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First published online February 15, 2008; 10.1104/pp.107.112326 Plant Physiology 146:1996-2007 (2008) © 2008 American Society of Plant Biologists
Influence of Green Leaf Herbivory by Manduca sexta on Floral Volatile Emission by Nicotiana suaveolens1,[W]Institute of Biological Sciences, Biochemistry, University of Rostock, 18059 Rostock, Germany
Plants have to cope with various abiotic and biotic impacts as a consequence of changing environments, which can impair their ability to sexually reproduce. The main objective of this study was to investigate whether green leaf herbivory, having one of the most hazardous biotic impacts, would have any direct effect on the production and emission of floral volatiles because volatiles are known to play a crucial role in pollination. Nicotiana suaveolens plants were challenged with Manduca sexta feeding on leaves, and alterations in the quality and quantity of the floral blend, shifts in emission patterns, and changes in expression patterns of the floral benzoic/salicylic acid carboxyl-methyltransferase were monitored in noninfested and infested plants. Leaves responded to larval feeding by herbivory-induced diurnal emission of semiochemicals, whereas the emission of floral volatiles remained unchanged in comparison to the noninfested control. Neither the volatile composition nor the quantity of components or the nocturnal emission patterns was altered. The mRNA and protein levels of the benzoic/salicylic acid carboxyl-methyltransferase, as well as its enzyme activity, also did not show any significant differences. These results indicate that metabolism in flowers at and postanthesis is an autonomous process and is independent of metabolic changes in green leaves. By this sustaining mechanism, N. suaveolens plants ensure sexual reproduction even under unfavorable conditions.
The emission of volatile organic compounds (VOCs) is a characteristic trait of flowers of most seed plants. Floral VOCs are part of pollination syndromes and thus represent a very crucial factor to ensure sexual reproduction (Pellmyr et al., 1991  ; Dobson, 1994, 2006; Pichersky and Gershenzon, 2002). However, plants are challenged by constantly changing abiotic and biotic environmental conditions that might affect a plant's capacity to invest in sexual reproduction (Euler and Baldwin, 1996; Carroll et al., 2001; García and Ehrlén, 2002). Besides direct impacts, like floral oviposition (Dufaÿ and Anstett, 2003) or floral herbivory (Leege and Wolfe, 2002; Röse and Tumlinson, 2004; Theis, 2006; Sanchez-Lafuente, 2007), flowers are mostly exposed to a changing environment as part of an entirely affected plant (Sampson and Cane, 1999; Carroll et al., 2001). One of the most deleterious biotic influences on plants is green leaf herbivory. Infested leaves respond with a complex defense strategy, including an immediate damage-induced de novo production and emission of volatiles that repels herbivores or attracts host-seeking parasites as well as prey-searching natural enemies of the plant plaguer (De Moraes et al., 1998; Röse et al., 1998; Paré and Tumlinson, 1999; Pichersky and Gershenzon, 2002; van Poecke and Dicke, 2004). Intraplant and interplant signaling mediated by herbivore-induced volatiles also triggers a defense response in noninfested parts of the plant or noninfested neighboring plants (Mattiacci et al., 2001; Baldwin et al., 2002; Röse and Tumlinson, 2005; Heil and Bueno, 2007). The most severe consequence of green leaf herbivory is the loss of photosynthetic capacity. Possible impacts on floral traits, like flower size (Steets and Ashman, 2004; Cole and Ashman, 2005; Ivey and Carr, 2005), flower number (Cresswell et al., 2001; Canto et al., 2004), morphology, and nectar production (Ornelas et al., 2004), a change in pollinator service (Steets and Ashman, 2004; Ivey and Carr, 2005), fruit and seed production (Ornelas et al., 2004), and progeny (García and Ehrlén, 2002), are rather well documented. However, little attention has been paid so far to the influence of green leaf herbivory on floral VOC production and emission.
