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REVIEW ARTICLE
I. Vanninen
1 MTT Agrifood Research Finland, Plant Production Research, Jokioinen 31600, Finland
Norway
2 Bioforsk Plantehelse, Norwegian Institute of Agricultural and Environmental Research, Hoegskoleveien 7, N-1432 As,
3 Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre Harrow, ON, Canada N0R 1G0
Keywords
Articial lighting; greenhouse crops; pest
management; plant resistance; primary
metabolites; secondary metabolites;
year-round production.
Correspondence
I. Vanninen,
MTT Agrifood Research Finland,
Plant Production Research, Jokioinen 31600,
Finland.
Email: Irene.Vanninen@mtt.
Received: 11 March 2010; revised version
accepted: 17 July 2010.
doi:10.1111/j.1744-7348.2010.00438.x
Abstract
This review describes the effects of the current and emerging lighting technologies on plants, and the plant-mediated effects on herbivorous and beneficial
arthropods in high-technology year-round greenhouse production, where light
quality, quantity and photoperiod differ from the natural environment. The
spectrum provided by the current lighting technology, high-pressure sodium
lamp (HPSL), differs considerably from that of solar radiation. The major plantmediated effects on arthropods were predicted to result from (a) extended
photoperiods and lower light integrals, (b) the attenuation of ultraviolet (UV)
wavelengths, particularly UV-B, (c) the high red: far-red (R : FR) ratio and lower
blue : red (B : R) in comparison with solar radiation and (d) the high proportion
of yellow wavelengths during winter months. Of these light factors (ad) (ceteris
paribus), (a) and (b) were hypothesised to result in increased performance of
herbivores in winter months, whereas the high R : FR ratio decreased herbivore
performance or not affected it, at least when interlights are used. The predictions obtained on the basis of this review are also discussed in relation to the
modifying factors prevailing in these production environments: enriched CO2
levels, high nutrient amounts, optimised irrigation and temperatures optimal
for plants needs. Based on the carbon/nitrogen and growth/differentiation
balance theories, these modifying factors tend to produce plants that allocate
most resources to growth at the expense of defensive secondary metabolism
and physicochemical defensive structures. At the end, this review discusses
knowledge gaps and future research prospects, in which light-emitting diodes,
the emerging lighting technology, play an important role by enabling the
targeted manipulation of plant responses to different wavelengths.
Introduction
In greenhouses, it is possible to manipulate light as
well as other environmental factors to improve plant
production and quality (Gruda, 2005). A variety of
desired functional or structural changes in crop plants,
for example increasing photosynthesis, modulating crop
morphogenesis and controlling the timing of physiological events such as induction of flowering, can be
obtained by manipulating light (Moe, 1997). Natural
Ann Appl Biol 157 (2010) 393414 2010 The Authors
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Cladding materials
Greenhouse covers change quantitatively or qualitatively
the transmission, reflection and absorption of the solar
radiation when it enters the greenhouse (Kittas & Baille,
1998). Recent developments of plastic films aimed at
manipulating the light environment include UV blocking,
near-infrared (NIR) blocking, fluorescent and ultrathermic films (Esp et al., 2006). Such films are principally used
for the benefit of the crop (Hemming-Hoffmann et al.,
2005; Magnani et al., 2008). In northern areas, transmission of the total solar wavelength band (4002500 nm)
is desirable to maximise heat influx to the greenhouse
during cooler seasons. On the other hand, in the winter low transmission of long-wave radiation (250040
000 nm) is desirable to reduce heat loss from the greenhouse (Pearson et al., 1995). For combined plant growth
and energy-saving purposes, the challenge is to develop
cover materials that combine high light transmission and
high insulation values (Bakker, 2008). Examples of such
materials are antireflex glass (Hemming-Hoffmann et al.,
2006), triple layer systems (Bot et al., 2005), Lexan ZigZagTM greenhouse roof (Sonneveld & Swinkels, 2005a) and
micro-V-treated glass (Sonneveld & Swinkels, 2005b).
Incoming light transmission and light quality can also
be modulated by using films containing photoselective
pigments (for a review, see Esp et al., 2006). For example,
blue fluorescent film was developed to increase light
transmission as well as to increase the blue range of
the spectrum for transmitted light in northern European
climates (Hemming-Hoffmann et al., 2005).
