Vol.1, No.3, 57-62 (2011) http://dx.doi.org/10.4236/oje.2011.13007 Open Journal of Ecology C opyright © 2011 SciRes. OPEN ACCESS Rhizobium alters inducible defenses in broad bean, Vicia faba Misty Cree Summers, Edward Brian Mondor* Department of Biology, Georgia Southern University, Statesboro, USA; *Corresponding Author: emondor@georgiasouthern.edu Received 18 September 2011; revised 16 October 2011; accepted 28 October 2011. ABSTRACT Conversion of inorganic nitrogen by mutualistic nitrogen-fixing bacteria is essential for plant growth and reproduction, as well as the devel- opment of chemical and mechanical defenses. It is unclear, however, how these bacteria alter co- occurring symbioses at higher trophic levels; e.g., extrafloral nectary (EFN) induction, in re- sponse to herbivory, to attract defensive mutu- alist s. We hypothesized that plants colonized by nitrogen-fixing bacteria would mount a larger inducible, defensive response than plants lack- ing symbioses, as defensive traits are costly. We predicted that bean plants, Vicia faba L., harboring Rhizobium leguminosarum bv. viciae Frank would produce more EFNs upon leaf damage, than plants lacking the symbionts, as EFN induction in V. faba is resource-dependent. Here we report that V. faba colonized by R. leguminosarum produced similar numbers of EFNs as did plants without symbionts. Plants with symbionts, however, produced signifi- cantly fewer EFNs over 1 week in response to leaf damage, than those without leaf damage. As such, nitrogen-fixing bacteria may not al- ways benefit the host plant, but rather, the utility of these bacteria may be dependent on the prevailing ecological conditions. Keyw ords: Extrafloral Nectary; Inducible Defense; Mutualism; Phenotypic Plasticity; Rhizobia 1. INTRODUCTION Nitrogen-fixing bacteria—host plant mutualisms have been studied for decades [1,2]. Fixed nitrogen, the con- version of atmospheric nitrogen to ammonium in plant root nodules, is used for plant growth and reproduction as well as chemical defenses [3,4]. Despite their ubiquity, these symbioses are very host specific; only certain spe- cies or strains of bacteria can colonize host plants [5,6]. Broad bean, Vicia faba L., roots are one of the most dis- criminating mutualists, being colonized only by Rhi- zobium leguminosarum bv. viciae Frank [5,7,8]. This nitrogen-fixing bacteria increases plant size, vigor, and seed set [9]. Whether this symbiont alters broad bean ecological interactions with higher trophic levels, throu- gh altered defensive capab ilities, however, is unknown. Defensive mutualisms between plants and predatory arthropods are common. Over 93 plant families produce sugar-producing structures, called extrafloral nectaries (EFNs) [10], which are highly attractive to predatory ants [11,12]. Plants increasing nectar secretion rates generally attract more ants, have lower rates of herbivory, and increased survivorship [12-15]. Increased nectar production may also be inducible depending upon environmental conditions [13,16]. In broad bean, EFNs are located on the stipules at the base of each leaf petiole [17,18]. Attractive to ants [18,19], broad bean plants increase EFN numbers when herbivory increases [17, 20]. As broad bean EFNs are visually conspicuous it may be adaptive to produce a more striking visual dis- play rather than to augment nectar from existing nec- taries [17]. The induction of extrafloral nectar [13,16,21] and nectaries [17,20,22] are believed to be costly as, in se- veral cases, these responses are resource dependent [14, 20]. Resultantly, many plants have evolved phenoty- pically plastic responses to augment these defensive traits only when risk of herbivory increases [23,24]. As nitrogen-fixing bacteria provide plants with additional nitrogen, broad bean plants with rhizobia may have the ability to produce additional defensive structures (e.g., EFNs) in response to leaf damage. As defensive traits have frequently been shown to be costly, we hypothesized that plants with nutritional sym- bionts would produce a larger inducible response than plants lacking nutritional symbionts. More specifically, we predicted that broad bean plants, V. f a b a , harboring the nitrogen-fixing bacteria, R. leguminosarum bv. viciae,
