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First published online April 6, 2007; 10.1104/pp.107.097543 Plant Physiology 144:1223-1232 (2007) © 2007 American Society of Plant Biologists
Sebacina vermifera Promotes the Growth and Fitness of Nicotiana attenuata by Inhibiting Ethylene Signaling1,[W]Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Beutenberg Campus, 07745 Jena, Germany
Sebacina vermifera, a growth-promoting endophytic fungus, significantly increases Nicotiana attenuata's growth but impairs both its herbivore resistance and its accumulation of the costly, jasmonic acid (JA)-regulated defense protein, trypsin proteinase inhibitor (TPI). To determine if the fungi's growth-promoting effects can be attributed to lower TPI-related defense costs, we inoculated transformed N. attenuata plants silenced in their ability to synthesize JA, JA-isoleucine, and TPI by antisense (lipoxygenase 3 [as-lox3] and Thr deaminase [as-td]) and inverted repeat (ir-tpi) expression, and found that inoculation promoted plant growth as in untransformed wild-type plants. Moreover, herbivore-elicited increases in JA and JA-isoleucine concentrations did not differ between inoculated and uninoculated wild-type plants. However, inoculation significantly reduced the morphological effect of 1-aminocyclopropane-1-carboxylic acid on wild-type seedlings in a triple response assay, suggesting that ethylene signaling was impaired. Furthermore, S. vermifera failed to promote the growth of N. attenuata plants transformed to silence ethylene production (1-aminocyclopropane-1-carboxylic acid oxidase [ir-aco]). Inoculating wild-type plants with S. vermifera decreased the ethylene burst elicited by applying Manduca sexta oral secretions to mechanical wounds. Accordingly, oral secretion-elicited transcript levels of the ethylene synthesis genes NaACS3, NaACO1, and NaACO3 in inoculated plants were significantly lower compared to these levels in uninoculated wild-type plants. Inoculation accelerated germination in wild-type seeds; however, uninoculated wild-type seeds germinated as rapidly as inoculated seeds in the presence of the ethylene scrubber KMnO4. In contrast, neither inoculation nor KMnO4 exposure influenced the germination of ir-aco seeds. We conclude that S. vermifera increases plant growth by impairing ethylene production independently of JA signaling and TPI production.
Plants that associate with beneficial rhizosphere microorganisms, which include symbiotic and other endophytic and free-living rhizobacteria, often grow better than plants that don't (Glick, 1995  ; Varma et al., 1999; Strack et al., 2003; Barazani et al., 2005; Waller et al., 2005). The symbiotic associations of plants with arbuscular mycorrhizae (AM), ectomycorrhizal fungi, and nitrogen-fixing bacteria are referred to as mutualistic interactions. Symbiotic fungi or bacteria benefit from the plants' carbohydrates, while plants benefit when the supply of more stationary nutrients such as nitrogen, phosphorus, calcium, magnesium, zinc, copper, and iron is increased. The sequence of events that leads to the development of symbiotic association involves regulating defense-related genes, which have been characterized during the early establishment of AM symbiosis (Kapulnik et al., 1996; Garcia-Garrido and Ocampo, 2002; Liu et al., 2003; Balestrini and Lanfranco, 2006). In addition, phytohormones, usually associated with plants' responses to biotic stresses, were shown to play a role in mycorrhizal development. In Allium sativum, for example, treatment with jasmonic acid (JA) was shown to stimulate mycorrhizal development (Regvar et al., 1996), and JA and its conjugated form JA-Ile accumulated in the roots of barley (Hordeum vulgare) colonized with Glomus intraradices (Hause et al., 2002). Furthermore, silencing the allene oxide cyclase gene, which encodes allene oxide cyclase, an enzyme of the JA biosynthesis pathway, suppressed AM colonization (Isayenkov et al., 2005), suggesting that jasmonates are associated with establishment of a strong carbon sink in the roots (Hause et al., 2002; Strack et al., 2003). In contrast, the mycorrhization of tobacco (Nicotiana tabacum) with G. mosseae reduced salicylic acid (SA) levels in the plant, and colonization by the fungus was suppressed by constitutive SA synthesis (Medina et al., 2003).
