In light of the fact that plant pathogens drastically reduce growth in both agricultural and natural ecosystems worldwide, and that estimates of financial loss due to such reductions amount to more than $33 billion annually in the United States alone (Pimentel et al., 2000), it is natural to wonder -- and important to determine -- how plant-pathogen interactions will be impacted by the ongoing rise in the atmosphere's CO2 concentration. Several researchers have studied numerous aspects of this important subject; and this review examines what they have learned about these phenomena from experiments conducted on various types of trees.

Leaf spot disease, which is characterized by chlorotic to necrotic localized leaf lesions, is caused by the Cercospora (a large genus of ascomycete fungi) that affect, in the words of McElrone et al. (2010), "numerous economically important plant species around the world, including grapes, cereals, soybeans, peanuts, orchids, coffee, alfalfa and potatoes (Sinclair et al., 1987)," as well as redbud (Cercis canadensis) and sweetgum (Liquidambar styraciflua) trees, such as those growing at the Duke Forest Face Facility in Orange County, North Carolina (USA), where McElrone et al. studied the disease throughout the growing seasons of five different years (2000-2003 and 2005).

During this time, the six scientists assessed how elevated CO2 (to 200 ppm above the ambient air's CO2 concentration) and natural interannual climatic variability affected the incidence and severity of leaf spot disease among the sweetgum and redbud trees growing in the several FACE rings at the Duke Forest experimental site, while in order "to determine how photosynthetic capacity surrounding pathogen damage was affected by CO2 exposure, the spatial pattern of photosystem II operating efficiency was quantified on C. canadensis leaves still attached to plants with an imaging chlorophyll fluorometer."

Based on their analysis, McElrone et al. determined that "disease incidence and severity for both species were greater in years with above average rainfall," while "in years with above average temperatures, disease incidence for Liquidambar styraciflua was decreased significantly." On the other hand, they found that elevated CO2 increased disease incidence and severity "in some years." However, they say that the "chlorophyll fluorescence imaging of leaves revealed that any visible increase in disease severity induced by elevated CO2 was mitigated by higher photosynthetic efficiency in the remaining undamaged leaf tissue and in a halo surrounding lesions," indicating that although atmospheric CO2 enrichment was observed to sometimes increase the incidence and severity of leaf spot disease, the photosynthesis-enhancing effect of the extra CO2 was found to compensate for the photosynthetic productivity lost to the disease by enhancing productivity in healthy portions of diseased leaves and in leaves without lesions, for no net ill effect.

In another study, where it appears at first glance that pathogens might have the advantage at higher CO2, Fleischmann et al. (2010) grew well-watered European Beech (Fagus sylvatica L.) trees from seed for a period of four years within growth chambers that were maintained at either 400 or 700 ppm CO2 within a greenhouse. During this period, the trees received an adequate supply of all essential nutrients; but in the case of nitrogen (N), there were low N and high N treatments, where the high-N treatment received twice as much nitrogen as the low-N treatment. In addition, half of the seedlings were infected with Phytophthora citricola -- a root pathogen known to infest the roots and trunks of European Beech trees -- in the early summer of the third year of the study. Half of the trees in each treatment were then harvested and examined at the ends of the third and fourth years of the experiment.

In discussing their findings, the three German researchers report that "chronic elevation of atmospheric CO2 increased the susceptibility of beech seedlings towards the root pathogen P. citricola, while additional nitrogen supply reduced susceptibility." In fact, they found that 27% of the infected plants in the low-N high-CO2 treatment had been killed by the pathogen by the end of their study, while only 9% of the infected plants in the high-N high-CO2 treatment had died. In terms of the bigger picture, however, they found that surviving beech seedlings of the low-N high-CO2 treatment "managed to tolerate the root infection by (a) increasing their carbon gain, (b) improving their fine root functionality and (c) changing their allometric relation between below-ground and above-ground biomass."

