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Plant Physiology 132:1755-1767 (2003) © 2003 American Society of Plant Biologists Convergent Responses to Stress. Solar Ultraviolet-B Radiation and Manduca sexta Herbivory Elicit Overlapping Transcriptional Responses in Field-Grown Plants of Nicotiana longiflora1,[w]Ifeva, Consejo Nacional de Investigaciones Científicas y Técnicas, and Universidad de Buenos Aires, Avenida San Martín 4453, C1417DSE Buenos Aires, Argentina (M.M.I., A.L.S., C.L.B.); and Max Plank Institute for Chemical Ecology, Department of Molecular Ecology, Winzerlaer Strasse 10, D–07745 Jena, Germany (I.T.B.)
The effects of solar ultraviolet (UV)-B (280–315 nm) on plants have been studied intensively over the last 2 decades in connection with research on the biological impacts of stratospheric ozone depletion. However, the molecular mechanisms that mediate plant responses to solar (ambient) UV-B and their interactions with response mechanisms activated by other stressors remain for the most part unclear. Using a microarray enriched in wound- and insect-responsive sequences, we examined expression responses of 241 genes to ambient UV-B in field-grown plants of Nicotiana longiflora Cav. Approximately 20% of the sequences represented on the array showed differential expression in response to solar UV-B. The expression responses to UV-B had parallels with those elicited by simulated Manduca sexta herbivory. The most obvious similarities were: (a) down-regulation of several photosynthesis-related genes, and (b) up-regulation of genes involved in fatty acid metabolism and oxylipin biosynthesis such as HPL (hydroperoxide lyase),  -DIOX (alpha-dioxygenase), LOX
(13-lipoxygenase), and AOS (allene oxide synthase). Genes encoding a
WRKY transcription factor, a ferredoxin-dependent glutamate-synthase, and
several other insect-responsive genes of unknown function were also similarly
regulated by UV-B and insect herbivory treatments. Our results suggest that
UV-B and caterpillar herbivory activate common regulatory elements and provide
a platform for understanding the mechanisms of UV-B impacts on insect
herbivory that have been documented in recent field studies.
UV-B induces multiple responses in terrestrial plants. These responses have been studied using a variety of experimental approaches, from controlled-environment experiments to large-scale field trials, and covering a broad spectrum of scales, from molecular to ecosystem level processes. Controlled-environment experiments have contributed most of the information presently available on responses at the molecular level. However, this type of experiment, particularly those that are based on the use of heavily unbalanced light sources (i.e. with unnaturally high ratios of UV-B to photosynthetically active radiation [PAR] or UV-B to UV-A [315–400 nm]), are frequently criticized on the grounds that they lack functional and ecological realism (Fiscus and Booker, 1995  ;
Caldwell and Flint, 1997). It
has been shown clearly that treatments with high UV-B to PAR ratios, which are
the norm in controlled-environment exposures, tend to result in greatly
exaggerated effects of UV-B on photosynthesis and growth inhibition. Because
these effects have been hard to duplicate under field conditions, it is
unclear to what extent the molecular and mechanistic data that have been
produced under spectrally unbalanced conditions (which commonly involve PAR
levels lower than 1:10 of full sunlight) contribute to our understanding of
the normal physiological responses of plants to ambient UV-B stress. In fact,
it has been clearly demonstrated that the level of PAR strongly modulates the
effect of UV-B on the transcription of various photosynthetic genes: the
higher the PAR, the smaller the UV-B-induced alteration in message abundance,
which in several cases could be completely eliminated
(Jordan et al., 1992;
Strid et al., 1996).
