Carbon-based Secondary Compounds Research Articles

Carbon-based secondary and structural compounds in Mediterranean shrubs growing near a natural CO2 spring

We studied carbon-based secondary and structural compounds (CBSSCs) in Myrtus communis, Erica arborea, and Juniperus communis co-occurring in a natural CO2 spring site and in a nearby control site in a Mediterranean environment. Leaf concentrations of phenolics and CBSSCs, such as lignin, cellulose, and hemicellulose, total nonstructural carbohydrates (TNCs), and lipids were measured monthly (phenolics) and every two months (the other compounds) throughout a year. There was a slight seasonal trend towards maximum concentrations of most of these CBSSCs during autumn–winter and minimum values during the spring season, particularly in Myrtus communis. For most of the CBSSCs and species, there were no consistent or significant patterns in response to the elevated [CO2] (c. 700 μmol mol−1) of the spring site. These results were not due to a dilution effect by increased structural or nonstructural carbon. Therefore, in contrast to many experimental studies of CO2 enrichment, mainly conducted for short periods, there were no greater concentrations of phenolics, and, as in many of these studies, there were neither greater concentrations of the other CBSSCs. These results do not agree with the predictions of the carbon source-sink hypotheses. Possible causes of this disagreement are discussed. These causes include the complex heterogeneous environmental conditions and the variability of resource availabilities in the field, photosynthetic down-regulation, and/or the homeostatic and evolutionary nature of organisms. These results suggest evolutionary adaptive responses to changes in CO2. They also suggest caution in attributing increased CBSSC concentrations to elevated [CO2] at long-term scale in natural conditions, and therefore in their implications for plant–herbivore interactions and for decomposition.

Regulation of Woody Plant Secondary Metabolism by Resource Availability: Hypothesis Testing by Means of Meta-Analysis

Our aim in this study was to determine how well phenotypic variation in foliar concentrations of carbon-based secondary compounds (CBSCs) in woody plants can be predicted on the basis of two resource-based hypotheses, i.e. the carbon-nutrient balance (CNB) and growth-differentiation balance (GDB) hypotheses. We conducted a meta-analysis of literature data with respect to responses of CBSCs, carbohydrates and nitrogen to six types of environmental manipulations (fertilization with nitrogen or phosphorus, shading, CO 2 enrichment, drought stress, ozone exposure). Plant responses to nitrogen fertilization, shading and CO 2 enrichment in terms of pooled CBSCs and carbohydrates were consistent with predictions made with the two hypotheses. However, among biosynthetically distinct groups of CBSCs only concentrations of phenylpropanoid-derived compounds changed as predicted; hydrolyzable tannins and terpenoids, in particular, were less responsive. Phosphorus fertilization did not affect concentrations of CBSC or primary metabolites. Plant responses to drought and ozone exposure presumably were driven by plant demands for particular types of compounds (osmolites in the case of drought and antioxidants in the case of ozone exposure) rather than by changes in resource availability. Based on the relative importance of the treatment effects, we propose a hierarchical model of carbon allocation to CBSCs. The model implies that CBSC production is determined by both resource availability and specific demand-side responses. However, these two mechanisms work at different hierarchical levels. The domain of the CNB and GDB hypotheses is at the high hierarchical levels, predicting the total amount of carbon that can be allocated to CBSCs. Predicting altered concentrations of individual CBSCs, i.e. low hierarchy levels, probably demands biosynthetically detailed models which also take into account the history of plant interactions with biotic and abiotic factors.

Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization?

We propose that variation in the responses of carbon-based secondary compounds to fertilization in woody plants has a biosynthetic cause. The synthesis of phenylpropanoids and derived compounds (e.g., condensed tannins) competes directly with the synthesis of proteins, and therefore with plant growth, because of a common precursor, phenylalanine. In contrast, the biosynthesis of terpenoids and of hydrolyzable tannins proceeds presumably without direct competition with protein synthesis. Therefore, accelerated plant growth induced by fertilization may cause a reduction in concentrations of phenylpropanoids but may affect less or not at all the levels of other classes of secondary compounds. A meta-analysis based on fertilization experiments with 35 woody plant species supported the predicted differences fertilizing significantly decreased concentrations of phenylpropanoids but not of terpenoids or hydrolyzable tannins.

Can elevated CO 2 affect secondary metabolism and ecosystem function?

It has generally been assumed that increasing atmospheric CO 2 concentrations will increase plant carbon-based secondary or structural compounds concentrations. These changes may have far-reaching consequences for herbivory and plant litter decomposition. Recent experimental results provide evidence of increases in concentrations of soluble phenolics and condensed tannins but not in lignin, structural polysaccharides or terpenes. They also show significant effects of these plant chemical changes on herbivores and little or any effects on decomposition. However, there is no consistent evidence of any of these effects at the complex long-term ecosystem level.

The effect of elevated CO2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda).

We examined the extent to which carbon investment into secondary compounds in loblolly pine (Pinus taeda L.) is changed by the interactive effect of elevated CO2 and N availability and whether differences among treatments are the result of size-dependent changes. Seedlings were grown for 138 days at two CO2 partial pressures (35 and 70 Pa CO2) and four N solution concentrations (0.5, 1.5, 3.5, and 6.5 mmol l-1 NO3NH4) and concentrations of total phenolics and condensed tannins were determined four times during plant development in primary and fascicular needles, stems and lateral and tap roots. Concentrations of total phenolics in lateral roots and condensed tannins in tap roots were relatively high regardless of treatment. In the smallest seedlings secondary compound concentrations were relatively high and decreased in the initial growth phase. Thereafter condensed tannins accumulated strongly during plant maturation in all plant parts except in lateral roots, where concentrations did not change. Concentrations of total phenolics continued to decrease in lateral roots while they remained constant in all other plant parts. At the final harvest plants grown at elevated CO2 or low N availability showed increased concentrations of condensed tannins in aboveground parts. The CO2 effect, however, disappeared when size differences were adjusted for, indicating that CO2 only indirectly affected concentrations of condensed tannins through accelerating growth. Concentrations of total phenolics increased directly in response to low N availability and elevated CO2 in primary and fascicular needles and in lateral roots, which is consistent with predictions of the carbon-nutrient balance (CNB) hypothesis. The CNB hypothesis is also supported by the strong positive correlations between soluble sugar and total phenolics and between starch and condensed tannins. The results suggest that predictions of the CNB hypothesis could be improved if developmentally induced changes of secondary compounds were included.

