Seduced by the dark side: integrating molecular and ecological perspectives on the
influence of light on plant defence against pests and pathogens.
Michael R. Roberts* and Nigel D. Paul,
Department of Biological Sciences,
Lancaster Environment Centre,
Lancaster University,
Lancaster,
LA1 4YQ
UK.
*Author for correspondence:
Michael Roberts
Tel:
00 44 1524 510210
Fax:
00 44 1524 593192
e-mail:
m.r.roberts@lancaster.ac.uk
Contents
Summary
I. Introduction
II. Light as an environmental variable
III. Long term effects of light on plant-herbivore or plant-pathogen interactions
IV. Mechanisms of responses to the light environment: the whole plant perspective
V. Short-term responses to the light environment – induced defences
VI. Mechanisms for light-dependent induced defences
VII. Interpreting interactions between light and defence responses
Acknowledgements
References
1
Summary
Plants frequently suffer attack from herbivores and microbial pathogens, and have
evolved a complex array of defence mechanisms to resist defoliation and disease. These
include both preformed defences, ranging from structural features to stores of toxic
secondary metabolites, and inducible defences, which are activated only after an attack is
detected. It is well known that plant defences against pests and pathogens are commonly
affected by environmental conditions, but the mechanisms by which responses to the
biotic and abiotic environments interact are only poorly understood. In this review, we
consider the impact of light on plant defence, both in terms of plant life histories and
rapid scale molecular responses to biotic attack. We bring together evidence that
illustrates that light not only modulates defence responses via its influence on
biochemistry and plant development, but in some cases, is essential for the development
of resistance. We suggest that the interaction between the light environment and plant
defence is multifaceted, and extends across different temporal and biological scales.
Key words:
Light, defence, resistance, tolerance, pathogen, herbivore.
Abbreviations:
CBDC – carbon-based defensive chemicals; CHS – chalcone synthase; CNB – carbon nutrient
balance; GDB – growth differentiation balance; HR – hypersensitive response; PAL –
phenylalanine ammonia lyase; PAR – photosynthetically active radiation; PET – photosytnthetic
electron transport; PR – pathogenesis-related; ROS – reactive oxygen species.
2
I. Introduction
Light is fundamental to the existence of plants. It affects all aspects of growth and
development, since a primary requirement for plant fitness is to optimise light harvesting
for photoautotrophic growth. Hence, photoreceptors such as phytochromes and
cryptochromes sense quantitative and qualitative features of the light environment and,
via associated signal transduction pathways, regulate plant physiology and development.
Light, through photosynthesis, also controls much of the biochemical activity within plant
tissues, something that is reflected by the fact that a wide array of genes are
transcriptionally regulated by the circadian clock in Arabidopsis thaliana (Harmer et al.,
2000). By sensing day length, plants also use light as a seasonal indicator which controls
the transition to reproductive growth in many plant species. Although essential, light can
also pose problems for plants. Increased doses of UV light can cause damage at the
molecular level, and even simple changes in ambient sunlight can over-load
photosynthetic electron transport (PET), causing damaging reactive oxygen species
(ROS) to accumulate. Plants have evolved many systems to minimise the impacts of such
deleterious effects of light, including the production of photoprotective pigments,
biochemical systems to rapidly modulate chloroplast electron transport, physiological
responses such as the ability to re-orient chloroplasts, and photomorphogenic responses
that optimise the interaction of the leaves with light over longer time scales.
As well as direct effects on plant metabolism, growth and development, light inevitably
influences many other plant responses to the environment. These include defences against
pests and pathogens. There is a wide range of information in the scientific literature on
3
the effects of light on defence responses, ranging from ecological to molecular scale
investigations of both short and long term responses. Our aim here is to draw some
general conclusions on the impact of light on plant defence, and to attempt to suggest
conceptual models that explain the observations in terms of both the molecular and
ecophysiological responses to light and biotic attack.
II. Light as an environmental variable
Light is an extremely dynamic component of the terrestrial environment. Changes are
both quantitative (including variation in instantaneous irradiance, dose accumulated over
time, and day length) and qualitative (in terms of light spectral balance). Plants and their
associated herbivores and pathogens may respond to each of these different components
of variation.
1. Variation in the quantity of light.
The quantity of light falling on a surface at a given moment, usually referred to as “light
intensity,” is formally defined in terms of either energy per unit area (= irradiance) or
quanta per unit area (= photon flux: see Bjorn, 2002). Some elements of the variation in
irradiance are predictable, for example variation with time of day, season and latitude are
all functions of the elevation of the sun in the sky (the higher the solar elevation, the
higher the irradiance). As a result, irradiance reaches a maximum near the equator, at
mid-day, and, at mid-high latitudes, in mid-summer. Superimposed on these systematic
geographical and seasonal variations in irradiance are variations due to factors like cloud
cover, aspect on a sloping site, or shade from nearby structures or plant canopies (Fitter &
4
Hay, 2002). Some of these factors affect all wavelengths of light more or less equally,
others are much more wavelength specific (see below).
Many biological responses to light can be described as simple functions of irradiance.
The rate of photosynthesis in plants is a typical example. Although photosynthesis is a
function of irradiance, growth is determined by the sum of photosynthetic carbon fixation
over time which is, in turn, a function of the amount of light received by the plant over
that period. Thus, growth and yield, and many other long-term effects of light, are best
described by the accumulated dose of photosynthetic radiation, for example by daily light
integral (Kitaya et al., 1998; Korczynski et al., 2002; Dielen et al., 2004). Light damage
is also often a function of accumulated dose, as with many whole-plant responses to UV
radiation (Gonzalez et al., 1998; de la Rosa et al., 2001).
2. Variation in the quality of light
Light quality is the balance between different wavelengths. Different organisms perceive
different wavelengths in different ways. The three primary colours of human vision
define “visible” light (approx. 400-700 nm), but other animals, including many
invertebrate and some vertebrate herbivores, may perceive different wavebands, notably
in the ultraviolet region (primarily UV-A: 315-400 nm). Thus, what is actually perceived
as “visible light” varies substantially between species. Photosynthetically active radiation
(PAR) is usually defined as 400-700 nm, but plants also detect and utilise different
wavelengths as environmental cues. Responses to red and far red (detected by
phytochromes), blue and UV-A (detected by cryptochromes, phototropins and related
5
photoreceptors) are well defined (Gyula et al., 2003; Spalding & Folta, 2005). The
mechanistic basis for responses to UV-B (290-315m) remains poorly defined: some may
be a function of damage to DNA and other biological molecules, but there is also
evidence for a specific UV-B photoreceptor (Jenkins et al., 2001).
The spectral balance of sunlight in the field is influenced by a range of factors. Temporal
changes in the ratio of UV to longer wavelengths are largely driven by the increase in the
ratio at high solar elevations. At temperate and high latitudes sunlight is relatively
enriched in UV, especially UV-B, in summer compared with winter. Similarly, the ratio
of UV to PAR is highest near noon. There is some enrichment of far-red relative to red at
twilight (Salisbury, 1981). Spatially, UV:PAR ratios are typically higher at low latitudes.
Cloud typically reduces all wavelengths of sunlight but shorter wavelength UV less than
PAR, resulting in some increase in UV:PAR ratio under cloud conditions (Calbo et al.,
2005). Shade from plant canopies has major effects on spectral balance, notably in terms
of R:FR (Ballare, 1999; Gyula et al., 2003; Vandenbussche et al., 2005), but also the ratio
of UV:PAR (Grant & Heisler, 2001; Heisler et al., 2003; Grant et al., 2005).
III. Long term effects of light on plant-herbivore or plant-pathogen interactions
Studies of the effects of both shade and diurnal variation in light on plant interactions
with their natural enemies deal mostly with herbivores; effects on disease remain
relatively poorly known. Studies of herbivory (Table 1) have mostly been in the context
of variation in the light environment due to plant canopies, such as the effect of position
relative to neighbours, including gaps in woodland canopies, or woodland edge
6
(individuals within gaps or at the forest edge receiving more sunlight than those within).
Studies of woody plants have also considered the influence of vertical position in the
canopy (foliage at or near the top of the canopy receiving greater insolation than that low
down in the canopy), and the direction in which foliage faces (in the northern
hemisphere, south facing foliage receives higher irradiances than north-facing).
Experiments have either used these natural variations in light environment (for example
taking foliage from, or placing plants in, different locations) or artificially manipulated
light using shade cloth etc. (Table 1). In some cases, the latter experiments have related
to the use of shading as a tool in crop production. Of course, shading results in complex
changes in the light environment, both quantitative and qualitative, which can differ
depending on the source of shade. Thus, although some studies implicitly assume that
shade influences plant-herbivore interactions through changes in photosynthesis driven
simply by the reduction in PAR, there may be independent effects of altered spectral
balance in shade (R:FR or UV:PAR see above). Artificial shade treatments do not
necessarily reproduce these spectral changes.
In the field, shade will also influence overall radiation balance with possible
consequences for the abiotic environment of the host, the herbivore and potentially other
organisms such as parasitoids or predators of the herbivore. Temperatures of the air and
of organisms are typically lower in the shade, with direct effects on a wide range of
processes, and indirect effects such as altered water balance, which may result in reduced
plant water deficits compared with full sunlight. Equally, “shade” in the field, may alter
the biotic environment through mechanisms unrelated to any effect on solar radiation. For
7
example, there is a substantial literature on the role of tree canopies in determining the
number and species richness of the community of insectivorous birds that can have a
major influence on herbivory (Marquis & Whelan, 1994; Strong et al., 2000; Van Bael &
Brawn, 2005). Certainly the effects of tree canopies on herbivory in crops such as coffee
can be interpreted in relation to the greater predation by birds, not changes in the light
environment (Perfecto et al., 2004). Such effects highlight the complexity of shade as an
environmental variable. Clearly, many of the same arguments can be made in relation to
comparisons between day and night, which differ in far more than simply the light
environment. While these broader mechanisms are largely beyond the scope of this
review, they provide an important context for any assessment of light-mediated changes.