Under field conditions, the inhibitory effect of ambient UV-B on the growth
of herbaceous terrestrial plants seldom exceeds 20% (Ballaré et al.,
1996
Plants often activate a battery of defense mechanisms in response to
herbivore attack, which improve their chances of surviving further attacks by
the same species or other species of herbivores
(Karban and Baldwin, 1997
We wanted to determine whether the effects of solar UV-B on insect
resistance in field-grown plants are mediated by the elicitation of defense
responses similar to those induced by insect attack. As an initial step in
this direction, we attempted to identify genes involved in the responses of
field-grown plants of Nicotiana longiflora to solar UV-B using a
custom-made cDNA microarray that contained approximately 250 Nicotiana
attenuata genes known to be regulated in response to attack by chewing
larvae of Manduca sexta
(Halitschke et al., 2003
Experimental Design and Application of a cDNA Microarray to Study UV-B Impacts on Defense-Related Genes
The method used to array PCR fragments of insect-responsive N.
attenuata genes onto epoxy-coated slides has been described
(Halitschke et al., 2003
For our field experiments, we used 5-week-old plants of N.
longiflora, a wild species native to the central region of Argentina that
is closely related to N. attenuata. The plants were grown in large,
replicated plots for 3 weeks in a field site in Córdoba (Central
Argentina) under near-ambient or attenuated solar UV-B radiation (see
"Materials and Methods" for a description of the experimental
layout and the growth conditions). At the time of harvest, plants were still
at the rosette stage, and there were no obvious differences between UV-B
treatments in overall plant growth or morphology, which is consistent with the
results obtained in the field for other Solanaceous species exposed for short
periods to similar UV-B treatments
(Ballaré et al., 1996
Of the 241 M. sexta-responsive, regurgitate-responsive, and control genes included in the array, 48 revealed differential expression in response to solar UV-B in the field-grown plants of N. longiflora (Fig. 1; Table I; the complete data set is available as Supplemental Table I at http://www.plantphysiol.org). The genes included in the array were clustered into functional groups based on known or inferred function of the gene product. For many of the sequences, no functional information is available other than their transcript abundance is regulated in response to M. sexta herbivory or regurgitate treatment; therefore, they are likely to play some role in metabolic reconfiguration after insect attack. Those genes were included in two separate categories: M. sexta regulated and regurgitate responsive (see "Materials and Methods" for details).
The most consistent expression responses to solar UV-B were found in the clusters of photosynthesis- and fatty acid metabolism-related genes (Fig. 1; Table I). Most of the probes included in the array for genes that encode components of the photosynthetic apparatus indicated lower transcript abundance in plants chronically exposed to solar UV-B than in the control plants. Among these were genes for Calvin cycle enzymes, such as the small subunit of Rubisco, and genes encoding for PSII polypeptides (e.g. genes with similarity to the tomato lhbC1 gene for LHCII type III, spinach 6.1-kD polypeptide, and NtPII10). Interestingly, one photosynthesis-related gene, encoding a PSII-O2-evolving complex 23-kD polypeptide, was up-regulated in plants exposed to ambient UV-B (Table I).
In contrast to the response of photosynthesis-related transcripts, most of
the probes for genes that encode enzymes involved in fatty acid metabolism and
oxylipin synthesis showed increased transcript abundance in plants exposed to
solar UV-B. Among the up-regulated genes were A similar UV-B-induced increase in expression level was found for genes that encode enzymes directly or indirectly involved in N metabolism (such as the ferredoxin-dependent Glu-synthase [FDGS] and a molybdopterin synthase sulfurylase), and a gene encoding a WRKY-type transcription factor (WRKY-2). In contrast, exposure to solar UV-B reduced the abundance of PI transcripts and transcripts with similarity to the basic-type pathogenesis-related protein PR1 of tobacco. Solar UV-B also affected the abundance of several transcripts of unknown function that have been previously shown to be regulated by natural or simulated M. sexta herbivory and/or wounding + regurgitate treatment (Fig. 1; Table I).
We tested the generality of the UV-B impact by comparing the transcriptional responses shown in Figure 1 with those elicited in N. attenuata by realistic levels of UV-B provided against high PAR in a completely independent experiment under greenhouse conditions (see "Materials and Methods"). The two experiments showed a similar pattern of UV-B response (Fig. 2). The most obvious parallels were: (a) very similar effects on the abundance of photosynthesis-related transcripts, and (b) similar up-regulation of genes involved in fatty acid metabolism and oxylipin synthesis and consistent effects on FDGS (up-regulation) and PR1 (down-regulation). The only remarkable difference between the expression patterns detected in these experiments was the positive effect of artificial UV-B on PI expression in N. attenuata, which contrasts with the reduction in PI transcript abundance in N. longiflora plants exposed to ambient UV-B (Fig. 2; see Supplemental Table I at http://www.plantphysiol.org). Analysis of the data presented in Figure 2 shows a highly significant correlation between the data sets (P < 0.0001 for a linear model; R2 = 0.29; or R2 = 0.50 if the PI data points are removed). This similar regulation in two Nicotiana spp., tested in completely independent experiments, provides strong evidence that the results presented in Figures 1 and 2 reflect a general pattern of transcriptional response to ambient or near-ambient UV-B doses.