FR 700-800
NIR 800-3000
Photosynthetically Active Radiation
(PAR)
Chls /carotenoids
Chls
Pr and Pfr
250 300 350 400 450 500 550 600 650 700 750 800
Wavelength (nm)
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Table 1 Effects of different light wavelengths on plant physiology and morphology because of differential sensitivity of photoreceptorsa
Light Quality
The effects can be separated by UV-B dosage. Low doses induce UV-B-specic
photomorphogenetic and developmental responses. High doses result in more general
stress signal transduction.b
Tends to temper or negate the effects of blue and red.g Downregulates genes coding for
key enzymes in the Calvin cycle.e In moderate and strong intensities of white light, after
chlorophyll absorbance for red and blue light have become saturated, green light drives
photosynthesis more efciently than blue or red due to differences in light-absorption
proles within leaves for blue, red and green light.h
Downregulates genes coding for key enzymes in the Calvin cycle.e Suppresses growth of
some greenhouse plants.i
Often cancels the effects of preceding red light. In many species, inhibits seed
germination.m Stem elongation (de-etiolation).j
Crucial for photosynthetic activity.m
R : FR
plants by limiting photowhereas high light intenthe photosynthesis appaTo give a perspective, the
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Intensity
LIGHT
Photoperiod
Wavelength
Photosynthesis1,2
C/N ratio1
VOC emission3,4
Trichome density5
Stomatal density6
Leaf toughness1
Secondary metabolites (+/-)1
(extrafloral) Nectar production7
Physico-chemical leaf cuticle
properties8
Flowering
VOC emission10
Leaf injury (tomato)11
Nutrient uptake12
Leaf toughness13
Secondary metabolites23
Photosynthesis14
N content 15
Morphology16,17
Leaf thickness14
Stomatal control14
Phototropism18
VOC emission19
Secondary metabolites20
Quality and quantity of
cuticle wax14
Trichome density16
Growth21
Survival22
Foraging5
Oviposition1
Population
Densities21
Feeding1,21,22
Figure 2 Effects of light intensity, photoperiod and quality (wavelength) on plants and via plants on arthropods. References: 1, Roberts & Paul (2006); 2,
Gruda (2005); 3, Gouinguene & Turlings (2002); 4, Takabayashi et al. (1994); 5, Kennedy (2003); 6, Gay & Hurd (1975); 7, Pacini et al. (2003); 8, Shepherd
et al. (1995); 9, Stack & Drummond (1997); 10, Maeda et al. (2000); 11, Hillman (1956); 12, Mankin & Fynn (1996); 13, Dorais (2003); 14, Teramura &
Sullivan (1994); 15, Lindroth et al. (2000); 16, Jansen (2002); 17, Kakani et al. (2003); 18, Pinho (2008); 19, Kasperbauer & Loughrin (2004); 20, Treutter
(2006); 21, Mazza et al. (1999); 22, Zavala et al. (2001); 23, Kennedy et al. (1981).
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andez
et al.,
2006). The authors proposed that the insects responded
to the decreased emission of VOCs, which indicates lower
attraction of natural enemies to the plants.
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2009a). Furthermore,
UV-B light induces, for example, phenolics that are
not induced by herbivory (Izaguirre et al., 2007). Plant
responses can be dependent not only on plant species and
specific metabolites but also on plant growth stage and leaf
age (Tegelberg et al., 2004), type of herbivory and length
of UV-B light pretreatment periods of seedlings, as shown
in Broccoli for phloem-content and cell-content feeders
(Kuhlmann & Muller,
2009b).
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Narrow-bandwidth lighting
Available studies on the effect of specific wavelengths on
plants show that the photosynthesis, photomorphogenesis, germination, flowering, accumulation of biomass
and the phytochemical composition of crops can be
controlled and optimised by utilising supplemental lighting provided by LEDs (reviewed by Massa et al., 2008;
Pinho, 2008, Yeh & Chung, 2009). Higher photosynthetic pigment content and photosynthetic activity of
LED-illuminated plants have been observed in some, but
not all, experiments (for reviews, see Massa et al., 2008;
Pinho, 2008); the effect depends also greatly on which
wavelengths are used (Wang et al., 2009). The use of
specific wavelengths can result in altered relative contents of sugar types in leaves (Pinho 2008; Brazaityte
et al., 2009a; Urbonaviciut
e et al., 2009), changes in the
activity of nitrate reductase and, consequently, nitrate
contents of leaves (Pinho, 2008), and increased greenness
(amount of chlorophyll) of fruits (Lin & Jolliffe, 1996).
Such changes may also have importance for herbivory,
as primary metabolites affect the nutritive value of the
plant material for insects (Schoonhoven et al., 2006), and
induced changes in primary metabolism could themselves
be defensive (Schwachtje & Baldwin, 2008).
Studies in Lithuania have looked at the effects of
blue, red and far red LEDs in combination with supplemental UV-A, green, yellow and orange wavelengths.