In addition to establishing symbiotic associations, plants are associated with a diverse range of free-living microorganisms that increase plant performance (Glick, 1995
Recently, we reported that P. indica and its genetically related species Sebacina vermifera increase the growth and fitness of Nicotiana attenuata (Barazani et al., 2005 Here we falsify this hypothesis with plants transformed in their ability to produce TPIs and in two steps in the JA signaling cascade required to elicit TPI production and demonstrate that S. vermifera's growth-promoting effects result from alterations in ethylene signaling. We show that: (1) increases in plant performance related to the fungus are independent of JA and TPI, but depend on the ability of the plant to produce ethylene; (2) the beneficial effects of S. vermifera on seed germination and seedling growth are ethylene dependent; and (3) the OS-induced ethylene emission and increased transcript accumulation of ethylene biosynthesis genes are reduced in S. vermifera-inoculated plants compared to uninoculated plants.
TPI Activity and Transcript Accumulation Is Suppressed in OS-Elicited Inoculated Plants TPI activity in OS-elicited rosette-stage leaves, 72 h after OS elicitation was nearly twice as high in uninoculated plants compared to S. vermifera-inoculated N. attenuata wild-type plants (Fig. 1 ). This significant (t test, F1,6 = 6.67; P = 0.04) difference in defense metabolite deployment was also detectable at the transcriptional level 6 h after elicitation (Fig. 1, inset). In response to OS elicitation, TPI transcripts accumulated more rapidly in uninoculated plants than in inoculated wild-type plants (t test, F1,6 = 7.63; P = 0.04).
Growth Promotion by S. vermifera Is Unaffected in JA-, JA-Ile-, or TPI-Silenced Plants Next we determined whether the growth-promoting effect of S. vermifera resulted from the attenuation of the growth-related costs of TPI production or from the jasmonate signals that elicit TPI. We compared stalk length of inoculated and uninoculated wild-type plants and plants transformed with antisense (as) and inverted repeat (ir) constructs of lipoxygenase 3, Thr deaminase, and TPI to silence JA, JA-Ile, and TPI levels, respectively. S. vermifera inoculation significantly increased stalk lengths of wild-type plants (ANOVA with repeated measures, F1,23 = 76.85; P < 0.01). At the end of the growth phase, 56 d after germination, inoculated wild-type plants were 6.7% taller (t test, F1,28 = 10.03; P < 0.01) than uninoculated plants (Fig. 2A ). In addition, inoculated wild-type plants started to flower 1 d earlier than uninoculated plants, a difference that was highly significant (Fig. 2A; t test, F1,27 = 11.79; P < 0.01).
Similarly, S. vermifera significantly increased the stalk lengths of as-lox3 and as-td transformed plants (Fig. 2, B and C; ANOVA repeated measures; as-lox3: F1,23 = 107.60, P < 0.01; as-td: F1,19 = 63.22, P < 0.01). S. vermifera-inoculated as-lox3 and as-td plants started to flower 1 to 2 d earlier (Fig. 2, B and C; t test as-lox3: F1,28 = 21.14; P < 0.01; as-td: F1,28 = 12.39; P < 0.01), and at the end of the growth phase, S. vermifera-inoculated as-lox3 and as-td plants were 6.7% and 3.1% taller than uninoculated plants, respectively (Fig. 2, B and C; t test, as-lox3: F1,28 = 21.14; P < 0.01; as-td: F1,25 = 4.79; P = 0.03). These results demonstrate that the growth-promoting effects are independent of the jasmonate signaling required to elicit herbivore defenses in N. attenuata. Similar results were found in trials with ir-tpi plants. Inoculation significantly increased the growth of the inoculated transformed plants (Fig. 2D; ANOVA with repeated measures, F1,23 = 84.04; P < 0.01) so that the final stalk lengths of S. vermifera-inoculated ir-tpi plants were 6.5% taller than those of uninoculated plants (t test, F1,28 = 13.40; P < 0.01). The day flowering began did not differ between the two inoculation treatments (Fig. 2D; t test, F1,28 = 0.18; P = 0.67). We conclude that the growth-promoting effects of S. vermifera cannot be attributed to an alleviation of the fitness costs of TPI production.