To compare the effects of solar UV-B and insect herbivory, we applied a simulated-herbivory treatment to field-grown N. longiflora plants. For the treatment, we wounded the leaves with a fabric pattern wheel and applied to the wounds oral secretions collected from fourth instar M. sexta caterpillars. Twenty-four hours after elicitation, the leaves were harvested, and RNA was extracted for analysis.
The observed expression responses for well-characterized genes (small
subunit of Rubisco gene and pseudogene, AOS, HPL,
Figure 3 shows direct
comparisons of gene expression responses to solar UV-B and simulated herbivory
in N. longiflora. The treatments had similar effects on various
functional groups of genes (Fig.
3A). In the photosynthesis-related group, the same genes encoding
for PSII polypeptides that were down-regulated by UV-B were also
down-regulated by simulated herbivory. Probes for Rubisco also showed reduced
transcript abundance in both treatments. Both treatments also resulted in
increased abundance of transcripts of genes involved in fatty acid metabolism
(
Simulated herbivory, like solar UV-B, increased the abundance of
WRKY-2 transcripts. Also, as expected from previous
herbivore-challenged experiments
(Hermsmeier et al., 2001 Few genes were affected in opposite directions by solar UV-B and simulated herbivory. This is indicated by the paucity of data points in the northwest and southeast quadrants of Figure 3, A and B. A noteworthy case of opposite response was PI, which was strongly up-regulated by simulated herbivory (as expected) and down-regulated by solar UV-B in N. longiflora. More cases of opposite responses were found among the genes known to be specifically responsive to components of M. sexta oral secretions and regurgitates (regurgitate-responsive genes; Fig. 3C).
Insect elicitation commonly results in increased plant resistance to
subsequent herbivore attacks. This increased resistance can be measured using
standardized insect growth bioassays, and in the particular case of M.
sexta and N. attenuata, induction of plant defenses by
caterpillar attack has been detected with bioassays within 24 h after the
elicitation with JA (Pohlon and Baldwin,
2001
Simulated herbivory induced higher PI activity in N. attenuata, as
expected (Pohlon and Baldwin,
2001
In the bioassay with both Nicotiana spp., insects fed on plants that were exposed to simulated-ambient UV-B before and during the experiment grew less rapidly than their counterparts fed on control plants (Fig. 5). Because the insects themselves were not exposed to UV-B during the feeding trials, it is clear that the growth differences reflected changes in plant tissue quality induced by UV-B.
Our data provide a first glimpse into the transcriptional changes activated by solar UV-B in fieldgrown plants. The comparison in Figure 3 indicates that ambient UV-B induces a transcriptional reorganization in N. longiflora that has parallels with the response induced by caterpillar herbivory. This result suggests that UV-B and chewing insects activate common regulatory elements and that this signaling convergence ultimately leads to increased plant resistance to herbivore attack in plants exposed to solar UV-B radiation (Fig. 5).
Where do the UV-B- and caterpillar-induced signaling cascades converge? A
major obstacle in the quest for answers to this question is our very limited
understanding of the mechanisms of UV-B perception and signaling in plants.