1. Light and herbivory
Day / night
Diurnal variation in herbivory has been viewed primarily as a function of the biology of
the herbivore rather than the host. The general expectation is that most invertebrate
herbivores are less active during the day than at night, at least partly because the risk of
predation or parasitism is greater during the day (Hassell & Southwood, 1978). However,
there are many exceptions to this pattern (Springate & Basset, 1996; VanLaerhoven et al.,
2003). For example, Novotny et al., 1999) reported a three times greater risk of predation
during day compared with night, yet herbivores were more abundant during daylight.
Some insect herbivores feed almost exclusively during the day (Kreuger & Potter, 2001),
with the temperature dependence of behaviour perhaps being a key driver. One host
characteristic that shows diurnal variation and which might influence both herbivores and
8
higher trophic levels is the emission of volatiles. There are quantitative and qualitative
differences in wound-induced volatiles between day and night (De Moraes et al., 2001;
Gouinguene & Turlings, 2002; Martin et al., 2003, and see Section V). Herbivores, and
their parasites and predators, are able to detect and respond to such changes, and diurnal
variation in the volatile signal may result in differential effects on different herbivores
(De Moraes et al., 2001) as well as on higher trophic levels (Maeda et al., 2000). On the
other hand, some predators appear capable of isolating key information against this
highly variable volatile signal (Meiners et al., 2003).
Shade
The general hypothesis that herbivory would be suppressed in plants grown in full sun
compared with those in shade has been shown to be correct in many systems, especially,
but not exclusively, with leaf chewing insects (Table 1a). This is true at least in the sense
that when consumed, leaf tissue from plants grown in shade is more favourable to
herbivore growth and/or development. However, plants grown in full sunlight may suffer
an increase in the leaf area consumed compared with shade-grown plants (Table 1a). This
increased consumption may be a function of reduced food quality in full light, since
insects often compensate for low food quality by increasing intake (Slansky & Wheeler,
1992). However, this mechanism may not fully explain increased consumption of highlight tissue, since preferences can persist even when extracts of sun or shade-grown
leaves are incorporated into artificial diets (Panzuto et al., 2001). These plant-mediated
changes interact with herbivore responses. For example, adults of some insect herbivores
may prefer high-light locations, including, for example, for egg laying (Alonso, 1997).
9
There are clear examples where such direct herbivore responses outweigh greater host
quality of shade-grown plants (Sipura & Tahvanainen, 2000). Interestingly, an example
where herbivore damage is more severe in plants grown at higher light is one of the few
examples where light-dependent variation in herbivory has been proven to have
significant effects on host population dynamics (Louda & Rodman, 1996). In that study,
the native crucifer Cardamine cordifolia suffered significantly greater herbivory when
natural shade was removed. Some components of host resistance were reduced in full
sun, but many were increased, and some of these changes appeared to be related to the
mild water deficits that occurred in plants growing in full sun. Insects were also more
abundant in the sun. Overall, changes in herbivory were attributed to the combined
effects of changes in host defence (with responses perhaps being partly to light and partly
to water deficits) and herbivore abundance (Louda & Rodman, 1996).
Although canopy shade may have slightly different effects on PAR and UV wavelengths
(Grant & Heisler, 2001; Heisler et al., 2003; Grant et al., 2005), in broad terms the two
are highly correlated across natural gradients between sun and shade. Thus, the great
majority of research into the effects of shade on herbivory will have manipulated both
PAR and UV, even though the possible role of the UV-component of sunlight is generally
ignored in interpreting results. The growing literature on the specific effects of UV
wavelengths on plant-herbivore interactions demonstrates that variation in UV, or at least
UV-B, can be significant in many systems (Table 2). Indeed, it has been suggested that
cyclical variation in the population of both vertebrate and invertebrate herbivores may be
driven by the effects of natural variation in solar UV-B on host defensive chemistry
10
(Selas et al., 2004). The experimental manipulation of UV-B alone results in changes in
plant-herbivore interactions that show many parallels with those seen with broadspectrum shading. In most studies, foliage from reduced UV-B environments is generally
found to be a higher quality resource for herbivores than foliage from unfiltered sunlight
in terms of herbivore mortality, growth rates or the efficiency of food utilisation (Table
2). In the field, defoliation due to herbivory is often increased when ambient solar UV-B
is reduced using wavelength-specific filters (Table 2). However, as with “total shade”
treatments, both laboratory and field studies show that these UV effects vary between
host species, and perhaps genotype, and also between herbivores (Table 2). The
mechanisms by which exposure to UV could directly affect insect herbivores remain
rather unclear, although the visual systems of many insects perceive longer wavelength
UV. The consequent disruption of foraging and dispersal in UV-deficient conditions can
be significant in both experimental studies (Mazza et al., 1999) and in the use of UVopaque plastics for the control of horticultural pests such as thrips and whiteflies
(reviewed by Raviv & Antignus, 2004). In the field, UV might also influence herbivore
populations through the suppression of entomopathogens, whether nematodes (Fujiie &
Yokoyama, 1998), fungi (Braga et al., 2001; Braga et al., 2002), bacteria (Myasnik et al.,
2001) or viruses (Shapiro & Domek, 2002).
The extent to which reductions in solar UV contribute to the overall effects of shade on
plant-herbivore interactions remains unclear. So far as we are aware, the only study to
explicitly consider the effects of both UV and shade is that of (Rousseaux et al., 2004)
who studied herbivory of Nothofagus antarctica. Both the number of sites attacked and
11
the area of leaf removed by insect herbivores were reduced on the sun-exposed side of the
canopy. This response occurred even when UV-opaque filters removed the UV-B
component of sunlight. However, removing UV-B significantly reduced leaf area
removed on both sun-exposed and shaded sites. This data suggests that the effects of UVB and those of other components of natural shade can act independently, a contention that
is supported by chemical changes induced (see below).
2 Light and disease
Day / night
Whilst defoliation by many herbivores is sufficiently rapid to differentiate damage
occurring during day from that at night, disease is a longer term process. Thus, it is not
surprising that, so far as we are aware, investigations of diurnal changes in plantpathogen interactions have dealt with specific aspects, such as sporulation, spore
dispersal or infection. The concentration of air-borne spores in and around plant canopies
is far higher at night than during the day in a wide range of fungi (Schmale & Bergstrom,
2004; Gilbert, 2005; Zhang et al., 2005). However, in other fungal pathogens spore
concentrations peak during the day (Gadoury et al., 1998; Su et al., 2000) or show more
complex diurnal patterns (Hock et al., 1995). These processes in plant-pathogen
interactions may be influenced by the lower temperature, higher humidity or the presence
of leaf surface water from dew occurring at night and, as with herbivory, it is not always
clear what role is played by direct effects of light. However, there is clear evidence that
spore release is initiated by light in some systems (Gadoury et al., 1998; Su et al., 2000).
Light also directly inhibits spore germination and or germ tube growth in many plant
12
pathogenic fungi (Elison et al., 1992; Joseph & Hering, 1997; Tapsoba & Wilson, 1997;
Mueller & Buck, 2003; Beyer et al., 2004), and this is certainly the case for UV (Paul,
2000). Overall, it is probably the case that plants are subject to greater challenge by many
pathogens at night than during the day, but this is certainly not the case for all pathogens.
Shade
The influence of shade on plant-pathogen interactions has been much less studied than
comparable effects on plant-herbivore interactions. However, a number of studies of noncrop systems have shown that shade increases infection by a range of pathogens (Table
1b). As with herbivory, there are exceptions to the usual expectation that disease is more
severe in the shade, as seen with coffee rust (Hemileia vastatrix) (Soto-Pinto et al., 2002),
anthracnose (Colletotrichum gloeosporioides) of Euonymus fortunei (Ningen et al., 2005)
and powdery mildew (Microsphaera alphitoides) on oak (Quercus petraea: Kelly, 2002).
For the most part, the mechanisms by which shade influences plant-pathogen interactions
remain poorly understood, although plant pathologists have often attributed the effects of
shade to factors such as humidity or leaf surface wetness, which are clearly central to the
biology of many plant pathogens (Jarosz & Levy, 1988; Meijer & Leuchtmann, 2000;
Koh et al., 2003). However, a number of studies have shown that infection by a range of
pathogens can be affected by the light environment of the host prior to inoculation. While
wheat seedlings exposed to low light intensity were more susceptible to subsequent
inoculation by Puccinia striiformis than dark-grown seedlings (de Vallavieille-Pope et
al., 2002), in other cases infection is inversely proportional to pre-inoculation irradiances
(Zhang et al., 1995; Shafia et al., 2001). This indicates direct effects of light on host
13
resistance. Furthermore, Pennypacker, 2000), showed that reduced light led to increased
infection by Sclerotinia sclerotiorum in soya bean, and Verticillium albo-atrum but not
Fusarium oxysporum in alfalfa. This was linked to host resistance mechanisms since the
effects of shade in both crops only occurred in resistant genotypes where resistance was
quantitative (requiring a large investment of resources) rather than qualitative (based on
the hypersensitive response, requiring a smaller investment of energy (Pennypacker,
2000). These conclusions parallel much thinking concerning herbivore resistance (see
below).