Applying OS to wounded leaves elicits a dramatic JA burst that occurs in concert with a JA-Ile burst (Kang et al., 2006
S. vermifera Inoculation Interferes with Ethylene Signaling Independently of 1-Aminocyclopropane- 1-Carboxylic Acid Deaminase Activity
The triple response assay is a rapid means of estimating the sensitivity of plants to ethylene and has been successfully used to identify ethylene-insensitive mutants (Ecker, 1995
To determine whether the above effects are related to the ability of the fungus to degrade ACC by secreting ACC deaminase, the activity of the enzyme was assayed by measuring the amount of  -ketobutyrate produced during ACC cleavage (Penrose and Glick, 2003). By comparing the absorbance of the -ketobutyrate standard curve to the samples we found no evidence for ACC deaminase activity in cultures of S. vermifera, suggesting that the reduced inhibitory effect is not related to the fungus' use of ACC as a nitrogen source.
The altered growth performance of S. vermifera-inoculated seedlings observed in the triple response assay may be due to changes either in ethylene biosynthesis or in its perception. To examine how inoculation affects ethylene biosynthesis, we first compared the performance of inoculated and uninoculated N. attenuata plants transformed to silence ACC oxidase (ACO) expression in ir constructs (ir-aco). S. vermifera did not increase the performance of inoculated ir-aco plants as it did with wild-type plants. Stalk lengths of ir-aco plants were also not influenced by inoculation with S. vermifera (Fig. 5A ; ANOVA with repeated measures P > 0.05). However, at the end of the growth phase, uninoculated ir-aco plants were 31.8% taller than uninoculated wild-type plants (compare Figs. 2A and 5A; t test, F1,27 = 161.85; P < 0.01). We therefore hypothesized that S. vermifera's ability to reduce ethylene synthesis in inoculated wild-type, as-lox3, as-td, and ir-tpi plants was the reason for the increased growth performance of inoculated plants.
In the triple response assay, ACC significantly inhibited the root and hypocotyl growth of ir-aco seedlings by 79.5% and 75.7%, respectively (Fig. 5B; root: t test, F1,6 = 21.04; P < 0.01; hypocotyl: t test, F1,6 = 3.43; P < 0.01). This demonstrates that ir-aco plants still harbor sufficient ACO activity to induce a triple response. However, the inhibitory effect of ACC on both roots and hypocotyls was significantly reduced by preinoculation with S. vermifera (Fig. 5B; multiple comparisons with Student-Newman-Keuls test, P  0.05). These results are consistent with the hypothesis that the fungus inhibits ethylene production in plants. To test this hypothesis, we compared the amount of ethylene produced in response to OS elicitation in inoculated and uninoculated plants. Measurements of ethylene emission from OS-elicited leaves revealed that uninoculated plants emitted 1.4 times more ethylene than did S. vermifera-inoculated plants (Fig. 6
, inset; t test, F1,14 = 8.91; P < 0.01).
To learn how the fungus inhibits ethylene production, we measured the transcript accumulation of N. attenuata's ethylene biosynthetic genes by quantitative reverse transcription-PCR. OS elicitation in both uninoculated and inoculated plants resulted in the rapid accumulation of NaACS3a (ACC synthase) transcripts, the first committed step of ethylene biosynthesis. Maximum transcript levels attained were not influenced by inoculation (t test, F1,8 = 0.01; P = 0.90). Six hours after OS elicitation, NaACS3a levels began to decrease; final transcript levels of inoculated plants were significantly lower than those of uninoculated plants (Fig. 6; t test, F1,6 = 7.39; P = 0.03). In addition, we measured the transcript levels of three ACO genes, which are involved in the second committed step of ethylene biosynthesis. Compared to transcript levels in uninoculated plants, those in inoculated plants of NaACO1 and NaACO3 were significantly reduced following OS elicitation: by 1.9-fold after 2.5 h and 3.0-fold after 6 h, respectively (Fig. 6; NaACO1 at 2.5 h: t test, F1,7 = 16.72; P < 0.01; NaACO3 at 6 h: t test, F1,8 = 8.34; P = 0.02). No differences between the two inoculation treatments were measured in NaACO2 transcripts (Fig. 6). Unlike levels of ethylene biosynthetic genes, levels of the ethylene receptor gene NaETR1 were not affected by either OS elicitation or fungal inoculation (Supplemental Fig. S1).