The main objective of this study was to investigate whether green leaf herbivory treatment of Nicotiana suaveolens would interfere with its floral VOC production and emission. Manduca sexta (Sphingidae), as one of the most intensively investigated model insects, served as the herbivore. N. suaveolens is native to coastal areas of Southeastern Australia (Japan Tobacco Inc., 1994
Manifestation of Damage Due to Larval Feeding Larvae of M. sexta were reared on leaves of young N. suaveolens plants. Larvae hatched after approximately 4 d post egg positioning. The transfer to the plants used for analysis did not impair these young first instar larvae. Already a few hours after transfer, they resumed their activity and first signs of feeding were obvious. The larvae preferably stayed on the abaxial surface of the leaves. After 5 d, distinct feeding signs at the leaf margin and hole injuries could be observed. Every single plant of the batch was affected. Ten days of herbivory caused severe damage (Fig. 1 ).
Larvae-Infested Green Leaves Emit Herbivore-Induced Volatiles
Leaves of noninfested N. suaveolens plants consistently emitted fatty acid derivatives at very low concentrations (data not shown), whereas infested leaves (Fig. 2A
) emitted at least seven new VOCs as a reaction to larval herbivory (Supplemental Table S1). The main compounds identified were (Z)-3-hexenyl acetate, (E)-β-ocimene,
Fresh Weight of Flowers Does Not Change during Green Leaf Herbivory Under the chosen conditions of plant cultivation, the flowering period of an individual flower of N. suaveolens lasted, on average, for 6 d. The weight on the day of anthesis ranged between 70 and 80 mg per flower (Supplemental Fig. S1). Postanthesis, the flower weight increased during flower development from day 3 on, and flowers weighed, on average, 120 mg, but could reach, in a few cases, a weight of 160 to 170 mg per flower. The weight did not significantly differ in two consecutive flowering periods regardless of whether plants were noninfested or infested. Similar results were obtained when the flower weight was analyzed during ongoing larval feeding (Supplemental Fig. S2). Noninfested plants produced 2-d-old flowers that constantly weighed between 100 and 120 mg, which was not significantly influenced by the introduction of larvae and subsequent green leaf herbivory up to 10 d.
Flowers of noninfested N. suaveolens plants emitted a complex VOC mixture, which was dominated by the benzenoids benzyl benzoate, benzyl salicylate, methyl benzoate, and benzyl alcohol (Table I
). Cinnamic acid derivatives, as well as benzenoids like methyl salicylate, β-phenylethyl alcohol, p-cresol, and β-phenylethyl benzoate, terpenoids like 1,8-cineole and
Green Leaf Herbivory Does Not Alter the Amount and Emission Pattern of Floral VOCs Besides an influence on the quality of the floral blend, VOC amounts and emission patterns could be altered by green leaf herbivory. To address this presumption, the amounts of the main 15 components of the floral blend were quantified to compare (1) the total amount of these VOCs emitted over the whole flowering period of an individual flower; (2) the relative amounts of a single VOC within the floral VOC mixture; and (3) the emission pattern of major constituents. In two consecutive flowering periods, identical individuals of N. suaveolens plants yielded a similar total amount of the 15 main volatiles regardless of whether plants were noninfested or larvae infested (Fig. 3 ), which corresponded with independent control experiments comparing two consecutive flowering periods of identical noninfested plants (Supplemental Fig. S3). The relative percentage of these components within the floral VOC mixture also did not vary significantly (Fig. 4 ). The dominant component by far was benzyl benzoate, which represented 57% of the total amount in noninfested and 63% in larvae-infested plants. All other main components were equally consistently emitted during both flowering periods. Significant differences were only observed for the cinnamic acid derivatives. Larvae-infested plants emitted significantly less cinamaldehyde and cinnamyl alcohol compared to noninfested plants (Fig. 4, inset). However, these differences could also be observed in independent control experiments using noninfested plants in two consecutive flowering periods (Supplemental Fig. S4). Regardless of larval infestation, flowers of some N. suaveolens batches investigated did not emit cinnamic acid derivatives at all during one or the other flowering periods or emitted them at undetectable levels, which may explain this phenomenon (see also Supplemental Table S3).