M. C. Summers et al. / Open Journal of Ecology 1 (2011) 57-62 Copyright © 2011 SciRes. OPEN ACCESS 58 would produce more EFNs in response to leaf damage, than plants lacking these mutualists. 2. MATERIALS AND METHODS 2.1. Experiment To carry out this study broad bean seeds were spr- outed in deionized water. Water was changed every 24 hours, for 5 days. After 5 days, sprouted beans (n = 60) were used for the experiment. Thirty sprouts were each inoculated with 1g of Royal Peat Inoculant; containing 2 × 108 viable cells of R. leguminosarum bv. viciae per gram (Becker Underwood, Ames, Iowa 50010). We chose to use a commercially available inoculant, con- taining R. leguminosarum bv. viciae, so that others could easily repeat our experimental protocol. Each seed was dipped into deionized water and coated with inoculant. The remainder of the 1g of inoculant was sprinkled on the soil directly under the sprout. The remaining 30 sprouts were each dipped in water but not inoculated prior to planting. Sprouted seeds were planted in Sta- Green All-Purpose Potting Mix (NPK 0.14:0.11:0.08; Spectrum Brands, A tlanta, GA 3 0328) in 1L pots (ITML Horticultural Products, Brantford, ON Canada N3T 5M8). Unsterilized soil was used for this experiment so as not to kill any beneficial microbes in the soil, which could alter the experimental results. Plants were grown under greenhouse conditions (32˚C - 41˚C, 27% - 95% rh, natural lighting) in a computer-generated random order (JMP 5.1) [25]. Treatments were randomized using a random number generator (JMP 5.1) [25]. Pots were then labeled with the experimental treatments: RD (Rhizobium , leaf dam- age; n = 15), RND (Rhizobium, no leaf damage; n = 15), NRD (no Rhizobium, leaf damage; n = 15) and NRND (no Rhizobium, no leaf damage; n = 15). Plants were wa- tered every second day. Once plants reached a height of approximately 10cm, they were staked to help the plant grow upright. After the fourth week, when plants were approximately 60 cm tall (mean = 56 ± 9 cm), initial pl- ant traits were recorded and treatments were conduc- ted. We recorded the plant traits: plant height, number of fully expanded leaves, number of partially expanded lea- ves, and number of EFNs. While each broad bean leaf pair generally has 0 or 2 EFNs on the associated stipules, broad beans can alter the total number of EFNs on a pl- ant by clustering the stipules, and hence the EFNs, on the apical meristem prior to the leaves unfolding [20]. After recording these traits, leaf damage treatments were administered to the appropriate plants. For replicates with leaf damage, the outer one-third of each of the pl- ants fully and partially ex panded leaf pairs were excised using floral scissors. To ensure that compounds were not transferred between plants, the scissors were cleaned with an alcohol swab after excising tissue from each plant. After allowing the plants to grow for 1 additional we- ek, plant traits were again recorded. A few plants, dis- tributed across treatments, broke before final traits could be assessed; these plants were not included in any ana- lyses. We calculated the degree of change in all of the traits by subtracting the initial trait values from the final trait values. We also destructively sampled the plants to assess: total numbers of root nodules, total root nodule weight, shoot dry weight, and root dry weight (minus nodules). Once to tal nodule numbers were recorded, no- dules were excised from the root, placed in aluminum weighing dishes, and placed in a drying oven (55˚C ± 2˚C) for 2 weeks. Roots and shoots were placed in sepa- rate brown paper bags and dried similarly. Root nodule, shoot, and root weights were determined using a micro- balance (ExplorerPro, Ohaus Corporation, Pine Brook, NJ 07058). 