Dedicated photoreceptors for red, far-red, blue, and UV-A radiation are well
characterized in plants; in contrast, no specific UV-B receptors have yet been
identified. Based on evidence from studies in other organisms, some plant
responses to UV-B are thought to be initiated by signals derived from
UV-B-induced DNA damage (Beggs and
Wellmann, 1994
Another potential point of overlap between UV-B- and herbivore-induced
defense responses may occur at the level of the generation of reactive oxygen
species (ROS). Work in tomato seedlings has shown that hydrogen peroxide
(H2O2) is generated systemically in response to wounding
and systemin, and this response is absent in def-1, a mutant impaired
in the octadecanoid pathway
(Orozco-Cárdenas and Ryan,
1999
As noted earlier, work on the Arabidopsis model also has provided evidence
for interactions between UV-B and oxylipin signaling. UV-B, provided against
backgrounds of low PAR, has been shown to induce the expression of the
defensin gene (PDF1.2), a gene known to be up-regulated by wounding
and JA (A.-H.-Mackerness et al.,
1999 Regardless of the precise way of interaction, our data suggest that one of the mechanisms whereby solar UV-B makes Nicotiana plants less suitable for insect consumers (Fig. 5) may be by supercharging the octadecanoid pathway, increasing the abundance of transcripts of oxylipin biosynthetic genes (Fig. 1). This effect of UV-B appears to result in higher PI accumulation upon herbivore attack in N. attenuata but not in N. longiflora (Fig. 4). N. longiflora produces very low PI levels, which suggests that other defense products, and not PI, are involved in UV-B- (and insect-) induced defenses in this species.
Many of the effects of solar UV-B on transcript abundance detected in our
experiments involved genes that have not been investigated before; therefore,
comparisons with other studies are difficult to establish. Transcriptional
responses to UV-B have been studied for several photosynthesis-related genes
in controlled-environment experiments. In all cases, previous results with pea
(A.-H.-Mackerness et al., 1996
There were also some apparent contrasts between the transcriptional
responses to UV-B that we detected and those obtained in previous studies. In
N. longiflora, we found down-regulation of PI in plants
exposed to solar UV-B (Fig. 1).
In tomato, PI expression increased in response to treatment with
germicidal UV-C (Conconi et al.,
1996
From an ecophysiological point of view, it is to some extent puzzling that
the effects of UV-B and caterpillar herbivory on certain functional categories
of genes are so similar (Fig.
3). This is particularly true in the case of photosynthetic genes
because the parallels between the challenges imposed by UV-B photons and
herbivore attack on the photosynthetic machinery are far from obvious. The
similar regulation by UV-B and simulated herbivory on genes for WRKY, FDGS,
molybdopterin synthase sulfurylase, PR1, and on various transcripts of unknown
function (Fig. 3) also resists
facile explanations. One possibility is that this similarity is only apparent
and that subtle differences in timing and relative changes in expression
levels of key genes are of central importance to define the functional
specificity of the transcriptional reorganization triggered by each particular
stimulus (for discussion, see Bowler and
Fluhr, 2000
Seed Sources and Germination
Seeds of the native plant Nicotiana longiflora Cav. were collected
from wild specimens growing near the La Falda lake, in the Punilla Valley
(Córdoba, central Argentina) and sown directly on agar plates for
germination. Nicotiana attenuata Torr. Ex W. (seven times inbred line
of seeds collected from the DI Ranch, Section T40S R19W, Utah) seeds were
soaked for 1 h in a GA3 (100 mM) + smoke solution (House
of Herbs, Passaic, NJ; Baldwin et al.,
1994
Our field experiments were located at the Dr. Miguel Culaciati Botanical Garden in Huerta Grande (31° south, Córdoba, central Argentina, within 5 km of the N. longiflora seed collection site). Seedlings were grown for 1 week in a greenhouse after transplanting, then transferred to the field plots and assigned to the experimental UV-B treatments. The individual pots were sunk into the recently cultivated soil of the plots to facilitate watering and avoid overheating of the root zone. There were three independent blocks of plants (replicates). During the period in the field (3 weeks), the plants were fertilized twice with 0.5 g of N:P:K per pot and watered twice daily to maintain the soil near field capacity. The experimental plants of N. longiflora were very similar in appearance to their wild relatives that occurred in moist areas near river banks or abandoned fields.