The emission patterns of the four major floral VOCs benzyl benzoate, methyl benzoate, benzyl salicylate, and benzyl alcohol for noninfested plants and infested plants are shown in Figure 5 . Both patterns were similar. The emission of these four volatiles peaked between midnight and 6 AM. Flowers already released considerable amounts of benzoic acid esters on the first day postanthesis, but maximal emission was reached between days 2 and 4 postanthesis. The emission of benzyl alcohol gradually increased up to its maximum on day 4. On day 5 postanthesis, the emission of all four volatiles declined, and on day 6 only very small amounts were detectable. Noninfested independent control plants exhibited almost identical oscillation characteristics in two consecutive flowering periods (Supplemental Fig. S5), leading to the conclusion that the emission pattern of floral VOCs also remained uninfluenced by green leaf herbivory.
Floral and Herbivore-Induced  -Farnesene Display an Opposite Emission Pattern
The sesquiterpene
Green Leaf Herbivory Does Not Significantly Influence the Expression Characteristics of the Floral BSMT In addition to monitoring the methyl benzoate emission (Fig. 5), a comparative analysis of the relative values of the bsmt transcript level, protein level of BSMT, and BSMT enzyme activity was performed to gain an overall insight into the BSMT expression status at the molecular level. Flowers of noninfested and larvae-infested plants displayed similar transcript, protein, and activity levels as well as expression patterns (Fig. 7 ). High amounts of the bsmt transcript could only be found in young flowers. The maximal daily oscillation was reached around 6 PM (Fig. 7A). The BSMT protein levels did not exhibit pronounced oscillation (Fig. 7B), whereas the BSMT activity showed weak nocturnal oscillation (Fig. 7C). The protein level and enzyme activity quickly increased in young flowers. On days 5 and 6 postanthesis, the BSMT protein level decreased noticeably. These characteristic expression patterns were, in general, also found in independent control experiments using noninfested plants in two consecutive flowering periods (Supplemental Fig. S6).
Investigating flowers of the same age, it could be demonstrated that, at up to 10 d of larval feeding, the three parameters of BSMT expression also remained unaltered. As shown in Figure 8 , 2-d-old flowers of noninfested plants exhibited similar transcript levels, protein levels, and enzyme activities on several subsequent days. After the introduction of larvae and ongoing green leaf herbivory, the daily reassessment of BSMT expression levels did not reveal any tendency toward decline or increase. Differences in noninfested plants could be noticed at some time points, but they were never consistent. The BSMT protein levels were very similar and the bsmt transcript levels and enzyme activities supported the same trend.
In conclusion, the molecular analysis of BSMT expression supported the results obtained from investigations of VOC emission. Green leaf herbivory did not provoke changes in floral VOC production, as demonstrated for methyl benzoate.
To investigate the impact of green leaf herbivory on floral scent production and emission, the tobacco N. suaveolens was infested with M. sexta larvae. This sphingoid moth is a well-characterized and widely used organism in animal and plant sciences. Native host plants are Nicotiana attenuata (Voelckel and Baldwin, 2004 ), Datura wrightii (Mira and Bernays, 2002), and the more recently discovered nonsolanaceous Proboscidea parviflora (Martyniaceae; Mira and Bernays, 2002), but as an oliphagous specialist, M. sexta accepts solanaceous plants in general (del Campo and Renwick, 1999; Voelckel and Baldwin, 2004). However, to assess and compare the susceptibility to M. sexta, the green leaf response of N. suaveolens was scrutinized. To adapt M. sexta larvae to N. suaveolens right from the beginning of the experiment (del Campo and Renwick, 2000) and to minimize stress due to diet change, eggs and hatchling larvae were kept off an artificial diet but reared on N. suaveolens. Infested leaves of N. suaveolens responded with the de novo synthesis of (E)-β-ocimene, -bergamotene, and - and β-farnesene as well as (Z)-3-hexenyl acetate and traces of (Z)-3-hexenyl butanoate and β-linalool, indicating that, in our experiments, the plant responded to larval herbivory. Interestingly, the composition of the mixture of these semiochemicals was similar, but not identical, to that of the VOC mixture induced by larval feeding of Manduca quinquemaculata on leaves of N. attenuata (Kessler and Baldwin, 2001). N. attenuata additionally emitted (Z)-3-hexenol and methyl salicylate, the latter in very small amounts. -Farnesene was not present. This similarity of emitted compounds in both Nicotiana species is quite striking and supports the hypothesis that foliar feeding of M. sexta larvae or other herbivores triggers a specific set of semiochemicals in Nicotiana species (Kessler and Baldwin, 2001).