2.2. Statistical Analyses For a robust statistical analysis we conducted similar two-factor ANCOVAs, pre- and post-leaf damage treat- ments. By conducting similar analyses we could confirm that significant differences did not exist in the treatment groups prior to leaf damage. Independent variables in both analyses were: Rhizobium (no vs. yes), leaf damage (no vs. yes), and the first-order interaction Rhizobium × leaf damage. Covariates in the pre-treatment model were: number of partially expanded leaves and number of fully expanded leaves. Covariates in the post-treatment model were: change in th e number of partially expanded leaves and change in the number of fully expanded leaves, over 1 week. The dependent variables were: the number of EFNs per plant (pre-treatment model) or change in num- ber of EFNs over 1 week (post-treatment model). To more accurately quantify the effects of rhizobia on EFN induction we conducted two multiple regression analyses exclusively on the Rhizobium treatment group (i.e., there were almost no root nodules on plants in the “no Rhizobium” group). In the first regression, the in- dependent variables were: leaf damage (no vs. yes), change in the number of partially expanded leaves over 1 week, change in the number of fully expanded leaves over 1 week, and total number of root nodules. In the second regression, total weight of root nodules was in- corporated as a variable, instead of root nodule number. For both multiple regressions the dependent variable was the change in number of EFNs over 1 week. To better understand the effects of rhizobia on overall plant growth, we conducted 2, two-way ANOVAs. Inde-
M. C. Summers et al. / Open Journal of Ecology 1 (2011) 57-62 Copyright © 2011 SciRes. OPEN ACCESS 5959 pendent variables in the analyses were : Rhizobium (no vs. yes), leaf damage (no vs. yes), and the first-order inter- action Rhizobiu m × leaf damage. Dependent variables were: shoot dry weight, and root dry weight (minus no- dules). All data was analyzed using JMP 5.1 [25]. Post-hoc treatment effects were determined with Tukey’s Hon-es- tly Significant Difference (HSD) test. 3. RESULTS Prior to leaf damage, there was no difference in the number of EFNs on inoculated vs. uninoculated plants. There was also no effect of leaf damage, or any inter- action between our main variables, showing that we did not have an apriori differences in our treatment groups, prior to leaf excision treatments (Table 1). There were however, positive relatio nships between numbers of par- tially expanded leaves and fully expanded leaves with EFN numbers (Table 1). As EFNs are located on the leaf stipules, a high correlation between leaf pairs and EFN numbers is not unexpected. Post-leaf damage, colonization with mutualistic nitro- gen-fixing bacteria did alter EFN numbers in broad bean plants. Overall, inoculated plants did not produce more EFNs over 1 week compared to uninoculated plants (Ta- ble 1). Plants also did not produce more EFNs in res- ponse to leaf damage (Ta ble 1). There was, however, a significant interaction between Rhizobium and leaf da- mage (Table 1; Figure 1). Plants without nitrogen- fixing bacteria produced approximately the same number of EFNs whether or not they suffered leaf damage. Con- trary to our hypothesis, however, plants with Rhizobi- um produced fewer EFNs after experiencing leaf da- mage, compared to inoculated plants without leaf da- mage (Figure 1). Like in pre-treatment plants, there was a significant relationship between numbers of partially Table 1. Effects of Rhizobia and (or) leaf damage on the num- bers of extrafloral nectaries, in broad bean, before and after leaf excision. Pre-treatment Post-treatment Variable F P F P Rhizobia (df = 1, 41) 0.010 0.92 0.0130.91 Leaf damage (df = 1, 41) 0.30 0.59 0.201 0.66 Rhizobia × Leaf damage (df = 1, 41) 1.56 0.22 5.60 0.023 *Partially developed leaf pairs (df = 1, 41) 8.03 0.0071 7.080.011 *Fully developed leaf pairs (df = 1, 41) 7.96 0.0073 2.020.16 *Post-treatment analyses used the “change in partially developed leaf pairs” over 7 days, following leaf damage treatments (see text for further detai ls ). Figure 1. Extrafloral nectaries