Light quality as well as light quantity can affect disease. Red light suppressed powdery
mildew of cucumber, and the effect appeared to be reversed by far-red (Schuerger &
Brown, 1997). There are also indications that host resistance may be induced by preinoculation exposure to red light (Islam et al., 1998; Rahman et al., 2002; Khanam et al.,
2005). Pathogenic fungi may respond directly to spectral balance, and this is exploited by
the use of plastic films which modify spectral balance as a component of disease control
in horticulture. Films which transmit more blue light than longer or shorter wavelengths
can be used to suppress sporulation in downy mildews and Botrytis cinerea (Reuveni &
Raviv, 1992, , 1997). Similarly, many plant pathogens use UV radiation as a cue to
regulate sporulation, and films opaque to UV radiation can be used to reduce a wide
range of crop diseases (reviewed by Raviv & Antignus, 2004). However, manipulating
UV has complex effects on pathosystems. While UV-A may stimulate sporulation,
exposed fungal tissues can be vulnerable to UV-B radiation, and solar UV-B is a major
constraint on the spore survival of many pathogens (Paul, 2000). The effects of reduced
14
UV-B may be sufficient to explain the overall increase in disease in shade (Gunasekera et
al., 1997) or variation in cloud cover (Paul, 2000; Wu et al., 2000). Equally, prior
exposure to UV can affect various components of host resistance. Exposure of the host
before inoculation reduced subsequent infection in a range of pathosystems, but there are
exceptions (reviewed by Gunasekera et al., 1997; Paul et al., 2000). Increases in infection
with increased UV-B have been sometimes attributed to host injury providing sites for
colonisation by necrotrophic pathogens (Manning & von Tiedemann, 1995), but it is now
recognised that this mechanism is probably confined to UV doses well above the ambient
range (Paul, 2000). Contrasting responses between pathosystems are certainly not
explained simply on the basis of biotrophic and necrotophic pathogens. Powdery mildews
(Erysiphales) are biotrophic pathogens that grow on leaf surfaces exposed to incident
radiation. There are several reports that UV-B exposure reduces powdery mildew
infections, both in the laboratory (Willocquet et al., 1996; Paul, 1997), and in the field
(Keller et al., 2003). However, exposure to increased UV-B led to increased powdery
mildew (Microsphaera alphitoides) in oak (Newsham et al., 2000), which is consistent
with the greater occurrence of this disease in open sites (Kelly, 2002). Overall, the
contribution of UV to shade effects on plant-pathogen interactions is likely to be a
function of interactions between the relative effects of UV-A and UV-B on direct damage
and spore induction in the pathogen, and host resistance mechanisms.
IV. Mechanisms of responses to the light environment: the whole plant perspective.
As discussed above, the literature on the whole plant biology or ecology of the influence
of light on plant-herbivore or plant-pathogen interactions is diverse. Responses are
15
attributed to a wide range of possible underlying mechanisms not only in the host plant,
but also light effects on the herbivore or pathogen, or higher trophic levels. Responses
may also be associated with other environmental factors correlated with the light
environment, rather than light per se. With this broad view of underlying mechanisms of
response, light-mediated changes in the host plant are viewed as just one component of
many. Furthermore, agronomists, and especially ecologists, consider a wide range of host
characteristics as being significant in determining the overall effects of light on herbivory
or disease. Chemical traits influencing herbivory include tissue nitrogen chemistry (e.g.
total N concentration, C:N ratio, protein or amino acid concentration), carbohydrate
composition (total carbohydrates or components such as the soluble fraction), or water
content. Aspects of morphology and physical properties such as leaf thickness, toughness
and the possession of thorns or spines can also be significant for plant-herbivore
interactions. In addition, the increase in specific leaf area with increasing shade that is
commonly observed across a range of species (e.g. Crotser et al., 2003; Curt et al., 2005;
Poorter et al., 2006) not only influences leaf physical properties but may also change how
herbivores respond to chemical defence by changing the relationship between chemical
contents and leaf area or biomass. Changes in host resistance, whether constitutive or
induced by attack, certainly play an important role in coupling herbivory or disease to the
light environment, but this is certainly not the only significant mechanism.
1. Host quality as a food resource for herbivores or pathogens
In a meta-analysis of studies of the effects of abiotic factors on leaf chemistry (Koricheva
et al., 1998), shade appeared to have little consistent effect on total leaf nitrogen
16
concentration or free amino acid concentration across a wide range of woody plant
systems. That analysis was explicitly limited to experimental manipulations of shading,
and subsequent studies of this type have shown that shade increases total nitrogen and/or
amino acid concentrations in some systems (Crone & Jones, 1999; Hemming & Lindroth,
1999; Moon et al., 2000; Dormann, 2003; Henriksson et al., 2003; Baraza et al., 2004;
Moran & Showler, 2005) although not in all (Louda & Rodman, 1996; Rowe & Potter,
2000). Koricheva et al., 1998) did not consider responses to natural variation in light
environment, due to position in canopy for example. Such studies frequently show
significant decreases in leaf nitrogen under shade (e.g. Fortin & Mauffette, 2001, , 2002;
Yamasaki & Kikuzawa, 2003). Research into canopy photosynthesis also shows that the
distribution of nitrogen in the canopy is in proportion to the distribution of absorbed light,
with the result that leaves in high light have high nitrogen concentration and contribute
the bulk of canopy carbon fixation (Leuning et al., 1995; dePury & Farquhar, 1997).
Exposure to UV-B often increases foliage nitrogen concentration (Hatcher & Paul, 1994;
McCloud & Berenbaum, 1999; Lindroth et al., 2000; Warren et al., 2002; Keller et al.,
2003; Milchunas et al., 2004) but has no effect in some systems (Salt et al., 1998; de la
Rosa et al., 2001; Zavala et al., 2001; Veteli et al., 2003; Zaller et al., 2003) and in others
causes decreased foliar nitrogen (Robson et al., 2003).
Koricheva et al., 1998) showed that shading of woody species had highly significant
effects on the foliar concentrations of total carbohydrates, non-structural carbohydrates,
starch and, to a lesser extent, sugars. This analysis is corroborated by more recent
research (Wainhouse et al., 1998; Hemming & Lindroth, 1999; Rowe & Potter, 2000;
17
Fortin & Mauffette, 2001; Henriksson et al., 2003) and the same response also occurs in
herbaceous species (Moran & Showler, 2005). Shade also increases leaf water content
(Louda & Rodman, 1996; Henriksson et al., 2003; Moran & Showler, 2005), which may
have a major influence on herbivore performance (Henriksson et al., 2003).
2. Mechanical defence: spines, thorns and leaf toughness.
Leaves grown under high light have greater mechanical toughness in a wide range of
species (Sagers, 1992; Dudt & Shure, 1994; Bergvinson et al., 1995; Louda & Rodman,
1996; Rowe & Potter, 1996; Henriksson et al., 2003; Martinez-Garza & Howe, 2005),
although this is not always the case (Rowe & Potter, 2000). Leaf trichomes typically
decrease with shading (Franca & Tingey, 1994; Liakoura et al., 1997; Bentz, 2003) and
in tomato, more mites were trapped in the trichomes of leaves grown under high light
conditions (Nihoul, 1993). The effect of shade on spines, thorns and prickles is less clear.
Fisher et al., 2002) showed that reductions in the density of thorns in the tropical liana,
Artabotrys hexapetalus growing in shaded sites was due to reduced irradiance rather than
spectral quality. Bazely et al., 1991) also showed reduced physical defence (prickles) in
Rubus fruticosus in shaded sites, though this could not be attributed to light per se.
Changes in the overall morphology and habit of woody plants under shade, rather than
any specific physical defence, appear to be a key factor influencing some vertebrate
herbivores (Iason et al., 1996; Hartley et al., 1997).
3. Defensive chemistry
18
Many ecological studies of the mechanisms by which light influences herbivory (there is
little comparable research on pathogens) have been conducted in the context of
alternative theories of plant defence, such as the resource availability hypothesis (Coley
et al., 1985), growth differentiation balance hypothesis (GDB: Herms & Mattson, 1992)
and carbon nutrient balance hypothesis (CNB: Bryant et al., 1983). These hypotheses
share in common the principle that plant allocation to defence is a function of
competition between end-points (growth, storage, defence) for limited resources, such as
photosynthate. A meta-analysis of almost 150 published experimental tests of CNB in
woody species (Koricheva et al., 1998) revealed that the basic prediction of the
hypothesis that shading would reduce concentrations of “carbon-based defensive
chemicals” (CBDCs) was broadly correct. Indeed, shading appeared to have a far
stronger influence on such compounds than nitrogen supply, which CNB predicts will be
inversely related to defence (Koricheva et al., 1998). When CBDCs were divided into
three subgroups, phenylpropanoids, hydrolysable tannins and terpenoids, all three were
reduced by shading, with phenylpropanoids showing the greatest response (Koricheva et
al., 1998). More recent research confirms that shading reduces concentrations of CBDCs,
in herbaceous as well as woody species (Jansen & Stamp, 1997; Crone & Jones, 1999;
Hemming & Lindroth, 1999; Rowe & Potter, 2000; Tattini et al., 2000; Briskin &
Gawienowski, 2001; Henriksson et al., 2003). In addition, it is now clear that shading
may reduce concentrations of a wide range of secondary metabolites, not only of CBDCs,
which have been the primary focus of studies associated with testing the CNB hypothesis.