Whereas the germination of wild-type seeds on S. vermifera-inoculated media was significantly higher (85%; t test, F1,5 = 9.54; P = 0.03) than on uninoculated media (53%; Fig. 7 ), the germination rate (70%) of ir-aco seeds was not influenced by the presence of the fungi (Fig. 7). The presence of the ethylene scrubber, KMnO4, increased the germination rates of uninoculated wild-type seeds to the level found in S. vermifera-inoculated seeds (t test, F1,6 = 5.85; P = 0.05). KMnO4 had no effect on the germination of inoculated and uninoculated ir-aco seeds (Fig. 7). These results are consistent with the hypothesis that reducing ethylene in the headspace of germinating seeds accelerates germination and that inoculating plants with S. vermifera reduces the amount of ethylene seeds produced during germination.
S. vermifera (Sebacinales) increases the performance of N. attenuata plants by down-regulating ethylene production. Previously we showed that the association of S. vermifera increased the performance of inoculated N. attenuata. This growth benefit was accompanied by a decreased resistance to attack from M. sexta larvae, which could be attributed to the down-regulation of TPIs (Barazani et al., 2005 ). Here we show that the association with S. vermifera also reduces the transcript levels of NaTPI (Fig. 1, inset). Since the production of defense compounds provides a fitness benefit when plants are exposed to herbivores, but exacts fitness costs from the plant under normal growth conditions (Zavala et al., 2004a, 2004b), growth promotion by S. vermifera could have resulted from reducing the costs of TPI production. However, inoculating transformed lines of N. attenuata impaired in their expression of NaTPI (ir-tpi) increased their growth performance just as it did in wild-type plants (Fig. 2, A and D). This indicates that the beneficial effects of S. vermifera are not solely the result of down-regulating TPIs. Furthermore, ir-tpi plants flowered earlier than wild-type plants, and the flowering time of ir-tpi plants did not differ between the two inoculation treatments (Fig. 2D). Fitness benefits have been associated with the silencing of TPIs under constitutive conditions (Zavala et al., 2004a); these beneficial effects might be stronger than any effect of S. vermifera inoculation. Therefore, we cannot exclude the possibility that earlier flowering time of S. vermifera-inoculated plants might be partially caused by down-regulating TPIs.
In addition to their effect on the nutritional status of a plant, its primary metabolism, and the plants' tolerance to stress, beneficial microorganisms can increase plant growth by modifying endogenous phytohormone levels in the plant (Smith and Read, 1997
O'Donnell et al. (1996)
We further hypothesized that plants decrease their ethylene production when inoculated with S. vermifera. When ACC was added to germinating seedlings, the fungus inhibited the triple response of inoculated seedlings of both wild-type and ir-aco plants (Figs. 4 and 5B). In addition, oxidizing ethylene with a KMnO4 ethylene scrubber mimicked the effect of S. vermifera on the germination of wild-type seeds (Fig. 7), providing further evidence that the fungus promotes growth by manipulating ethylene production. Several beneficial microorganisms modify ethylene production by metabolizing ACC and synthesizing and secreting ACC deaminase; the cleaved ACC can then be utilized as a nitrogen source by the fungus, and by reducing ethylene production in host plants, growth is promoted (Penrose and Glick, 2003
Several other reports have demonstrated the beneficial effects of P. indica on different plant species (Sahay and Varma, 1999
Plant Performance
Seeds of an inbred line of Nicotiana attenuata Torr. ex. Wats. (synonymous with Nicotiana torreyana Nelson and Macbr.; wild type) as well as of several genetically transformed as and ir lines, as-lox3 A-300-1 (Halitschke and Baldwin, 2003
Petri dishes were either preinoculated with Sebacina vermifera or left sterile. An axenic culture of S. vermifera (received from P. Franken, Max Planck Institute for Terrestrial Microbiology) was used to inoculate GB5 plates by preincubation in the dark at 26°C for 8 d (Barazani et al., 2005
Creating standardized puncture wounds and immediately applying Manduca sexta larvae OS to the puncture wounds precisely mimics the transcriptional (Roda et al., 2004