The diurnal rhythms of herbivory-induced green leaf VOCs has been frequently described (Loughrin et al., 1994
Green leaves of N. suaveolens responded with the well-known phenomenon of emission of semiochemicals as an immediate reaction to green leaf herbivory of M. sexta. The central question of this study was, however, whether the floral VOC production/emission would be comparably susceptible. The elucidation of nocturnally emitted floral volatiles from noninfested N. suaveolens plants resulted in the detection of 50 compounds. Most of the previously reported compounds (Loughrin et al., 1990
Based on the first scenario, the floral metabolism could be influenced by green leaf herbivory due to the loss of photosynthetic source tissue and subsequent insufficient supply of sinks with photosynthates and/or impaired translocation of photosynthates. The latter has been shown for silverleaf whitefly infestations, whose feeding on leaves caused reduced photosynthate export from source tissues (Lin et al., 2000
A second scenario would include a floral response as a consequence of the plant's adaptation to a changing biotic environment and would imply intraplant and/or interplant signaling between leaves and flowers similar to the signaling between vegetative organs (Gershenzon, 2007 To summarize, the results of this work indicate that, despite considerable damage of green leaf tissue by M. sexta, N. suaveolens plants retained the quality of the VOC composition as well as the quantity and emission patterns of their floral VOCs. There was no immediate floral response or delayed interference with the floral VOC production/emission due to green leaf herbivory. Within the time frame investigated, the plant's capacity to invest in VOC production and emission remained unchanged. The pattern of photosynthate allocation between green leaf source tissue and sink tissues, like roots, and the developing flower as well as the ability to assimilate storage in petal cells, might play a key role in this phenomenon. VOC emission would probably only be affected if adequate accumulation and storage of photosynthates in petal tissues failed prior to anthesis.
Plant Material and Growth Conditions
Seedlings of Nicotiana suaveolens Lehmann (Solanaceae) were raised on vermiculite (Deutsche Vermiculite Dämmstoff GmbH) in a growth room (temperature, 20°C ± 2°C; photoperiod, 16/8 h; illumination, 150 µmol m–2 s–1). At the onset of flowering, plants were transferred to the analysis plant chamber with a headspace collection device (temperature, 24°C ± 1°C; photoperiod, 14/10 h; illumination, 100 µmol m–2 s–1). Plants were watered with Hoagland solution (Hoagland and Aronon, 1938
Eggs of Manduca sexta (Lepidoptera, Sphingidae), kindly provided by Markus Huss (University of Osnabrück, Germany), were placed on leaves of young N. suaveolens plants and incubated at 27°C and a photoperiod of 16/8 h. Larvae hatched after 3 to 4 d. These young first instar larvae were used for experiments.