Seedlings (in individual 0.5-L pots) were grown for 4 weeks in a greenhouse in Buenos Aires (34° S), without supplemental lighting, and then transferred to the experimental UV-B treatments within the same greenhouse. There were three independent blocks of plants (replicates). During the period under the UV-B lamps (3 weeks), the plants were fertilized once with 0.5 g of N:P:K and watered daily to maintain the soil near field capacity. Peak PAR in the greenhouse was 1,400 µmol m–2 s–1; natural photoperiod varied between 12.5 and 13.5 h.
In the field, the plants were grown in 1- x 1.4-m plots covered with
clear plastic filters. The filters were of two types: clear polyester (Oeste
Aislante, Buenos Aires; 0.1 mm thick), which filtered out more than 90% of the
UV-B component of solar radiation (attenuated UV-B treatment); and
"Stretch" film (Bemis Co., Minneapolis; 0.025 mm thick), which has
very high transmittance in the UV-B region (near-ambient UV-B treatment). Both
films have very high transmittance in the UV-A and PAR regions of the spectrum
(for spectral scans and details, see Mazza
et al., 2000
In the greenhouse, the plants were randomly assigned to one of two
treatments: simulated ambient UV-B and no UV-B. UV-B radiation was obtained
with three UVB 313 fluorescent lamps (Q-Panel) filtered through one
0.13-mm-thick layer of cellulose di-acetate (JVC Plastics, Lemirada, CA) to
remove UV-C photons. In the no-UV-B treatment, the cellulose di-acetate film
was replaced by a 0.1-mm clear polyester sheet (which filtered out both UV-C
and UV-B). The cellulose di-acetate film was replaced every 4 d. The plants
were irradiated for 6 h each day, with the irradiation period centered at
solar noon. The biologically effective daily UV dose, calculated using the
generalized plant action spectrum of Caldwell
(1971
To simulate herbivore damage (microarray and PI determination experiments), three (third to fifth) fully expanded leaves of rosette stage plants of the attenuated UV-B plots were treated in all cases. Three rows of puncture wounds were created with a fabric pattern wheel on each side of the mid-vein and 20 µL per leaf of a 1:6 (v/v) dilution of Manduca sexta regurgitate collected from fourth instar caterpillars were applied to the fresh wounds (simulated caterpillar treatment).
Approximately 0.5 g of frozen tissue was ground in liquid N using a pestle and mortar. This was followed by the addition of 5 mL of extraction buffer (0.18 M Tris-HCl [pH 8.2], 0.09 M LiCl, 4.5 mM EDTA, and 1% [w/v] SDS) and 1.7 mL of phenol acid:chloroform (5:1 [v/v]). The frozen slurry was ground and then centrifuged (12,000g for 20 min at 4°C). The aqueous phase was then removed and nucleic acids precipitated by the addition of LiCl (final concentration 2 M). Samples were well mixed and nucleic acids precipitated overnight at 4°C. After the precipitation step, the samples were centrifuged (12,000g for 20 min at 4°C). The pellet was redissolved in 2 mL of water and 200 µL of AcONa followed by the addition of 5.5 mL of 100% (v/v) ethanol and precipitated at –20°C for 2 h. The samples were then centrifuged (12,000g for 30 min at 4°C), and the pellets were washed in 2 mL of 70% (v/v) ethanol and centrifuged (12000g for 20 min at 4°C). The pellets were dried and resuspended in water.
The method used to spot M. sexta- and regurgitate-responsive genes
and seven well-characterized N. attenuata control genes (PI,
HPL, PMT1, AOS, XET, WRKY,
3' region of LOX, and 5' region of LOX) onto
epoxy coated slides has been described by Halitschke et al.
(2003
The three treated leaves from each plant of the simulated caterpillar
treatment, three leaves per plant of equivalent nodal positions from unwounded
plants of the UV-B treatments, and three leaves per plant of unwounded plants
of the attenuated or no UV-B treatment were harvested 24 h after the simulated
caterpillar folivory and flash frozen in liquid N. In each experiment, there
were 12 individual plants for each treatment (four from each replicate block),
and leaves from the same treatment were pooled together for RNA extraction.
