state and unleashes the PIF factors to promote elongation growth [30]. The shade-induced wave of transcription is followed by a boost in auxin biosynthesis [31] that is required for elongation growth.
Molecular mechanisms of shade tolerance in plants
2023, New PhytologistSTAY-GREEN Accelerates Chlorophyll Degradation in Magnolia sinostellata under the Condition of Light Deficiency
2023, International Journal of Molecular Sciences