Yellow (596 nm) decreased cucumber transplant development and growth (Brazaityte et al., 2009a), and tomatoes receiving yellow (596 nm) or orange (622 nm)
during transplant stage had lower yield in the greenhouse (Brazaityte et al., 2009b). In the study of Wang
et al. (2009), monochromatic green (522.5 nm), yellow
(594.4 nm) and red (628.6 nm) affected all measured
photosynthetic parameters of young cucumber plants
negatively in comparison with white light, whereas
purple and blue had positive impacts. Based on gene
expression studies, the authors concluded that purple and
blue light upregulate most of the genes that encode key
enzymes in the Calvin cycle, whereas green, yellow and
red downregulate them. In lettuce, adding supplemental
yellow (594 nm) to the light spectrum consisting of natural daylight and supplemental monochromatic blue and
red components increased the number of leaves (Pinho,
2008), whereas Dougher & Bugbee (2001) traced the
suppressed growth of lettuce plants under HPSLs as compared to metal halide lamps to the negative effect of
yellow (580600 nm). The discrepancies concerning the
effect of green and yellow wavelengths on plant growth
are an example of how the effects of certain monochromatic light treatments on photosynthetic processes are
only being revealed, whereas the mechanisms behind the
effects are less well known.
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Other changes attributed to the effects of NBL concern antioxidant activity, phenolics, vitamins, flavonoids,
anthocyanins, tannins, and other secondary metabolite
contents that either increase or decrease depending on
the wavelength selection, ratio of different wavelengths
such as UV-B, blue, yellow and R : FR (see Tegelberg
et al., 2004; Wu et al., 2007; Urbonaviciut
e et al., 2009).
The role of such NBL-induced changes for herbivores and
their natural enemies has not been studied so far. The first
challenge is in designing an optimum plant lighting system with wavelengths essential for specific crops (Massa
et al., 2008). Once this problem has been solved and plant
composition can be reliably influenced by the spectral
composition of artificial light sources, the consequences
of NBL-induced secondary metabolites for herbivory are
easier to investigate. The study by Hong et al. (2009)
shows one way of advancing such understanding. The
authors engineered a transgenic Artemisia annua to overexpress the blue light photoreceptor cryptochrome 1
obtained from Arabidopsis. As a result, the engineered
plants increased the production of a valuable antimicrobial secondary metabolite, artemisin, by 3040%.
Light also affects the synthesis and emission of VOCs
by plants (Penuelas
& Llusia,
` 2001) and light quality
seems to contribute to determining the VOC profile as
shown in VOCs emitted by cotton plants grown over
different colour mulches of polyethylene (Kasperbauer &
Loughrin, 2004). Plants that received mulch-reflected
light with reduced R : FR ratio in comparison with
ambient sunlight emitted more insect-attracting volatile
monoterpenoids. The quantity and composition of the
plant VOC blends are important for host location of
herbivores as well as for host/prey location of natural
enemies (Schoonhoven et al., 2006).
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Table 2 Predictions for plant-mediated effects of articial light based on high-pressure sodium lamps (HPSLs) in year-round greenhouse cropsa
Characteristics of Articial Lighting
Extended photoperiods
Attenuated/absent
UV-B
Attenuated blue
High yellow
LED, light-emitting diode; R : FR, red: far-red ratio; UV, ultraviolet; VOC, volatile organic compound.
a The predictions are for individual light-related factors. The relative strength of the predicted effects must be considered with respect to the modulating
factors of enhanced CO2 , high amount of nutrients and water as well as the temperature, which is adjusted to the plants needs and light and CO2 levels.
The combined effect of the individual light-related factors is less easy to predict and deserves investigation. The predictions concerning effects of specic
wavelengths and their combinations can be extended to light environments created by narrow-bandwidth LED lights.
b Based on the reviewed literature.
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Concluding remarks
High-pressure sodium lamps are the current artificial light
technology used in greenhouse at high latitudes, and fulfil
to a certain extent the plant needs. The extended photoperiods used during winter months with the characteristic
light spectra of HPSLs may, however, result in differences
in plant resistance traits between summer and winter
crops. This consequently may lead to differences in population dynamics of pests and their natural enemies. With
this review, we intended to show that current artificial
light conditions during winter might not be the best in
terms of plant protection. Deepening the knowledge of
effects of light on the secondary metabolism of plants and
the plant-mediated effects of light on arthropods could
408
improve greenhouse artificial lighting conditions to harmonise crop yield and quality with herbivores and natural
enemy populations, particularly during winter months.
Besides, increased knowledge in this research area will
make us better prepared to evaluate the possible effects
of future lighting technologies on plant protection.
Acknowledgements
We thank Yrjo and Maija Rikalas horticultural foundation and the Horticultural foundation of the Finnish
Greenhouse Growers Association for financial support
for this study. Our thanks are also to Mike Bourget and
Bob Morrow, Orbitec Inc., USA, for clarifying us some
newest developments of LED lighting. We are grateful to
Prof Paula Elomaa at the Department of Applied Biology,
University of Helsinki, for reading and commenting on
an earlier version of the manuscript. Last, our thanks are
to two anonymous reviewers whose comments greatly
improved the manuscript.
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