The UV-B- and simulated caterpillar-treated samples served as treatment (Cy3),
and the unperturbed, non-UV-B-exposed samples were labeled and hybridized as
controls (Cy5). mRNA isolation, labeling, determination of labeling
efficiency, and microarray hybridization were carried out as described
(Halitschke et al., 2003
Our criteria to assess the significance of the expression changes for a
given gene were: (a) a significant Student's t test value in the
comparison against ER = 1 (n = 4 replicate spots; P <
0.05), (b) a deviation of at least ±0.25 from ER = 1, and (c)
verification that criteria (a) and (b) were fulfilled by the ERs obtained for
both PCR fragments (i.e. ER1 and ER2). An arbitrary threshold was utilized for
two reasons: first, to account for normalization errors; and second, to
account for the fact that replicate data did not result from repeated
hybridizations with the same RNAs but from repeated probe spotting. An ER
calculated as a mean of replicate ERs and the use of statistically rigorous
criteria to evaluate within-array variance allowed us to use lower thresholds
with this polyepoxide microarray in comparison with the poly-Lys microarray
used in a previous study (Hui et al.,
2003
The UV-B and simulated caterpillar treatments and the leaf harvest
procedures were carried out as described above for the microarray experiments.
The simulated caterpillar treatment was applied in the early afternoon, and
leaves were harvested before and several times after elicitation and flash
frozen in liquid N. There were three replicates (three individual plants) per
treatment and time point. PI activity in leaf extracts were determined using
the method of Jongsma et al.
(1993
M. sexta eggs were obtained from the Entomology Department of North Carolina State University (Raleigh). Two neonate larvae were placed on each of 16 plants of N. longiflora, and 20 plants of N. attenuata were grown under greenhouse conditions (see above). The two caterpillars were placed on the same leaf (fourth–fifth fully expanded leaves of rosette stage plants). One-half of the plants of each species had received UV-B supplementation for at least 2 weeks before the caterpillars were placed on them, and one-half belonged to the no-UV-B control. The UV-B treatments continued during the feeding period (1 week). To prevent direct exposure of the caterpillars to UV-B, the host leaf in each plant was enclosed in a cotton gauze bag that had its upper side covered with aluminum foil. These bags were applied to UV-B-exposed and control plants. Caterpillars were weighted at the end of the experiment.
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third party owners of all or parts of the material. Obtaining any permissions will be the responsibility of the requestor.
We thank the Jardín Botánico and Dr. Miguel Culaciati for granting us access to the facilities in Huerta Grande. We are especially grateful to Johannes Stratmann for stimulating discussions on UV signaling; Carlos Mazza for assistance with the experiments and data analysis; Klaus Gase, Matthias Held, Thomas Hahn, and Susan Kutschbach for invaluable assistance in microarray hybridization, reading, and data analysis; and Jorge Zavala for practical advice on PI determinations. Received March 26, 2003; returned for revision April 15, 2003; accepted April 26, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.024323.
1 This work was supported by Agencia Nacional de Promoción
Científica y Tecnológica (grant to C.L.B. and A.L.S.), by the
Guggenheim Foundation (grant to C.L.B.), by the Max Plank Gesellschaft (grant
to I.T.B.), and by the Consejo Nacional de Investigaciones Científicas
y Técnicas (fellowship to M.M.I.). C.L.B. and A.L.S. are Investigators
of Consejo Nacional de Investigaciones Científicas y
Técnicas.
[w] The online version of this article contains Web-only data. The supplemental
material is available at
http://www.plantphysiol.org. * Corresponding author; e-mail ballare{at}ifeva.edu.ar; fax 54-11-4514-8730.
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ABSTRACT
RESULTS
), N metabolism
(
), carbohydrate and cell wall metabolism (x), membrane transport
(*), stress response and signaling (
), oxylipin synthesis (
), PI
(
), pathogen-responsive (
), M. sexta-responsive genes of
unknown function (
), and regurgitate-responsive genes of unknown function
(
). The complete list of the responses of all arrayed genes is
available as Supplemental Table I
(
-1,3-Glucanase mRNA is locally, but not
systematically induced in Nicotiana tabacum L. cv Bel W3 after ozone
fumigation. J Plant Physiol 148:
215–221