Influence of Larval Leaf Damage on Floral VOC Emission and BSMT Expression Floral VOCs were collected and analyzed according to the flowering time of individual flowers, starting with the first collection interval from 6 PM to midnight on the day of anthesis. For the next 6 d, flowers were labeled on their day of anthesis. On day 6, two to eight flowers of every age (day of anthesis to 6 DPA) were harvested at 6 AM, noon, 6 PM, and midnight. Flowers were weighed and divided. The two halves were separately pooled and used for protein and RNA extraction to assess BSMT activity and amounts as well as bsmt mRNA levels. The tissue for protein extraction was processed and immediately used for activity assays. Aliquots of the crude protein extracts were then stored at –70°C for subsequent use in dot-blot western experiments. The tissue for RNA extraction was immediately submerged into liquid nitrogen and stored at –70°C until processing. After the last collection interval of flowering period 1, new buds were inserted into glass containers and flowering period 2 was investigated. In case of use of infested plants during flowering period 2, six to 10 first instar M. sexta larvae were placed onto young rosulate leaves of each plant at 6 PM on the day of flower anthesis. Floral VOCs were collected starting with the first interval (6 PM to midnight) on the day of anthesis. Again, for the next 6 d, flowers were labeled on their day of anthesis, harvested, and processed as described above. Analysis of BSMT Expression in Flowers of the Same Age during the Progression of Larval Damage. The accumulation of bsmt transcripts (northern-blot analysis), BSMT amounts (western dot-blot analysis), and BSMT activities was investigated using flowers of the same age (2 DPA). Eight- to 12-week-old N. suaveolens plants that had started flowering were adapted to the conditions of the analysis plant chamber. Two-day-old flowers (two to seven) were harvested for several days at midnight, 6 AM, noon, and 6 PM, weighed, and divided. The halves were separately pooled and processed for protein and RNA extraction as described above. Thereafter, five to 13 first instar larvae of M. sexta were distributed at 6 PM on young rosulate leaves of each plant of the batch and the test series was subsequently conducted. Again, 2-d-old flowers were harvested at midnight, 6 AM, noon, and 6 PM for up to 10 d while larval feeding was ongoing. Flowers were weighed, divided, and processed as described above. The VOC collections were replicated six times (n = 6). The corresponding control measurements using noninfested plants in both consecutive flowering periods were carried out in triplicate (n = 3). The investigations of bsmt transcript accumulation, BSMT amount, and BSMT activity were performed in duplicate.
Analysis of VOCs Emitted from Leaves during Larval Herbivory
Sampling and accumulation of VOCs of N. suaveolens flowers were performed with an open loop system as described by Heath and Manukian (1994) To collect headspace VOCs emitted from the leaves of N. suaveolens, the setup was slightly modified. The glass containers were adapted to the oblanceolate shape of the leaves (Ø 6 cm, length 14 cm), with the leaf inlet on one side, the air inlet on the opposite, and the air outlet on the top of the glass container. VOCs of two containers were combined to yield one green leaf VOC sample. Because flowers were analyzed in parallel, independent floral and green air flows were established. Each flow was supplied with charcoal-purified air delivered by aquarium pumps (1.1 L min–1). Volatile-enriched air was sucked over the trap using membrane pumps (Riechle), which provided a constant flow of 0.7 L min–1. Time-controlled sampling allowed two collection periods of 12 h/d for 5 d.
Samples were analyzed using a GC-MS-QP5000 from Shimadzu (70 eV; Kyoto) equipped with a DB5-MS column (60 m x 0.25 mm x 0.25 µm; J&W Scientific). Splitless liquid injection of 1 µL of sample was performed at 200°C with a sampling time of 2 min using a CTC autosampler (CTC Analytics). The initial column temperature was set at 35°C, followed by a ramp of 10°C min–1 up to 280°C, with a final hold for 15 min at 280°C. Helium was used as the carrier gas. The column flow was set at 1.1 mL min–1, with a linear velocity of 28 cm–1. Mass spectra were obtained using the scan modus (total ion count, 40–280 m/z). The confirmation of compound identity was done by comparison of mass spectra and retention times with those of available authentic standards or essential oils, by comparison of retention indices (Kovats indices), and by comparison of obtained spectra with spectra in the library of the National Institute of Standards and Technology (NIST147).