produced by inoculated vs. uninoculated broad bean, Vicia faba, plants over 7 days when given mechanical leaf damage. Rhizobia × leaf damage inter- action; F1,41 = 5.41, P = 0.025. Data are presented as Least Squared Means. Columns with different letters are significantly different; Tukey’s HSD (P < 0.05). expanded leaves and EFN numbers. Unlike the pre- treatment analysis, however, the relationship dissipated between numbers of fully expanded leaves and EFN numbers (Table 1). Looking more closely at the Rhizobium plants, there was a trend towards th e total number of root nodu les, bu t not total weight of nodules, influencing EFN production. In the first regression analysis, total number of root nodules was marginally non-sign ificant (F1,21 = 3.31, P = 0.083; Figure 2) in being inversely related to EFN pro- duction after factoring out the effects of leaf damage (F1,21 = 6.47 , P = 0.019), change in partially expanded leaf pairs (F1,21 = 1.99, P = 0.17), and fu lly expanded leaf pairs (F1,21 = 0.31, P = 0.59). The second regression analysis showed that the total weight of root nodules was not significantly related to EFN production (F1,21 = 1.94, P = 0.18) even when accounting for leaf damage (F1,21 = Figure 2. The effect of Rhizobium leguminosarum cv. viceae colonization on EFN production in broad bean plants. There was a trend towards reduced EFN induction responses as root colonization rates increased (t1,21 = –1.82, P = 0.083).
M. C. Summers et al. / Open Journal of Ecology 1 (2011) 57-62 Copyright © 2011 SciRes. OPEN ACCESS 60 4.87, P = 0.039), chang e in par tially expanded leaf pairs (F1,21 = 2.59 , P = 0.12), and fully expanded leaf pairs (F1,21 = 0.51, P = 0.48). In regards to overall plant growth, dry shoot biomass was not significantly altered by rhizobia colonization (mean ± 1se; no rhizobia, 1.13 ± 0.04; rhizobia, 1.13 ± 0.04: F1,44 = 0.0060, P = 0.94). There were lower shoot weights in plants that experienced leaf damage (mean ± 1se; no damage, 1.19g ± 0.04; damage, 1.07g ± 0.04: F1,44 = 3.98 , P = 0.052), as leaf tissu e had been removed from these plants. There was no significant interaction between rhizobia and leaf damage on dry shoot weights (F1,44 = 0.0113, P = 0.92). Dry root weights were sig- nificantly lower when colon ized b y rhizob ia (mean ± 1se; no rhizobia, 0.57 ± 0.04; rhizobia, 0.47 ± 0.03: F1,44 = 4.42, P = 0.041), but there was no effect of leaf damage on shoot weights (no damage, 0.55g ± 0.04; damage, 0.49g ± 0.04: F1,44 = 1.50 , P = 0.23), and there was no interaction between these main variab les (F 1,44 = 0.0058 , P = 0.94). 4. DISCUSSION Despite their ubiquity, nitrogen-fixing bacteria – host plant mutualisms are exceedingly specific interactions [26-29]. Vicia faba, for example, is one of the most discriminating of the legume hosts towards different strains of R. leguminosarum [5]. Adding additional complexity, symbioses are frequently nested within each other [30], thus changes in one mutualism may indirectly alter the functioning of other mutualisms. Here we showed that the presence of nitrogen-fixing bacteria directly altered the induction of EFNs in broad bean plants. The direction of this response, however, ran counter to our hypothesis and prediction; plants with rhizobia produced fewer EFNs when damaged. Without rhizobia, plants did not produce more EFNs when damaged, compared to those that were undamaged. This might seem contrary to prior experiments, where damaged plants produce more EFNs compared to unda- maged plants [17,20,22]. It must be noted, however, that EFN induction has also been shown to be resource dependent [20]. It is likely that the plants in our experi- ments, grown in soil with extremely low fertilizer levels (NPK 0.14:0.11:0.08), did not have the resources to produce additional EFNs when herbivory increased. Ex- trafloral nectary [20] and food body induction [14] are both influenced by nu trient availability. Overall, plants with rhizobia did not produce more EFNs than did plants without nitrogen fixing bacteria. Plants experiencing leaf