Species-Specific Response of Glucosinolate Content to Elevated Atmospheric CO2

The carbon/nutrient balance hypothesis has recently been interpreted to predict that plants grown under elevated CO2 environments will allocate excess carbon to defense, resulting in an increase in carbon-based secondary compounds. A related prediction is that, because plant growth will be increasingly nitrogen-limited under elevated CO2 environments, plants will allocate less nitrogen to defense, resulting in decreased levels of nitrogen-containing secondary compounds. We present the first evidence of decreased investment in nitrogen-containing secondary compounds for a plant grown under elevated CO2. We also present evidence that plant response is species-specific and is not correlated with changes in leaf nitrogen content or leaf carbon–nitrogen ratio. When three crucifers were grown at 724 ± 8 ppm CO2, total foliar glucosinolate content decreased significantly for mustard, but not for radish or turnip. Glucosinolate content of the second and fourth youngest mustard leaves decreased by 45% and 31%, respectively. In contrast, no significant change in total glucosinolate content was observed in turnip or radish leaves, despite significant decreases in leaf nitrogen content. Total glucosinolate content differed significantly among leaves of different age; however, the trend differed among species. For both mustard and turnip, glucosinolate content was significantly higher in older leaves, while the opposite was true for radish. No significant CO2 × leaf age interaction was observed, suggesting that intraplant patterns of allocation to defense will not change for these species. Changes in nitrogen allocation strategy are likely to be species-specific as plants experience increasing atmospheric CO2 levels. The ecological consequences of CO2-induced changes in plant defensive investment remain to be investigated.

Chronic Defoliation Impacts Pine Sawfly (Hymenoptera: Diprionidae) Performance and Host Plant Quality

We assessed the effects of chronic defoliation on host plant quality and larval performance of a pine sawfly. Neodiprion autumnalis larvae were reared on ponderosa pine (Pinus ponderosa) that had experienced moderate to severe defoliation (>50%) of mature foliage for at least 15 yr and on trees sustaining no observable defoliation during the same time interval. N. autumnalis performance was 23% (total instar survival) to 12% (potential fecundity) higher on chronically defoliated trees compared with non-defoliated trees. Perennially attacked trees had reduced dry matter (an estimate of total carbon) content of mature needles, higher foliar nitrogen, and a 10% lower carbon/nitrogen balance compared with non-defoliated trees. No differences were detected in foliar toughness. Based on these findings, we maintain that chronic defoliation of evergreen conifers reduces the production of carbon-based secondary compounds in foliage and increases plant nutrition resulting in a positive feedback loop.

Carbon-based Secondary Compounds at Elevated CO<sub>2</sub>

From literature sources we compiled the data on carbon-based-secondary compounds CBSC (phenolics and terpenoids) and biomass of 17 plant species grown at different CO2 concentrations under low and high nutrient availabilities. With a low nutrient availability a possible inverse correlation was found between the biomass and CBSC changes. On the contrary, under a high nutrient availability, both the CBSC and biomass increased with elevated CO2. The wide variation in the CBSC production among species and compounds (larger responses in phenolics than in terpenoids) indicates that the allocation to CBSC may not completely be governed by changes in CO2 and nutrient availabilities per se. Yet the comparison shows that elevated CO2 generally loads the carbon into CBSC [their leaf concentration increased an overall average of 14 % at 700 umol(CO2) mol-r] which may improve our understanding of the carbon storage and cycling in ecosystems under the "global change" of climate.

Antiherbivore Defenses of Myrmecophytic Cecropia under Different Light Regimes

In a greenhouse experiment, we compared presumed biotic, chemical, physical and phenological defenses of six myrmecophytic Peruvian Cecropia species under high and low light regimes. For all species, increased light intensity enhanced both dry mass production of glycogen-rich Millerian bodies (MBs) and levels of condensed tannins and total phenolics. The production of lipid-rich pearl bodies (PBs), the leaf toughness, and the expansion rate of new leaves were not enhanced consistently by higher light intensity. The six species were comprised of three pairs of close congeners; each pair consisted of a of riverine and stream edges or land-slips, and a species from treefall openings in primary forest. Each gap species grew more slowly than did its pioneer counterpart and allocated proportionally more resources to MBs. Gap species produced a greater dry mass of MBs per unit of leaf area, and initiated their production earlier in seedling ontogeny. In comparison with pioneer relatives, gap species also possessed somewhat longer-lived and tougher leaves. Both PB production and leaf expansion rates were greater in pioneers than in closely related gap species. Disparities in the behaviors of MBs and PBs in interspecific comparisons probably reflect differences in the initial construction costs versus continuing or maintenance costs of these two types of ant rewards. Interspecific differences in the production of carbon-based secondary compounds by pioneers and gap species are pair specific and appear to be related to the degree of morphological differentiation within pairs, and, possibly, to time since divergence. We relate our results to current theories of plant defense.