As a result of the latter three phenomena, Fleischmann et al. were able to write that infected beech seedlings in the low-N high-CO2 treatment rose to the challenge presented by the pernicious pathogen and "enhanced [their] primary production rates in the second year of the experiment and increased above-ground biomass significantly as compared to control trees," thereby providing an exemplary illustration of the popular proverb that affirms that "whatever doesn't kill me makes me stronger."

In another multiple variable study, but using ozone (O3) instead of nitrogen, Percy et al. (2002) grew the most widely distributed North American tree species -- trembling aspen -- in twelve 30-m-diameter FACE rings near Rhinelander, Wisconsin, USA in air maintained at ambient CO2 and O3 concentrations, ambient O3 and elevated CO2 (560 ppm during daylight hours), ambient CO2 and elevated O3 (46.4-55.5 ppb during daylight hours), and elevated CO2 and O3 over the period of each growing season from 1998 through 2001. Throughout this experiment they assessed a number of the young trees' growth characteristics, as well as their responses to poplar leaf rust (Melampsora medusae), which they say "is common on aspen and belongs to the most widely occurring group of foliage diseases." Their work revealed that elevated CO2 alone did not alter rust occurrence, but that elevated O3 alone increased it by nearly fourfold. When applied together, however, elevated CO2 reduced the enhancement of rust development caused by elevated O3 from nearly fourfold to just over twofold.

Another study fueling optimism was conducted by Parsons et al. (2003), who grew two-year-old saplings of paper birch and three-year-old saplings of sugar maple in well-watered and fertilized pots from early May until late August in glasshouse rooms maintained at either 400 or 700 ppm CO2. In these circumstances, the whole-plant biomass of paper birch was increased by 55% in the CO2-enriched portions of the glasshouse, while that of sugar maple was increased by 30%. In addition, concentrations of condensed tannins were increased by 27% in the paper birch (but not the sugar maple) saplings grown in the CO2-enriched air; and in light of this finding, Parsons et al. conclude that "the higher condensed tannin concentrations that were present in the birch fine roots may offer these tissues greater protection against soil-borne pathogens and herbivores." Within this context, it is also interesting to note that Parsons et al. report that CO2-induced increases in fine root concentrations of total phenolics and condensed tannins have likewise been observed in warm temperate conifers by King et al. (1997), Entry et al. (1998), Gebauer et al. (1998) and Runion et al. (1999), as well as in cotton by Booker (2000). See also, in this regard, our reviews of Phenolics and Tannins.

In another more direct atmospheric CO2/plant pathogen analysis, McElrone et al. (2005) "assessed how elevated CO2 affects a foliar fungal pathogen, Phyllosticta minima, of Acer rubrum [red maple] growing in the understory at the Duke Forest free-air CO2 enrichment experiment in Durham, North Carolina, USA ... in the 6th, 7th, and 8th years of the CO2 exposure." Surveys conducted in those years, in their words, "revealed that elevated CO2 [to 200 ppm above ambient] significantly reduced disease incidence, with 22%, 27% and 8% fewer saplings and 14%, 4%, and 5% fewer leaves infected per plant in the three consecutive years, respectively." In addition, they report that the elevated CO2 "also significantly reduced disease severity in infected plants in all years (e.g. mean lesion area reduced 35%, 50%, and 10% in 2002, 2003, and 2004, respectively)."

With respect to discovering the underlying mechanism or mechanisms that produced these beneficent consequences, thinking it could have been a direct deleterious effect of elevated CO2 on the fungal pathogen, McElrone et al. performed some side experiments in controlled environment chambers. In doing so, however, they learned that the elevated CO2 benefited the fungal pathogen as well as the red maple saplings, observing that "exponential growth rates of P. minima were 17% greater under elevated CO2." And they obtained similar results when they repeated the in vitro growth analysis two additional times in different growth chambers.

Taking another tack when "scanning electron micrographs verified that conidia germ tubes of P. minima infect A. rubrum leaves by entering through the stomata," the researchers turned their attention to the pathogen's mode of entry into the saplings' foliage. In this investigation they found that both stomatal size and density were unaffected by atmospheric CO2 enrichment, but that "stomatal conductance was reduced by 21-36% under elevated CO2, providing smaller openings for infecting germ tubes." In addition, they concluded that reduced disease severity under elevated CO2 was also likely due to altered leaf chemistry, as elevated CO2 increased total leaf phenolic concentrations by 15% and tannin concentrations by 14%.