damage, however, actually had decreased EFN numbers compared to undamaged plants. Furthermore, there were indications that the number of EFNs decreased as root nodule numbers increased. In the rhizobia—plant mutualism, symbiotic bacteria con- sume plant photosynthate in exchange for increased ni- trogen availability [31,32]. A negative relationship bet- ween EFN induction and total number of root nodules indicates a possible tradeoff in resource allocation bet- ween symbiont nutrition and host plant defense [33]. As plants have only a finite photosynthetic capability, the development of rhizobial colonies may come at the ex- pense of EFN induction. Such tradeoffs may be common between plants and their mutualistic partners, especially under relatively nutrient-poor conditions [33]. So why did damaged plants with rhizobia produce significantly fewer EFNs than undamaged plants with rhizobia? We advance several, non-mutually exclusive hypotheses to explain these enigmatic results. First, rhi- zobia may have contributed to alternate forms of defense, e.g., increased production of phenolics [3,4]. Upon leaf damage, it is possible that broad bean plants increase secondary compound production at the expense of other forms of defense (e.g., EFN production). Second, rhi- zobia may enable plants to produce additional EFNs, but reduced leaf tissue resulting from leaf damage may have prevented increased expression due to reduced photo- synthetic capacities [34]. Third, as all plan ts were grown in a common greenhouse environment, it is possible that plants received volatile compounds from damaged cons- pecifics [35,36]. These compounds may have induced EFN formation in the undamaged rhizobial plants, as EFN induction is resource dependent [20]. More resear- ch needs to be conducted to determine the mechanism underlying this induction, and lack thereof. Plants may respond very differently when inoculated with different rhizobia strains [5,6,28]. A more effective symbiosis might promote EFN induction, even under adverse circumstances (i.e., when herbivory is intense). Conversely, ineffective symbioses may lead to decreased or nearly non-existent nitrogen fixation , leading to a pos- sible parasitic relationship between the two parties [37, 38]; but see [39] for an alternate viewpoint]. For ex- ample, bacteria are not needed if nutrient rich soil is al- ready providing the necessary components for plant growth. Under this scenario, rhizobia do not carry out nitrogen fixation, but form small, ineffective nodules [1]. While a very different mutualism, it is important to note that arbuscular mycorrhizal fungi also significantly decreased EFN numbers in V. faba, even when plant growth increased [40]. Unlike nitrogen-fixing bacteria, mycorrhizal fungi promote phosphorous uptake, in the absence of other phosphorous sources, leading to aug- mented plant growth [41,42]. As damaged broad bean plants increase EFN numbers when sup plemented with a balanced fertilizer [20], it is uncertain which element promotes EFN induction. While many questions remain to be answered about
M. C. Summers et al. / Open Journal of Ecology 1 (2011) 57-62 Copyright © 2011 SciRes. OPEN ACCESS 6161 the nitrogen-fixing bacteria—host plant mutualism, it is clear that rhizobia alter EFN induction responses in damaged broad bean, V. faba, plants. Thus, belowground mutualisms have the potential to alter aboveground symbioses [43,44]. Corroborating other studies, nitro- gen-fixing bacteria colonizing the roots of host plants may span the c ontinu u m from mutuali stic to parasitic [4 5- 48], depending on current ecological conditions, resulting in altered trophic functi oning. 5. ACKNOWLEDGEMENTS Authors thank M. Heil and M. Tremblay for insightful discussions on this topic. Laboratory assistance was provided by T. Brew. Funding for this project was provided by Georgia Southern University. REFERENCES [1] Chen, H.K. and Thornton, H.G. (1940) The structure of “ineffective” nodules and its influence on nitrogen fixa- tion. 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