Shade reduced cyanogenic glycosides but not CBDCs in Eucalyptus cladocalyx (Burns et
al., 2002), while in Prunus turneriana, shade resulted in a change in the distribution of
19
cyanogenic glycosides between older and younger leaves (Miller et al., 2004). However,
shading did not affect the concentration of defensive amides in Piper cenocladum (Dyer
et al., 2004). Exposure to UV-B increased cyanogenic alkaloids in some genotypes of
Trifolium repens (Lindroth et al., 2000) and the effects of UV-B on plant phenolics are
now very well established, and are not related to the ideas of resource limitation inherent
in the CNB hypothesis. In general, increased exposure to UV-B results in increased
concentrations of total phenolics (Bassman, 2004), although there are exceptions
(Rousseaux et al., 1998; Salt et al., 1998; Levizou & Manetas, 2001). Specific phenolic
compounds may show contrasting responses to UV-B, with flavonoids showing
particularly consistent increases (Lavola et al., 1998; Tegelberg & Julkunen-Tiitto, 2001;
Warren et al., 2002; Lavola et al., 2003; Tegelberg et al., 2003; Warren et al., 2003;
Rousseaux et al., 2004), with well established dose responses in some cases (de la Rosa
et al., 2001).
Of course, it is certainly not the case that low light reduces the concentration of defensive
chemicals in all plants (Burns et al., 2002), and a fundamental point is that not all
compounds decline in concentration under low light. This specificity in the effect of
shading, and its relationship to the responses of herbivores to putative defensive
compounds has been the subject of intense discussion in the context of alternative
defence theories (Lerdau et al., 1994; Berenbaum, 1995; Hamilton et al., 2001; Close &
McArthur, 2002; Koricheva, 2002; Nitao et al., 2002). Specificity is best characterised
for phenolic compounds in woody species. For example, in Populus tremuloides, low
light reduced proanthocyanidins (condensed tannins) but had less effect on phenolic
20
glycosides, which were the main factor influencing herbivory (Hemming & Lindroth,
1999). In Betula pubescens, total phenolics and soluble proanthocyanidins were reduced
by shade netting treatments, but gallotannins (hydrolysable tannins), cell-wall-bound
proanthocyanidins and flavonoids (including kaempferols and quercetins) were not
affected (Henriksson et al., 2003). The phenolic composition of another birch species
(Betula pendula) is influenced by light spectral quality. Tegelberg et al., 2004) concluded
that increasing R:FR shifted the balance of phenolics from chlorogenic acids to
flavonoids, and that this effect was distinct from those of increasing UV-B, which
increased concentrations of many flavonoids (kaempferols and quercetins) and
chlorogenic acids. Spectral modification had no effect on proanthocyanidins in Betula
pendula (Tegelberg et al., 2004), unlike shading treatment in Betula pubescens
(Henriksson et al., 2003). Increased R:FR increased total phenolics in seedlings of
Impatiens capensis (Weinig et al., 2004), although both these authors and Tegelberg et
al., 2004) linked changes in phenolics with the reduced growth observed at higher R:FR.
In Nothofagus antarctica, removal of solar UV-B radiation increased the concentration of
hydrolysable tannins (gallic acid and its derivatives) but decreased the concentration of a
flavonoid aglycone (Rousseaux et al., 2004). Flavonoid aglycone was also increased on
the sun-exposed side of the canopy, as was quercetin-3-arabinopyranoside (Rousseaux et
al., 2004).
The responses of herbivore to shade-induced change in host chemistry are less well
explained by bulk chemistry (total phenolics for example), than concentrations of specific
compounds (Crone & Jones, 1999; Ossipov et al., 2001; Henriksson et al., 2003;
21
Lahtinen et al., 2004; Rousseaux et al., 2004). Overall, it is increasingly clear from the
ecophysiological literature that the responses of defence-related chemicals to shade are
far more subtle that can be explained by the bulk diversion of carbon into secondary
metabolism that is predicted by the CNB hypothesis. The molecular and cellular literature
is now beginning to shed light on some of the underlying mechanisms through which this
fine-tuning of plant secondary metabolism is controlled (see Section VII).
V. Short-term responses to the light environment – induced defences
In addition to the constitutive defences produced by plants that can be influenced by light,
evidence is accumulating that induced defences may also be affected. Induced defences
are those which involve rapid changes in biochemistry and gene expression in response to
herbivore attack or pathogen infection. In the case of pathogen infection, such responses
usually require molecular recognition events, such as classic gene-for-gene based
resistance. Physical damage can also be sufficient to activate some responses, especially
in the case of herbivore defence, although several elicitors of specific responses have
been isolated from herbivore oral secretions. The term “induced resistance” broadly
refers to plant responses such as the hypersensitive response (HR), the biosynthesis of
defensive secondary metabolites (e.g. phytoalexins), and the up-regulation of expression
of defence genes (such as those encoding pathogenesis-related (PR) proteins and protease
inhibitors).
22
1. Pathogens
There is anecdotal evidence that the development of plant resistance to microbial
pathogens can often require illumination during the infection process. The scientific
literature contains a number of reports confirming this idea. For example, light is
necessary for development of resistance responses to Pseudomonas solanacearum in
tobacco (Lozano & Sequeira, 1970), Xanthomonas oryzae in rice (Guo et al., 1993), and
P. syringae and Peronospora parasitica in Arabidopsis (Mateo et al., 2004; Zeier et al.,
2004). Furthermore, red light treatments were able to induce resistance to Botrytis
cinerea and Alternaria tenuissima in broad bean (Islam et al., 1998; Rahman et al.,
2003). As well as these studies on interactions between plants and pathogens, there are
also several examples of plant responses to isolated pathogenic elicitors that are also
light-dependent. For example, leaf necrosis in tomato in response to an avirulence elicitor
from Cladosporium fulvum is substantially reduced in the dark (Peever & Higgins, 1989),
and cell death induced by the fungal toxins AAL from Alternaria alternata (Moussatos et
al., 1993) and fumonisin B1 (Asai et al., 2000; Stone et al., 2000) requires light, as does
the fumonisin B1-induced expression of the SAR marker gene, PR1 (Asai et al., 2000). In
addition, necrotic lesion formation activated by over-expression of the tomato Pto disease
resistance gene also requires light, although the same authors found that HR mediated by
the endogenous Pto gene in plants inoculated with an incompatible strain of P. syringae
was light-independent (Tang et al., 1999). This contrasts with the light-dependence of
resistance to the same pathogen in Arabidopsis conferred through a different resistanceavirulence gene interaction (Zeier et al., 2004). Interestingly, programmed cell death
caused by UV-C treatment also requires illumination with white light following a lethal
23
UV-C dose in Arabidopsis (Danon et al., 2004). It is important to note, however, that in
addition to these examples, there are many inducible defence responses that are clearly
not light-dependent. Indeed, responses to the same stimuli can involve light-dependent
and independent elements. For example, whereas cell death in response to C. fulvum
elicitor in tomato was light-dependent, lipoxygenase enzyme activation was not (Peever
& Higgins, 1989). Finally, it should be noted that these findings tend to be rather ad hoc
and based on light/dark differences – very few studies have considered the qualitative or
quantitative effects of light on resistance.
In green tissues, chloroplasts are an obvious target that can respond to changes in the
light environment, although chloroplasts might not be considered an obvious part of a
defence response. However, links between chloroplast function and disease resistance
have been identified in several systems. For example, silencing of the 33K subunit of the
oxygen-evolving complex of photosystem II (Abbink et al., 2002), or over-expression of
the DS9 chloroplast metalloprotease (Seo et al., 2000), both increase susceptibility of
tobacco plants to TMV infection. White leaves of the variegated albostrians barley
mutant support increased growth of the fungal pathogen Bipolaris sorokiniana (Schäfer et
al., 2004) and fail to produce SA in response to powdery mildew infection (Jain et al.,
2004). In Arabidopsis, the presence of functional chloroplasts is also required for HR in
leaves infected with an incompatible strain of P. syringae (Genoud et al., 2002). Thus,
resistance in a number of different plant-pathogen interactions requires chloroplast
function, though this does not necessarily mean that it requires light.
24
2. Herbivores
In contrast to pathogen defence, there are relatively few specific studies on the influence
of light on induced resistance against herbivores or responses to wounding. One
exception to this is the class of so-called indirect defences. These involve the generation
of complex mixtures of volatile compounds that are used by predators and insect
parasitoids, such as parasitic wasps, as cues to locate their prey or hosts respectively
(Paré & Tumlinson, 1999). As noted above, many investigations of herbivore-induced
volatile production have shown that this response is largely light-dependent (e.g.
Loughrin et al., 1994; Halitschke et al., 2000; Maeda et al., 2000; Gouinguene and
Turlings, 2002). In general, volatile emission induced by herbivore feeding or by
application of methyl jasmonate appears to follow a diurnal cycle, with emission being
much stronger during the light period than the dark. However, other defence-related
volatiles are also produced during the night (e.g. De Moraes et al., 2001).
The plant hormone jasmonic acid (JA) plays a central role in controlling responses to
wounding and herbivore attack and to infection by some pathogens, especially
necrotrophic fungi. The early steps of JA biosynthesis occur in the chloroplasts of
wounded leaves (Turner et al., 2002), but JA synthesis is not necessarily light-dependent.