RNA was extracted as described by Chang et al. (1993) Hybridization was performed at 50°C in DIG-Easy-Hyb (Roche Diagnostics) overnight. After washing in 2x SSC (0.3 M NaCl, 30 mM sodium citrate, 0.1% [w/v] SDS, pH 7.0) at room temperature for 3 x 5 min and in 0.1x SSC (15 mM NaCl, 1.5 mM sodium citrate, 0.1% [w/v] SDS, pH 7.0) at 50°C (55°C for 18S probe) for 2 x 15 min, the membranes were incubated with anti-DIG antibodies linked to alkaline phosphatase (Roche Diagnostics) and subsequently with CDP-Star (Roche; 0.25 µM) in the dark. They were then exposed to the luminescent image analyzer LAS-1000 (Fujifilm), and the luminescence was read for 30 to 40 min (5–10 min for 18S probe). Quantification was performed using the appending Fujifilm Image Gauge software.
Crude floral protein extracts were prepared as described by Wang et al. (1997)
The enzyme assay was performed according to Wang et al. (1997)
The bsmt gene was amplified by reverse transcription-PCR and cloned into the vector pET101/D-TOPO (Invitrogen), which carries a C-terminal hexa-His (Pott et al., 2004
Western-blot experiments were performed using the dot-blot technique. Crude native protein extracts were spotted onto a nylon membrane (Roche Diagnostics; 3 µg/dot) using a dot-blot device. The membrane was treated for at least 2 h with blocking solution containing 1% (v/v) blocking reagent (Roche Diagnostics) in maleic buffer (0.1 M maleic acid, 0.15 M NaCl, pH 7.5). After a 2-h incubation with the BSMT-specific antibody diluted 1:10,000 in Tris-buffered solution containing 0.05% (v/v) Triton X-100 (TBS-T) and repeated washing with TBS-T, the membrane was incubated with the secondary anti-rabbit alkaline phosphatase-conjugated antibody (Sigma-Aldrich; diluted 1:20,000 in TBS-T) and again washed with TBS-T and TBS. The membrane was then equilibrated in detection buffer (100 mM Tris-HCl, 100 mM NaCl, 50 mM MgCl2) and incubated with CDP-Star (Roche; 0.25 µM in detection buffer) in the dark. Luminescence was read and quantified using the luminescent image analyzer LAS-1000 and the appending Fujifilm Image Gauge software (Fujifilm).
VOCs were quantified per flower and per sampling interval. For total amounts, VOC amounts of the entire flowering period of an individual flower were summarized. Assessment of significance of floral VOC emission between noninfested and infested plants was performed using the Wilcoxon-Mann-Whitney test ( Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number AJ628349.
The following materials are available in the online version of this article.
We wish to thank Markus Huss (Animal Physiology, University of Osnabrück, Germany), who kindly provided M. sexta eggs; Sandra Saschenbrecker and Anja Vespermann for preliminary studies; and Hubert Bahl (Microbiology, University of Rostock) for helpful discussion. Received November 2, 2007; accepted February 7, 2008; published February 15, 2008.
1 This work was supported by the Deutsche Forschungsgemeinschaft (grant to B.P.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Uta Effmert (uta.effmert{at}uni-rostock.de).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.112326 * Corresponding author; e-mail uta.effmert{at}uni-rostock.de.
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ABSTRACT
RESULTS
, 
, 
, (E)-β-ocimene; 
, (Z)-3-hexenyl acetate. A sampling period of 3 d served as the noninfested control (–d 3 to –d 1). First instar larvae of M. sexta were introduced on day 0 at noon (
). Volatiles were collected for the following 5 d. Time-controlled sampling allowed two collection intervals per day. n = 2; data = means ± difference.
) in two consecutive flowering periods. For infestation, first instar M. sexta larvae were introduced to green leaves at 6 PM on the day of anthesis. d 0 = day of anthesis; n = 6; data = means ± SE.
) volatiles of noninfested plants were sampled for 3 d (–d 3 to –d 1). First instar larvae of M. sexta were introduced on day 0 at noon (
) and floral (