Because the phenomena they found to be important in reducing the amount and severity of fungal pathogen infection (leaf spot disease) of red maple have been demonstrated to be operative in most other plants as well, McElrone et al. say these CO2-enhanced leaf defensive mechanisms "may be prevalent in many plant pathosystems where the pathogen targets the stomata." Indeed, they state that their results "provide concrete evidence for a potentially generalizable mechanism to predict disease outcomes in other pathosystems under future climatic conditions." And because of their insightful work, that future is looking particularly bright in terms of the never-ending struggle between earth's plants and the pathogens that prey upon them. Although elevated CO2 helps both sides of the conflict, it helps plants more and in more ways.

In one final study, Runion et al. (2010) write as a prelude to their work that obligate pathogens "have a more intimate relationship with their host and must have the host to survive," whereas facultative pathogens "live saprophytically and generally result in disease (or tend to be more severe) under conditions of plant stress such as low nutrition or water."

Against this backdrop, the authors grew well watered and fertilized seedlings of loblolly pine (Pinus taeda) and northern red oak (Quercus rubra) out-of-doors in open-top chambers constructed within large soil bins located at the USDA-ARS National Soil Dynamics Laboratory in Auburn, Alabama (USA), where they were exposed to atmospheric CO2 concentrations of either 360 or 720 ppm with or without being infected by the fusiform rust fungus (the obligate pathogen Cronartium quercuum f.sp. fusiforme), and where the pines were also grown with or without being infected by the pitch canker fungus (the facultative pathogen Fusarium circinatum) for various lengths of time that ranged from weeks to a full year, with each of the three experiments being conducted twice.

With respect to the pine Fusarium rust study, Runion et al. report that "percent infection was not significantly affected by CO2 concentration," but that in spite of this fact "the percentage of loblolly pine seedlings which died as a result of rust infection was generally significantly lower under elevated CO2 in both runs of the experiment." With respect to the oak Fusarium rust study, they say "the percent of oak seedlings with uredia was consistently lower for seedlings exposed to elevated CO2 in both runs," and that "the percent of oak seedlings with telia was significantly lower for seedlings exposed to elevated CO2 at the 16 and 19 days evaluations in both runs of the experiment." Last of all, with respect to the pine pitch canker study, the four researchers indicate that "the percent of loblolly pine seedlings which developed cankers following inoculation with the pitch canker fungus was consistently lower for seedlings grown under elevated CO2 in both runs of the experiment ... with infection in elevated CO2-grown seedlings remaining about half that of ambient-grown seedlings."

Given such findings, Runion et al. state that "disease incidence -- regardless of pathogen type -- may be reduced as atmospheric CO2 concentration continues to rise," which phenomenon should significantly benefit the two species of trees in the high-CO2 world of the future.

In conclusion, the balance of evidence obtained to date demonstrates an enhanced ability of trees to withstand pathogen attacks in CO2-enriched as opposed to ambient-CO2 air. And as a result, in the years, decades and centuries to come, Earth's vegetation should fare ever better in its eternal battle to better withstand the ravages that have historically been inflicted upon it by a myriad of debilitating plant diseases, as the atmosphere's CO2 concentration continues to rise ever higher.

References
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Entry, J.A., Runion, G.B., Prior, S.A., Mitchell, R.J. and Rogers, H.H. 1998. Influence of CO2 enrichment and nitrogen fertilization on tissue chemistry and carbon allocation in longleaf pine seedlings. Plant and Soil 200: 3-11.

Fleischmann, F., Raidl, S. and Osswald, W.F. 2010. Changes in susceptibility of beech (Fagus sylvatica) seedlings towards Phytophthora citricola under the influence of elevated atmospheric CO2 and nitrogen fertilization. Environmental Pollution 158: 1051-1060.

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