Wound-induced JA biosynthesis was observed in soybean hypocotyls in the dark
(Creelman et al., 1992) and also occurs in non-photosynthetic tissues such as potato
tubers (Koda & Kikuta, 1994). Furthermore, Zeier et al. (2004), observed that pathogeninduced JA levels in Arabidopsis were higher in the dark than in the light. This suggests
that induced responses to wounding might be largely light-independent, though it is
25
important to note that in the vast majority of studies, no direct comparison has been made
between the wound-induced accumulation of JA under different light conditions, nor,
importantly, in the responses to wounding or JA. Where such comparisons have been
made, there is evidence in some cases that wound and JA-induced responses can in fact
be light-dependent. Most notable amongst these are the indirect defences, but direct
defence responses can also be light-dependent. For example, in a series of reports on the
expression of stress-inducible genes from rice, several were identified which in general,
required light for their induction by wounding and by exogenous JA application (Agrawal
et al., 2002a,b,c, 2003). In Arabidopsis, the ASCORBATE PEROXIDASE 2 (APX2) gene,
is also wound-induced, but by a JA-independent pathway. Instead, it appears to be
regulated by changes in photosynthetic electron transport (PET) in wounded leaves,
which results in increased levels of ROS (Chang et al., 2004). Interestingly, most of the
light-dependent wound-induced genes from rice are also responsive to applied H2O2 and
copper (a ROS generator), even in the dark (Agrawal et al., 2002b,c, 2003). These data
suggest that light-driven generation of ROS in chloroplasts around sites of wounding
might be responsible for the expression of a sub-set of wound-induced genes.
VI. Mechanisms for light-dependent induced defences.
Whilst there has been a large body of research defining the physiological basis for the
light-dependence of constitutive defences, the basis behind the affect of light on induced
resistance is less well understood. There are two general mechanisms by which light
could regulate defence responses in plants. The first of these is based on the energetic
status of light-driven chemical reactions (dependent on the ability of PET to generate
26
ATP and reducing power), and the second, the direct perception of light and downstream
light-responsive signalling pathways.
1. Photosynthesis and ROS
Photosynthesis uses light energy to drive electrons through complex electron transport
chains in the thylakoid membranes, which harvest the energy from activated carriers to
ultimately generate ATP and reducing power in the form of NADPH. These key
metabolites are then used in carbon fixation in the Calvin cycle, as well as in various
other metabolic reactions that take place in the chloroplasts, such as fatty acid
biosynthesis and assimilation of nitrogen into amino acids. There are two ways in which
these light-dependent processes in chloroplasts could impact on short term, induced
defence responses. First, major changes in gene expression, protein synthesis and defence
metabolism could potentially be affected by the loss in the dark of substrates synthesized
in chloroplasts. Interestingly, at least part of the biosynthetic pathways for three major
defence-related hormones, JA, SA and ABA are also located in plastids. Second, as
indicated above, chloroplasts can be a significant source of ROS during stress conditions.
Plant leaves acclimate to average ambient light intensities during their growth, such that
the levels of light harvesting complexes and Calvin cycle enzymes are optimised to make
most efficient use of the available light. However, when light intensities transiently
increase, or when carbon fixation is prevented, PET generates more electrons than can be
accepted by the available electron acceptor NADP+. In these situations, free electrons
from the electron transport chain can be transferred directly to oxygen to form ROS.
Secondly, increased excitation energy can be dissipated via photorespiration, which
27
ultimately results in the generation of H2O2 in the peroxisomes. Normally, a range of
biochemical and physiological systems to minimise over-reduction of the electron
transport chain and to scavenge those ROS that are produced. However, under severe
acute stress, ROS can accumulate to levels that exceed the chloroplast’s array of
antioxidant systems (Apel & Hirt, 2004). Additionally, damage to the chloroplasts or
disruption of chlorophyll biosynthesis can result in the accumulation of photosensitive
pigments that can directly generate ROS in the light. Since ROS are well known as
important regulators of several defence responses (Apel & Hirt, 2004), significant
perturbations in redox balance in the chloroplasts may contribute to ROS-regulated
defence.
The implications of the requirement for light for chloroplast-derived ROS may extend
beyond the direct signalling roles of ROS. For example, one consequence of ROS
production under stress conditions is lipid peroxidation. Many of the products of lipid
peroxidation reactions that occur following wounding or pathogen attack, are also
reactive electrophile species - molecules with reactive (electrophilic) carbonyl groups
(Vollenweider et al., 2000). Many of these electrophiles are now known to act as
important signalling molecules, eliciting a range of defence responses ranging from cell
death to defence gene expression (Vollenweider et al., 2000; Alméras et al., 2003; Thoma
et al., 2003; Cacas et al., 2005). Electrophiles produced as a consequence of stress may
either be derived from direct attack of ROS on membrane lipids, or from the activity of
lipoxygenase enzymes. Light is therefore likely to directly influence the generation of
ROS-derived electrophiles (and downstream responses), but not those generated by
28
lipoxygenase activity. Interestingly, such effects have been noted in several interactions
between plants and pathogens or their elicitors. For example, Montillet et al., (2005)
found that in response to the elicitor, cryptogein, cell death was mediated by lightdependent ROS in the light, but in the dark, cell death was independent of ROS and
correlated with the activity of a specific lipoxygenase activity. Hence, different
mechanisms for the production of bioactive electrophiles may be required to operate
under different light environments.
2. Photosensitive pigments and ROS
During pathogen resistance responses, the primary source of ROS is not the chloroplast,
but an enzyme found in the plasma membrane known as NADPH oxidase, or respiratory
burst oxidase (Apel & Hirt, 2004). One might therefore assume that light-dependent,
chloroplast-derived ROS are not likely to be important in pathogen defence. However,
the situation is not necessarily clear-cut, since the importance of the NADPH oxidase
does not preclude an additional role for chloroplast ROS. Many researchers have isolated
mutants from various species, collectively termed lesion mimic mutants, that display
spontaneous formation of necrotic lesions on their leaves (Lorrain et al., 2003). These
lesions are similar to those formed during the hypersensitive response (a key component
of disease resistance responses) and are generally accompanied by the increased
expression of PR genes and increased resistance to infection. Generally, lesion mimic
mutants were isolated and characterised as part of an effort to understand the mechanisms
of disease resistance signalling. However, it is likely that in many cases, these mutants in
fact highlight a more general link between chloroplast ROS and plant stress responses,
29
including pathogen resistance. This idea is discussed in detail elsewhere by Mullineaux
and colleagues (Karpinski et al., 2003; Bechtold et al., 2005), but is based on two
findings. First is the observation that lesion formation in many of these mutants is lightdependent (e.g. Johal et al., 1995; Genoud et al., 1998; Brodersen et al., 2002). Second,
cloning of several of the genes defined by these mutations has identified a number of
genes involved in chlorophyll biosynthesis or degradation (e.g. Hu et al., 1998; Ishikawa
et al., 2001; Mach et al., 2001; Pružinska et al., 2003). In addition, manipulation of the
expression of several other genes involved in chlorophyll biosynthesis also results in
light-dependent lesion mimic phenotypes and increased disease resistance (e.g. Kruse et
al., 1995; Mock & Grimm, 1997; Mock et al., 1999; Molina et al., 1999). The most likely
explanation for these observations is that reactive oxygen species are produced by the
action of light on chlorophyll intermediates that act as photosensitizers – that is, they
absorb light energy which excites electrons that are subsequently transferred to molecular
oxygen to form ROS. These ROS then act as signals to initiate plant defence responses,
including pathogen resistance.
Clearly then, the light-dependent generation of ROS from free photosensitive pigments or
those present in the photosynthetic light harvesting complexes can impact on defence in
mutants and transgenic plants with altered chloroplast biology. The question, then, is
whether they do so under normal circumstances. At present, it is not possible to answer
this question, but it is likely that plants have evolved mechanisms to deal with the
problems of light-dependent ROS generation in tissues under attack from pests and
pathogens. For example, the Arabidopsis CHLOROPHYLLASE 1 (AtCHL1) gene is
30
involved in chlorophyll degradation, and is required to remove photosensitive porphyrin
ring intermediates. AtCHL1 is induced by wounding and infection with necrotrophic
pathogens (Benedetti et al., 1998; Kariola et al., 2005), at which time it functions to
prevent accumulation of ROS generated from breakdown products of chlorophyll
released from damaged chloroplasts. Plants with reduced AtCHL1 gene expression show
increased resistance to Erwinia carotovora, a necrotrphic bacterial pathogen, but
increased susceptibility to Alternaria brassicicola, a fungal necrotroph (Kariola et al.,
2005). Resistance to E. carotovora is conferred by an SA-dependent pathway, whilst
resistance to A. brassicicola is normally regulated via JA-dependent signalling. Since
ROS can potentiate SA-dependent defences which in turn can antagonise JA-dependent
resistance, it appears that AtCHL1 might modulate the balance between SA- and JAdependent resistance pathways by controlling ROS generation from chlorophyll
metabolites. Interestingly, over-expression of the ACD2 red chlorophyll catabolite
reductase gene in Arabidopsis, which would be expected to reduce the accumulation of
photosensitizers, generated increased tolerance to a virulent strain of P. syringae (Mach
et al., 2001). In these plants, bacterial growth was not affected, but cell death symptoms
were reduced.
Whilst beyond the scope of this review, it is also notable that many plant species
synthesize photosensitizers that are thought to act as direct defences. In the presence of
UV-B or white light, these so-called phototoxins generate ROS that function to directly
inhibit herbivore or pathogen function (Downum, 1992). Conversley, several genera of
fungal pathogens also produce photosensitive toxins, such as cercosporin, that result in
31
plant cell necrosis (Daub & Ehrenshaft, 2000).