To determine TPI activity, leaf samples were harvested 3 d after OS elicitation, frozen in liquid nitrogen, and stored at –80°C until further processing. Samples were analyzed for TPI activity in an agar diffusion assay as described in van Dam et al. (2001)
Leaf samples for hormone analysis were harvested at the indicated time points following OS elicitation. Approximately 300 mg of harvested leaf tissue were homogenized in 1 mL ethyl acetate spiked with 200 ng mL–1 [13C2] JA and para chlorogenic acid, as internal standards for JA and JA-Ile, respectively. After centrifugation at 13,000 rpm for 20 min at 4°C, extraction was repeated with 1 mL ethyl acetate. The supernatants were combined and evaporated until dryness. The dried residue was redissolved in 500 µL 70% (v/v) methanol. Prior to analysis the samples were centrifuged for 10 min at 13,000 rpm and 15 µL of the supernatant was analyzed using a Varian 1200 L triple quadrupole mass spectrometer. For the HPLC, a Pursuit C8 column (150 mm x 2.0 mm, 3 µm particle size) was used and a gradient of water and methanol, both including 0.05% (v/v) formic acid, was the mobile phase with a flow rate of 0.2 mL min–1. The mass spectrometer was operated in negative electrospray ionization mode with an argon pressure of 0.279972 Pa (=2.1 mTorr) in the collision cell. A capillary voltage of –3,200 V, a shield voltage of 600 V, and a detector voltage of 1,800 V was used. The pressure of the drying gas (N2) was 131,005 Pa (=19 psi) at 300°C and that of the nebulizing gas (air) was 379,225 Pa (=55 psi). The most abundant and characteristic fragment ion was chosen for quantification.
Ethylene emission was measured continuously and noninvasively in real time with a laser photoacoustic spectrometer. The light source consisted of a line-tunable infrared laser and the detection device was a resonant photoacoustic cell (INVIVO). For a detailed description, see von Dahl et al. (2007)
We used the triple response assay to measure the effect of ACC supplementation and hence, ethylene, on the growth of uninoculated and S. vermifera-inoculated wild-type and ir-aco seedlings. Square (12 cm2) petri dishes were filled with 80 mL of GB5, with or without 5 µM ACC (Fluka, Sigma), and the solidified agar was portioned out into two plates. Seeds (sterile or preinoculated with S. vermifera) were placed on the agar to germinate. The plates were stored vertically in an incubator (26°C with an 11:13 h day/night cycle); after 3 d, when the radicles emerged, the light was turned off and seedlings were grown in the dark. Each inoculation and ACC treatment consisted of four plates each with 15 seedlings. After 10 d, the lengths of roots and hypocotyls were measured.
An ethylene scrubber (KMnO4) was used to test the role of ethylene in S. vermifera-mediated effects (Jayaraman and Raju, 1992
Measurement of ACC deaminase activity was performed following Penrose and Glick (2003)
Fully mature leaves (at nodal position +1) of rosette-stage plants were elicited with OS as described above. Leaves were collected at different time points after the elicitation (for ethylene biosynthesis genes: 0 nonelicited, 30, 60, 150, and 360 min; for NaTPI: 0, 6, 12, 24, 48, and 72 h), immediately frozen in liquid nitrogen, and kept at –80°C until further processing. For each time point, one leaf was harvested from five different elicited plants. Total RNA was extracted using TRI reagent (Sigma). cDNA was synthesized from 20 ng of total RNA as described by Schmidt et al. (2005)
The following materials are available in the online version of this article.
We thank E. Wheeler for editorial comments, Prof. C. Kuhlemeier, Dr. K. Groten, Dr. T. Krügel, and T. Riedel for helpful discussions and assistance in the greenhouse experiments. Dr. K. Gase, T. Hahn, W. Kroeber, S. Allmann, S. Kutschbach, and A. Wissgott for invaluable technical assistance; A. Weber and A. Schünzel for growing the plants, and D. Kessler for maintaining the cultures of M. sexta. Received February 5, 2007; accepted March 27, 2007; published April 6, 2007.
1 This work was supported by the Max Planck Society. 
2 Present address: Institute for Plant Sciences, Agricultural Research Organization, 50250 Bet Dagan, Israel. 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: Ian T. Baldwin (baldwin{at}ice.mpg.de).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.097543 * Corresponding author; e-mail baldwin{at}ice.mpg.de; fax 49–3641–571102.
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