3. Light signalling
The second major mechanism suggested above by which light may regulate defence is via
direct light-responsive signalling pathways. Evidence for this type of regulation has been
recently uncovered in Arabidopsis. Genoud et al. (1998) identified an Arabidopsis light
signalling mutant, psi2, that in addition to effects on light-dependent expression of
photosynthetic genes, displayed light-dependent development of spontaneous necrotic
lesions and increased PR1 gene expression. Further characterisation of these phenotypes
showed that light regulated the resistance responses at multiple levels. First, PSI2 is a
regulator of phytochrome-mediated responses, and PhyA and PhyB are also required for
light-dependent HR lesion formation and PR gene expression (Genoud et al., 2002).
Consequently, resistance to P. syringae is reduced in phytochrome mutants and increased
in the psi2 mutant. This illustrates an example of light acting in a direct signalling role to
modulate induced resistance. How and why phytochrome signalling might impact on
disease resistance is unclear, though it might represent a sensitive mechanism by which
cytosolic and nuclear responses are matched with changes in chloroplast activity caused
by variations in light intensity. Perhaps significantly, in these experiments, HR (although
not PR gene expression) also required the presence of functional chloroplasts, since cell
death was not observed in white sectors of variegated leaves. Hence, both metabolic and
signalling roles for light may combine to co-ordinate a full resistance response.
32
In terms of induced defences, therefore, we can identify a range of different levels of
interaction between light and responses to biotic attack. These include a range of effects
on ROS generation, as well as direct signalling roles for light via phytochrome signalling,
and are summarised in Figure 1.
VII. Interpreting interactions between light and defence responses.
In assessing the range of experimental systems discussed above, a general conclusion is
that where light has been found to modulate plant defence against herbivores or disease,
then its effect is usually to increase defence. A key question, therefore, is whether we can
identify mechanistic explanations for this observation. As is often the case, ecologists and
molecular biologists have taken very different approaches to the question of interactions
between light and defence. Given that this is a complex interaction with different
components, it is not surprising that such different approaches are possible. Clearly, the
fundamental importance of light for plant growth and development means that there is no
single explanation that can unite observations across widely different scales of
organisation. However, one way forward is to place the whole range of evidence, from
molecular to ecophysiological, within the framework of optimal defence theory
(Hamilton et al., 2001). Is a greater investment in defence in high light consistent with
optimal defence theory, and, if so, does the molecular and cellular data provide insights
into the mechanisms through which optimal defence is achieved? This relates to a second
important point which is the precise terminology used to describe defence. The semantics
of defence in plant pathogen or plant herbivore interactions, which has been widely
debated by ecologists and ecophysiologists (Clarke, 1986; Stowe et al., 2000), but less so
33
by cell and molecular biologists, forms a pertinent background to these questions.
Defence is defined as any mechanism that protects the plant from reductions in fitness in
the presence of herbivores or pathogens and has two components. The first component is
resistance, which reduces the severity of attack by inhibiting the activity or performance
of the herbivore or pathogen. The second component is tolerance, which reduces the
negative consequences of attack on host fitness. In our view the clear differentiation
between resistance and tolerance is essential to understanding mechanisms of interactions
between light and defence.
The first requirement of optimal defence theory, that tissues which have the greatest
value to the plant should be most defended, is clearly satisfied. Models of canopy
photosynthesis are consistent in showing that leaves exposed to high light contribute most
photosynthate (Leuning et al., 1995; dePury & Farquhar, 1997). Secondly, defence
should be in proportion to the probability of attack. There are clearly many systems in
which herbivores are more abundant and/or more active in high-light environments, for
example due to higher temperatures (see section III). Arguably, the higher nitrogen
concentration of high light tissues may increase their potential palatability for herbivores,
and so increase the risk of attack. There are certainly examples where exposed tissues
suffer more herbivory even though they are better defended (e.g. Louda & Rodman,
1996; Sipura & Tahvanainen, 2000). These arguments are harder to apply for pathogens,
and if anything, it might be expected that the probability of infection might be lower
under high light conditions due partly to direct light effects (see Section II) and partly to
the correlated lower humidity and leaf surface water. The third requirement of optimal
34
defence theory is that defence is a function of the balance between its benefits and its
costs. The “broad-brush” prediction of the CNB hypothesis, that defence is less costly
under high light conditions because substrates are more freely availability, fails to explain
the specificity in the responses of individual metabolites to the light environment.
Nonetheless, there are a number of other mechanisms that could result in altered costs of
defence under different light conditions.
One element of changed costs of defence may relate to the induction of shade-avoidance
mechanisms under low light conditions. The possible trade-offs between defence and
shade avoidance responses at low light as they relate to competitive ability has recently
been reviewed by Cipollini, 2004), who argued that shade avoidance responses could
constrain defence via a number of mechanisms. Firstly, the shift in allocation to extension
growth under shade might directly compete with allocation to defence, although not
necessarily by competition for resources. There may be direct interference between the
signalling mechanisms controlling acclimation to the light environment and those
regulating defence. Increased stem elongation in the shade response is under the control
of auxins and gibberellins (Vandenbussche & Van Der Straeten, 2004). Auxin may
interact with defence via cross-talk between IAA and defence signalling, such that IAA
reduces JA-induced production of defence compounds (Kernan & Thornburg, 1989;
Baldwin et al., 1997). Conversely, the levels of active auxins and the expression of auxin
response genes are reduced by wounding (Thornburg & Li, 1991; Cheong et al., 2002;
Schmelz et al., 2003) and herbivory (Schmelz et al., 2003). Cipollini, 2004) also
suggested that cell wall stiffening might be a mechanism for antagonism between shade
35
avoidance and defence, with the gibberellin–mediated cell wall loosening leading to
increased cell expansion in the shade being incompatible with the cell-wall stiffening that
can be a significant component of defence.
Cipollini (2004) described the interference between the shade-response and defence as an
opportunity cost but equally, there may be a range of “opportunity benefits” that reduce
the cost of defence in high light, because processes induced for photoprotection also
confer protection against biotic attack. High light stress, including UV-B irradiation,
activates molecular responses that have much in common with pathogen and herbivore
responses (Mackerness et al., 1999; Rossel et al., 2002; Kimura et al., 2003; Izaguirre et
al., 2003; Stratmann, 2003). In fact, the increasing documentation of the kinds of
responses induced by various biotic and abiotic stresses makes it clear that there are many
overlaps in these responses. To try to understand the significance of these overlapping
responses, it is useful to consider what the functions of induced responses to these
different environmental factors might be. For example, many stress responses include
increases in the accumulation of antioxidants and the expression of protective chaperone
proteins (such as heat shock proteins and osmoprotective proteins). Many forms of
environmental insult will disrupt biochemistry leading to increased ROS generation for
example, requiring increased antioxidant production to counteract their cytotoxic effects.
While there may be many mechanisms for “opportunity benefits”, in our view, many may
be based on the involvement of ROS in responses to light, herbivory and disease.
Understanding these potential mechanisms requires careful differentiation between
resistance and tolerance.
36
Light and the resistance components of defence against herbivore or pathogen
attack
Light-driven generation of ROS in damaged plants may be central to interactions between
light and the resistance components of defence against pathogens or herbivores.
Photosensitive chlorophyll degradation intermediates formed as a result of cellular
damage caused by herbivores and necrotrophic pathogens can contribute to ROS
generation and defence signalling (Kariola et al., 2005), as does excess hydrogen
peroxide derived from photorespiration (e.g. Champognol et al., 1998; Mateo et al.,
2004). Several studies described in Section V also indicate a requirement for functional
chloroplasts to activate the HR during pathogen resistance, which might also suggest a
functional relationship between light-driven reactive oxygen chemistry and defence.
NADPH oxidase is clearly an important source of ROS for defence signalling, but is
metabolically costly (in terms of NADPH consumption). It is possible that in some
systems, ROS generation is supplemented by the action of light on photosensitive
pigments such as chlorophyll. Potentially, ROS provides a basis for a “supply side”
hypothesis very different from CNB. Resistance is facilitated in (high) light tissue
because ROS for signalling can be supplied at less cost via light-driven reactions than
those occurring in the dark. Interestingly, there is evidence that elevated UV-B can
enhance wound-induced defensive chemicals (Levizou & Manetas, 2001).
There are also specific examples of proteins involved in both resistance and responses to
light that may be directly involved in signalling cross-talk. The zinc finger transcriptional
37
regulator, LSD1 is an Arabidopsis protein first identified through a genetic mutation
which conferred a runaway cell death phenotype (Jabs et al., 1996). The LSD1 gene has
been studied mainly with regard to its role as a negative regulator of pathogen-induced
hypersensitive cell death. More recently, however, it has also been shown that LSD1 is
also involved in acclimation to high light stress (Mateo et al., 2004). Interestingly, the
same authors showed that the effects of LSD1 on pathogen-induced cell death are
mediated by ROS generated during light-dependent photorespiration. NPR1/NIM1 is
another signalling protein identified as a key regulator of multiple pathogen resistance
pathways. Over-expression of a rice NPR1 gene leads not only to elevated disease
resistance, but also to hypersensitivity to light (Chern et al., 2005).
Light and the tolerance components of defence against herbivore or pathogen attack
As noted above, both biotic attack and light stress are sources of oxidative stress in plant
tissues. Furthermore, light and biotic attack may also act synergistically to increase
oxidative stress. Biotic stress can result in uncoupling of the light and dark reactions of
photosynthesis, meaning that “normal” ambient light levels cause ROS generation from
photosynthesis (Bechtold et al., 2005). One common feature of many stress responses is
the down-regulation of genes encoding many components of the photosynthetic
machinery (e.g. Izaguirre et al., 2003; Kimura et al., 2003). This may serve as a negative
feedback loop to reduce ROS generation, but also to shift metabolism into areas that
compete with photosynthesis, such as the oxidative pentose phosphate and shikimic acid
pathways (Scharte et al., 2005). Plant mechanisms involved in protection against
oxidative stress or repairing the damage it causes are known to be activated by both light
38
and herbivore or pathogen attack (e.g. Rossel et al., 2002; Kimura et al., 2003; Apel &
Hirt, 2004). A key point is that these are tolerance mechanisms not resistance. Clear
differentiation between such mechanisms and resistance (i.e. mechanisms that inhibit the
herbivore or pathogen) is central to understanding interactions between light and defence,
not least the widely discussed role of phenolic compounds in such interactions.
Plant phenolics are a highly diverse group of chemicals that fulfil a range of functions.
Some phenolics have demonstrable roles in plant interactions with herbivores or
pathogens, either as components of resistance (see above) or as attractants for herbivores
(e.g. Roininen et al., 1999; Ikonen et al., 2002). Other phenolics function as action as
“sunscreens” or antioxidants, and some authors have argued that photoprotection is the
primary role of many plant phenolics (Close & McArthur, 2002). In considering
interactions between light and defence, key points are (i) that plants in high light
conditions are potentially confronted with the risk of increased herbivory (see above) and
the concurrent need for photoprotection and (ii) that both light and attack can induce
oxidative stress. Under such conditions phenolic compounds might fulfil at least three
functions: (a) sun-screens reducing light penetration to vulnerable tissues (not selected for
by herbivory or disease), (b) antioxidants involved in reducing the damage caused by
ROS (selected for by biotic attack as well as light) and (c) resistance compounds
inhibiting the activity of herbivore or pathogen (not selected for by light).
These multiple functions would be expected to result in the compound-specific changes
in the concentration of phenolics evident in the recent ecophysiological literature (see
Section IV). They would also be expected to lead to different trade-offs in the production
39
of phenolics. In terms of tolerance, the production of phenolic antioxidants in high light
tissue might be seen as an opportunity benefit for defence against biotic attack.
Conversely, the synthesis of phenolics conferring resistance (sensuo stricto) against
herbivory or disease may represent an opportunity cost on the production of phenolics
acting as sun-screens, and vice versa.
The different trade-offs discussed above might be expected to be reflected in enzyme
activity and gene expression. From this perspective the three functions of phenolics noted
above, while distinct, might all be expected to be associated with an elevated basal flux
through the phenylpropanoid pathway. This may explain some of the parallels in terms of
global gene expression between herbivory and light stress (e.g. Izaguirre et al., 2003;
Gachon et al., 2005). Most commonly, it is the genes encoding the enzymes controlling
entry of substrates into the phenylpropanoid pathway, such as phenylalanine ammonia
lyase (PAL) and chalcone synthase (CHS) that are noted as responsive to multiple
stresses. However, such induction of PAL or CHS is clearly only one element in the
regulation of the phenylpropanoid pathways and there are examples of competition
between elements of phenylpropanoid metabolism delivering compounds with different
functions. In Sorghum bicolor there is competition between the accumulation of
anthocyanin in response to light and the synthesis of phytoalexins in response to
challenge by the fungus Cochliobolus heterostrophus (Lo & Nicholson, 1998). This was
attributed to the down-regulation of genes specific to anthocyanin biosynthesis and the
corresponding up-regulation of genes encoding enzymes involved in phytoalexin
synthesis (Lo & Nicholson, 1998). Similarly, in grapes, there appears to be competition
40
between the production of anthocyanins of photoprotection and phytoalexins (resveratrol)
for defence against pathogens (Jeandet et al., 1995).
These results show that the plant is able to “fine-tune” phenolic metabolism as the
balance of costs and benefits shift in the face of competing end-points. Recent detailed
analyses are revealing the details of the regulation of the phenylpropanoid pathway. In
the field, exposure of Vaccinium myrtillus to full sunlight up-regulates a whole series of
phenylpropanoid pathway enzymes but changes in PAL and CHS are much smaller than
changes in “downstream” enzymes involved in the synthesis of specific photoprotective
compounds (Jaakola et al., 2004). It is clear that sets of several phenylpropanoid pathway
genes, for example those involved in flavanol or monolignol biosynthesis, are coregulated during both development and stress responses (Gachon et al., 2005). In the case
of light-responsive expression of flavanol biosynthesis, one mechanism for this coregulation was demonstrated to stem from the possession of common transcription factor
binding sites in the promoters of co-regulated genes (Hartmann et al., 2005). However,
while there is clearly co-regulation of major elements of the phenylpropanoid pathway,
not all enzymes are represented in these gene expression clusters (Gachon et al., 2005).
Furthermore, many key downstream enzymes exist in different isoforms with different
substrates and products, fulfilling different functions (Kumar & Ellis, 2003). Thus, upregulation of a single enzyme, or even a cluster of co-regulated elements of a pathway
under high light or biotic attack may reveal little without understanding the behaviour of
those enzymes controlling pathway endpoints.
41
In our view, there is no single answer to the question of how light alters the cost of
defence against herbivory or pathogen attack. However, on the balance of the evidence, it
seems likely that costs will often become lower with increasing light. This, taken with the
greater value of high light tissues and the greater risk of attack, at least by herbivores,
suggests that the greater defence is consistent with the predictions of optimal defence
theory. The argument that plants have fine control of defence metabolism, which is a
major contrast to “supply-side” theories such as CNB, is well-established (e.g.
Berenbaum, 1995), and molecular studies are increasingly revealing the nature of such
fine control. Research at the scale of the transcriptome and metabolome have begun to
provide information on the mechanisms by which optimum defence is achieved.
However, it is clear that proper understanding of optimum defence cannot be gained
through quantification of bulk changes at the whole plant or whole organ level, whether
in global gene expression, or in bulk measures of defensive chemistry, such as total
phenolics. What is required is more detailed temporal and spatial resolution of the
responses of specific genes or compounds in the context of their function in the plant
under biotic attack and different light conditions.
Whilst ecologists and molecular biologists have mostly taken different approaches to the
question of interactions between light and defence, we feel that these approaches can
provide an interface which can deliver benefits to both sets of disciplines. Work across
these scales can be extremely effective in linking molecular responses with ‘real life’
ecological outcomes to stress (see, for example, work from the group of Ian Baldwin),
42
and we strongly encourage efforts to integrate molecular and ecological studies in all
areas of biology.
Acknowledgements
Work on this topic in the authors laboratories was supported by a Royal Society
University Research Fellowship (MRR) and research grants from DEFRA (CSA6138)
and the UK Horticultural Research Council (CP19) to NDP. We would also like to thank
the anonymous referees for their encouraging and helpful comments.
43
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Table 1 Overview of field experiments into the effects of the light environment on (a) plant-herbivore interactions and (b) plant-pathogen
interactions. These studies considered the effects of variation in total light, and in some cases responses have been attributed not just to
photosynthetic radiation but the longer wavelengths of sunlight, resulting in changes in the thermal environment. The potential role of UV
wavelengths was not considered in these studies. Key: +ve indicates that shade increases the leaf area eaten by a herbivore or infected by a
pathogen, or has some beneficial effect on herbivore performance or behaviour (e.g. reduced mortality, increased growth rate, increased
efficiency of food conversion etc. ), -ve indicates negative responses, 0 indicates that shade treatments had no significant effect. na indicates
not assessed.
Source of variation in the light
environment
Fagus crenata / Natural herbivore community
Natural variation with position in canopy
Betula pubescens / Epirrita autumnata
Natural variation with position in canopy
Tilia cordata / Popillia japonica
Natural variation with position in canopy
Prunus mahaleb / Yponomeuta mahalebella
Natural variation with position in canopy
Nothofagus antarctica and natural herbivore community
Natural variation with position in canopy
Liriodendron tulipifera and Cornus florida / Natural Range of natural field sites, plus artificial
herbivore community
shading,
Five trees species / Atta cephalotes
Plants grown in full sun or partial shade
Populus deltoides / Plagiodera versicolora
“Open” versus “shade” sites
Salix phylicifolia / Galerucella lineola and Salix
Field sites with or without tree canopy
myrsinifolia / Phratora vitellinae
Inga oerstediana / Atta cephalotes
Understory, tree-fall gaps and full sun
Cardamine cordifolia /Natural herbivore community.
Removal of natural shade.
Lycopersicon esculentum / Manduca sexta
Artificial shading
Betula pubescens / Epirrita autumnata
Artificial shading
Amaranthus palmeri/ Spodoptera exigua
Artificial shading
Borrichia frutescens / Pissonotus quadripustulatus
Artificial shading
Rhododendron mucronatum / Stephanitis pyrioides
Artificial shading
Vallisneria natans / Radix swinhoei
midday fluxes 15-280 mol m-2 s-1
Host/herbivore
65
Effect of shading
on leaf area eaten
Effect of shading
on the herbivore
Source
+ve
na
-ve
na
+ve
na
+ve
na
-ve
na
32
30
26
1
25
+ve
na
6
+ve
+ve
na
na
7
4
+ve/ 0
+ve / 0
28
-ve
-ve
+ve
+ve
+ve
na
-ve
-ve
na
-ve
na
na
-ve/+ve
+ve
+ve
+ve/-ve
21
17
11
10
20
19
3
16
Table 1b The effects of the light environment on plant-pathogen interactions
Host/pathogen
Source of variation in the light environment
Phlox / Erysiphe
Anemome nemorosa / Tranzchelia anemones
Anemome nemorosa / Ochropsora ariae
Agrostis stolonifera / naturally occurring
pathogens
Brachypodium sylvaticum / Epichloe sylvatica
Camellia sinensis / Exobasidium vexans
Camellia sinensis / Hemileia vastatrix
Shaded or open sites in the field
Shaded or open sites in the field
fungal
Quercus petraea / Microsphaera alphitoides
Betula papyrifera and naturally occurring soil pathogens
Forest tree seedlins/ Pythium spp.
Phacidium coniferarum
Glycine soya / Sclerotinia sclerotiorum
Medicago sativa / Verticillium albo-atrum
Medicago sativa /Fusarium oxysporum
Euonymus fortunei / Colletotrichum gloeosporioides
Picea mariana / Botrytis cinerea
Rhododendron sp / Erysiphe sp.
Triticum aestivum / Puccinia striiformis
Lycopersicon esculentum / Botrytis cinerea
Effect of shading
on infection
+ve
+ve
0
Source
12
8
Shaded or open sites in the field
+ve
15
Shaded or open sites in the field
Shaded or open sites in the field
Shaded or open sites in the field
Shaded or open sites in the field
Shaded or open sites in the field
Artificial shading
Artificial shading
+ve
+ve
-ve
-ve
+ve
+ve
+ve
+ve
+ve
0
-ve
+ve
+ve
-ve
+ve
18
19
Artificial shading
Artificial shading
Artificial light treatments, pre-inoculation only
Artificial light treatments, pre-inoculation only
Artificial light treatments, pre-inoculation only
Artificial light treatments, pre-inoculation only
29
13
2
31
24
22
33
14
5
27
Literature cited in Table 1.
1, Alonso, 1997); 2, Augspurger & Kelly, 1984; 3, Bentz, 2003); 4, Crone & Jones, 1999); 5, de Vallavieille-Pope et al., 2002; 6, Dudt &
Shure, 1994); 7, Folgarait et al., 1996); 8, Garcia-Guzman & Wennstrom, 2001; 9, Gunasekera et al., 1997; 10, Henriksson et al., 2003); 11,
Jansen & Stamp, 1997); 12, Jarosz & Levy, 1988; 13, Kelly, 2002; 14, Kenyon et al., 2002; 15, Koh et al., 2003; 16, Li et al., 2005); 17, Louda &
Rodman, 1996); 18, Meijer & Leuchtmann, 2000; 19, Moon et al., 2000); 20, Moran & Showler, 2005); 21, Nicholsorians, 1991); 22, Ningen et
al., 2005; 23, O'Hanlon-Manners & Kotanen, 2004; 24, Pennypacker, 2000; 25, Rousseaux et al., 2004; 26, Rowe & Potter, 1996); 27, Shafia et
al., 2001; 28, Sipura & Tahvanainen, 2000; 29, Soto-Pinto et al., 2002; 30, Suomela et al., 1995; 31, Wainhouse et al., 1998; 32, Yamasaki &
Kikuzawa, 2003; 33, Zhang et al., 1995
66
Table 2 Overview of the effects of ultraviolet radiation on plant-herbivore interactions. These studies specifically manipulated ultraviolet
radiation using lamps or wavelength-selective filters. Unless otherwise stated only UV-B (290-320nm) has been experimentally
manipulated.
Host / herbivore
Ipomoea
batata/
Bemisia
tabaci,
Frankliniella occidentalis, or Aphis gossypii.
Zea mays / Ostrinia nubilalis
Oryza sativa / Helicoverpa armigera
Bemisia argentifolii
occidentalis
and
Frankliniella
Pisum sativum / Autographa gamma
Trifolium repens / Spodoptera litura or
Graphania mutans
Glycine max / Caliothrips phaseoli
Caliothrips phaseoli
Lolium perenne and
Schistocerca gregaria
Festuca
spp.
/
Plantago lanceolata / Precis coenia or
Trichoplusia ni
Trialeurodes vaporariorum
Quercus robur / natural herbivore
community
Gunnera magellanica and natural herbivore
community
Gunnera magellanica and natural herbivore
community
Experimental conditions
Effect of UV manipulation
Polythene tunnels with ambient
Substantial reductions in attack by all three insects
or attenuated total solar UV
+ or – UV in the glasshouse
Larvae preferred leaves grown without UV-B
Extracts of irradiated leaves had antifeedant, growth-inhibitory
Artificial UV-B irradiation
and antibiotic properties against larvae, and effects persisted
into adults, which laid fewer, less viable eggs.
Polythene tunnels with ambient Insects dispersed preferentially into ambient UV
or attenuated total solar UV
environments, but UV had no effect on flight ability.
Increased UV-B increased leaf nitrogen and when foliage was
CE room with a range of UV-B fed to larvae this was correlated with an increase in larval
doses
growth rate and a reduction in the amount of plant material
consumed.
36% reduction in weight of S. litura on foliage grown at high
CE room with and without UVUV, but this depended on host genotype. G. mutans showed
B
little response
Ambient or near zero UV-B in UV-B reduced thrip herbivory: insects preferred leaves from
the field
reduced UV-B and avoided solar UV.
Ambient or near zero UV-B in
Insects preferred low UV-B environment
the field
No herbivore responses to excised leaves from different UV-B
Ambient and elevated UVA or
treatments except in F. pratensis where responses varied with
UV-B in the field
UV treatment and/or endophyte infection of the host
Growth of T. ni larvae was faster when fed excised leaves
CE room at high ambient or from elevated UV-B. Direct exposure of larvae to the UV
above.
treatments increased mortality of T. ni. UV had no significant
effects on P. coenia.
Polythene tunnels with ambient Attenuation of UV reduced whitefly dispersion, resulting in
or attenuated total solar UV
reduced populations in low UV tunnels
Ambient and elevated UVA or Plants under elevated UV-B or UV-A suffered greater
UV-B in the field
herbivory
Ambient or near zero UV-B in
Leaf area damaged increased under reduced UV-B.
the field
Ambient or near zero UV-B in
Leaf area consumed increased 25-75% under attenuated UV-B
the field
67
Source
1
2
3
4
5
6
7
8
9
10
11
12
13
14
Ambient or near zero UV-B in
Nothofagus antarctica and natural herbivore
the field, and sun-exposed and
community
shaded branches
Calluna vulgaris / Strophingia ericae Ambient and elevated UV-B in
(Homoptera)
the field
Salix myrsinifolia and S. phylicifolia /
Phratora vitellinae or natural herbivore
community
Populus trichocarpa / Chrysomela scripta
6 plant species and Deroceras reticulatum
(Mollusca)
Glycine max / Anticarsia emmatalis or
natural herbivore community
Morus nigra / Bombyx mori
Solar UV-B reduced insect damage by at least 30%, and this
occurred with foliage in both sunny and shaded positions.
Increased UV-B reduced herbivore population density over
two seasons
Herbivores more abundant under elevated UV-B but host did
not suffer greater herbivore damage. Excised leaves of S.
Ambient and elevated UV-B in
phylicifolia, from elevated UV-B reduced growth of P.
the field
vitellinae larvae compared with control leaves, but there was
no comparable effect with leaves of S. myrsinifolia.
Leaves from highest UV-B significantly reduced larval
Zero, ambient and 2x ambient
consumption efficiency
Significant effects in two of the six species. In Nothofagus
Ambient or near zero UV-B in antarctica, leaf area consumed reduced by 2/3rds in foliage
the field
from under near-ambient UV-B. In Carex decidua twice as
much as leaf area was consumed in reduced UV-B radiation.
Leaves from reduced UV-B were more attractive to larvae,
Ambient or near zero UV-B in supported higher growth rates and lower mortality. No direct
the field
effect of UV exposure on larval mortality. Attentuation of UV
increased natural herbivore damage by 2-fold.
Artificial UV irradiation in CE
UV treatments reduced consumption of foliage by larvae.
rooms
15
16
17
18
19
20
21
Literature cited in Table 2.
1, Antignus et al., 1996; 2, Bergvinson et al., 1995; 3, Caasi-Lit, 2005; 4, Costa & Robb, 1999; 5, Hatcher & Paul, 1994; 6, Lindroth et al., 2000; 7,
Mazza et al., 1999; 8, Mazza et al., 2002; 9, McLeod et al., 2001; 10, McCloud & Berenbaum, 1999; 11, Mutwiwa et al., 2005; 12, Newsham et al.,
1999; 13, Rousseaux et al., 1998; 14, Rousseaux et al., 2001; 15, Rousseaux et al., 2004; 16, Salt et al., 1998; 17, Veteli et al., 2003; 18, Warren et al.,
2002; 19, Zaller et al., 2003; 20, Zavala et al., 2001; 21, Yazawa et al., 1992.
68
Figure Legends:
Figure 1. Impacts of light on plant resistance against pests and pathogens.
Different forms of biotic attack (top row) activate different major routes to resistance
(second row), as well as repair and healing mechanisms. Light can act positively (solid
arrows) or negatively (barred lines), via a number of distinct pathways. Many of these
affect the generation of reactive oxygen species, which appears to be a key node for the
interactions between light and defence.
69